saccade, fixation, visual attention, salience, latency, model, competitive interaction, reciprocal inhibition, spatial selection, search selection
During active vision, the eyes continually scan the visual environment using saccadic scanning movements. This article presents a model for the human saccadic system. The model is described in terms of information processing and control with some close parallels to established physiological processes in the oculomotor system. The structure of the model consists of two separate pathways concerned respectively with the spatial and the temporal programming of the movement. A key aspect of the second pathway is the involvement of spatially distributed coding and the selection of the saccade target from a ‘salience map’. The two pathways descend through a hierarchy of levels, the lower levels operating automatically. An important feature is that visual onsets have automatic access to the eye control system via the lower levels. At various levels, centres in each pathway are interconnected via reciprocal inhibition. The model is used to account for a number of well-established phenomena observed in the study of target elicited saccades, notably: the gap effect, express saccades, the remote distractor effect and the global effect. High-level control of the pathways is discussed in relation to tasks such as visual search and reading. It is suggested that high level control operates through the two processes of spatial selection and search selection, which will generally combine in an automated way. Finally, some data from patients with unilateral neglect are examined in connection with the model.
Active human visual behaviour is dependent on saccadic eye movements, or saccades, rapid jerk like movements of the eyes that direct the gaze to a new location and redeploy the region of high visual acuity centred on the fovea. These movements are made several times each second during active scanning. They are ballistic movements in the sense that their duration is too short for new visual information to be used during their trajectory. Saccades are regarded as voluntary movements but are generally produced with highly automated routines. They are used in a great variety of ways in human behaviour. Saccades are used in the process of obtaining information about the visual environment and seeking new sources of stimulation. Saccades are used when searching visually for a particular target. Saccades are used in ordered scanning, such as human text reading. Finally, saccades are used to orient to salient new events in the visual field. Such orienting saccades have a reflex like quality and much of our knowledge about the saccadic system comes from study of the stimulus elicited saccade in which a subject is asked to make a saccadic orienting response to a new target appearing in the visual field.
This target article presents a framework for understanding human saccadic eye movement generation. We emphasise parallel processing of command signals for the movement and also processes of conflict resolution by competitive inhibition, which occur at various levels. We believe that conflict resolution is the important time consuming process even for simple orienting responses. Experimental studies on saccadic eye movements have generated a considerable body of data. In the case of eye movements elicited by specific visual targets, the significant measures are the metrics of the saccade (direction and amplitude) and the latency, that is the time from target appearance to the initiation of the movement. These measures provide a full specification of the movement since saccade trajectory and dynamics are generally constant for movements with a specified metric. We discuss the programming of both measures in the paper. Our framework is able to account for a number of robust effects which have been observed in research studies with stimulus elicited saccades, among them the gap effect, express saccades, the remote distractor effect, and the global effect. Although the main focus of our interest is on processes that operate in a stereotyped automatic fashion, we also indicate how the framework is ‘upward-compatible’ to allow more cognitive influences to be incorporated.
We present the framework in Section 2 in the form of an information flow model. We shall frequently refer to the framework as a ‘model’ in what follows although we appreciate that it does not at present satisfy the formal requirements of a quantitatively testable model. Section 3 discusses how the framework relates to existing work. In Section 4 we show how existing data can be interpreted and indicate a number of instances where the approach makes different predictions to those of other existing models.
The framework is described in functional terms, but has been considerably influenced by work in oculomotor neurophysiology. Possible correspondences are discussed, particularly in sect. 3.2. Our framework describes information and control flow in a conceptual neural network. However, we are interested in performance rather than learning so although we recognise that such a network has a capacity for learning, we are not concerned here with this plasticity and the important adaptational processes operative in connection with saccades (Deubel, 1987, 1995). Neither do we explore the converse problem of how the visual system takes account of changes produced by saccadic eye movements. New perspectives on this traditional theme have recently emerged (e.g. Bridgeman et al. 1994). Another limitation is that we shall ignore the third, depth, dimension of the visual world and retain the traditional account of saccades as conjugate eye movements. This must be recognised as only an approximation (Enright, 1984, 1992; Erkelens et al. 1989).
We hope that our proposal will be of interest to a broad spectrum of neuroscientists and cognitive scientists, including oculomotor physiologists, workers interested in visual cognition and workers in clinical areas who are attracted by the simplicity and elegance of eye movement control for investigative and diagnostic purposes.
The model is shown in diagrammatic form in Figure 1 which shows two parallel information and command streams running vertically through a hierarchy of processing levels. Information in the right hand (WHERE) stream is transmitted in spatially mapped pathways (elaborated in sect. 2.2.3) while in the left hand (WHEN) stream, a single non-spatial signal is involved. The distinction is shown symbolically with circular ‘map’ symbols and rectangular ‘gate’ symbols respectively.
Competitive interaction occurs when two centres, or two regions within a centre, are cross-connected with reciprocal inhibitory links. Such a pattern of cross-connections will mean that increased activity in one of the centres will tend to reduce activity in the other and vice versa. This is a push-pull situation and, apart from brief periods of dynamic non-equilibrium, either one centre or the other will become active in a winner-take-all manner. We identify three points where competitive interaction occurs during the process of saccade generation. The first two are between the WHEN and the WHERE streams, the final instance is when competition between potential targets arises in the WHERE pathway.
Of the five levels, we suggest that, at least for the range of phenomena and time scales discussed in connection with the model, the processes in levels 1,2 and 3 operate in a stereotyped way which is not modifiable by cognitive influences other than through the descending pathways of the model. In other words, at these levels, the processes are effectively automatic and hard wired. So, for example, the automatic access of visual onsets means that when saccades are made, visual onsets cannot be totally ‘ignored’. This does not of course entail that visual onsets will automatically result in saccadic orienting.
There are three pairs of oculomotor muscles that rotate each eye. The motor command to these muscles is produced at level 1. Saccadic movements occur when a trigger signal opens a gate in the WHEN pathway at this level. This leads to a spatially coded motor command being generated by the final stages of the WHERE pathway. Coding is here in terms of muscle activation, shown schematically by a symbol representing four recti. The processes at this level ensure that the eyes move with optimum speed and efficiency when a command signal is received, but otherwise remain immobile.
This level reflects, in a highly oversimplified way, the brainstem circuitry of omnipause cells and pre-motor burst cells (see sect. 3.2.1). An important feature is the separation of two processes at this level and two routes to these processes descending from higher levels of the WHEN and WHERE systems. Because of operations at level 2, the signals travelling down these pathways have been pre-packaged in a suitable form to produce a saccade. For example, we suggest that, as a result of Level 2 processes, the signal conveying the spatial characteristics of the saccade will in general have a constant value rather than being dynamically changing. Level 1 processes are, apart from the signals reaching them along these two routes, effectively immune to other higher level influences resulting in the stereotyped nature of saccade trajectories (see sec 3.3.2).
Competitive push-pull interaction is also a critical aspect of the processing at level 2. The major form of competition in this case is between the fixate centre and the move centre. Whereas at the motor command level the push-pull interaction served to shape a rapid movement, the operation at level 2 is more concerned with integrating the various competing information signals to decide whether and where a saccade should be made. It is suggested that this conflict resolution process involves a relatively slow build up of activation in one centre with a decline in the other. Moreover, it is this time consuming process that determines the exact point in time at which the saccade is initiated. Saccades are generated when the activity in the fixate centre falls below a certain threshold level at which point the level 1 gate is opened. Reduction in fixate centre activity may be termed disengagement. Any increased activity in the move centre will promote disengagement through the reciprocal inhibitory connections and disengagement can also occur via descending influences to level 2. The fixate centre is part of the WHEN pathway and thus operates as a single unit. However, as discussed in sect. 2.3, it can be directly influenced by events in the visual periphery as well as those at fixation.
The move centre forms part of the WHERE pathway and carries a spatial code. We envisage it as a two-dimensional map formed by a neural network with each point on the map coding a different visual direction. In contrast to the coding at the motor command stage, the coding at this stage is spatiotopic although in a highly distributed manner (see next sect.). This map is subject to descending influences from higher stages. The routes carrying these influences carry a topographic mapping and some of these routes arise, directly or indirectly, from retinotopically mapped visual sensory areas.
At any instant each point on the map registers an activity value. We term this the salience map. We postulate that, when a saccade is triggered, the point of current maximum salience determines its metrics. This deceptively simple statement will receive further elaboration and justification subsequently (sect. 3.3.3). The activity in the salience map is in competitive interaction with activity in the fixate centre as discussed previously. A further set of conflict resolution processes can occur within the move centre. We postulate multiple inhibitory cross-links between the various different regions of the map. These operate to ensure that activity in the network tends towards a winner-take-all state with a single salience peak. Conflict resolution between multiple potential saccade targets occurs in this way. Once this occurs, the single peak dominates and has the potential to shift the fixation-move balance in favour of a movement. We envisage that the processes at this stage operate like a sample-and-hold system so that in general saccade trajectories are not subject to influence from the continuously changing activity at higher levels.
An important characteristic of the salience map is the use of spatially distributed coding, alternatively termed population coding or ensemble coding. Spatially distributed coding maps a topographic spatial map with divergent and overlapping connections (i.e. through large and overlapping receptive fields). Distributed coding ensures that the salience landscape is one of smoothly changing contours rather than having multiple isolated peaks. This simplifies the conflict resolution process. It might appear that distributed coding results in a loss of accuracy in the spatial representation. However, if just a single target is involved, this is not the case (Hinton et al. 1986). The disadvantage of distributed coding is the lack of ability to code two simultaneous targets.
At the next level in the hierarchy, we identify routes by which visual stimulation influences the fixate-move system. The separate level for these influences indicates that these routes directly influence level 2 processes, resulting in effects that are not subject to cognitive influences. Our model postulates that stimulus change, in particular onset and offset of visual stimulation, has automatic effects on both processing streams as described in the next paragraph.
Central visual events at the currently fixated location have a direct effect on the fixate centre. Offset of central stimulation promotes disengagement, whereas onset increases activity in the fixate centre. Peripheral visual events occurring away from fixation generate effects in both the fixate and the move centres. The effect on the move centre is to stimulate activity in the salience map at the point corresponding to the event location. This will frequently determine or influence the choice of saccade target. This increase in activity in the move centre will render saccade triggering more likely. However, there is also a direct effect of a peripheral event on the fixate centre. Visual onsets, even in the periphery, act to enhance fixation centre activity. Reasons for including this apparently paradoxical route are spelt out in sects. 3.2.2 and 4.1.2.
In levels 4 and 5, we attempt to sketch the way in which our model is capable of integrating high level influences. Level 5 reflects the self evident point that, at least for normal individuals, all lower level processes can be over-ridden and an individual can either suppress saccades and maintain fixation, or can move the eyes voluntarily. Such considered actions are unusual. Normally, saccade control occurs at level 4 and the term automated has been chosen to describe the processes operative. This term both indicates that the processes operate below the level of conscious awareness and provides a marker that implicit learning and memory may be expected to play a significant role in the level 4 stages (Maljkovic & Nakayama, 1994; Lambert & Sumich, 1996).
The multiplicity of uses of saccades was mentioned in the introductory paragraph of this paper. This multiplicity gives rise to the problem of co-ordination of different sources and streams of information, echoing in a miniature way a general feature of human activity which is frequent multitasking and task switching (Norman & Draper, 1986). Situations will often arise in which more than one target could be selected for gaze redirection. The eye can of course only move to one at a time. How is conflict between the potential targets resolved? The salience map introduced in sect. 2.2.3 is envisaged as a two-dimensional contoured surface with the two spatial dimensions representing visual directions and ‘depth’ representing salience. There are multiple inputs which are integrated into this salience map. We propose that the point of highest salience in the map becomes the target for the saccade. The architecture of the move centre provides for some implicit conflict resolution to enhance the high salience point. We propose that conflict resolution is only resolved in this implicit way with no over-riding supervisory decisions or more elaborate processing.
We believe that two forms of cognitive control of saccade metrics can be identified. Spatial selection works by modifying the salience map in specific regions, in either a potentiating or an inhibitory manner. Thus selecting a particular region of the visual field will take the form of a potentiated spatial window. This window will always be quite extensive, because of the constraints of the distributed coding at level 2. Following such selection, saccades will be directed to a location constrained by the window although the exact landing position may be determined by the specific details of the visual stimulation within the window. The phenomenon of inhibition of return (Rafal et al 1989) is another spatial selection influence. Inhibition of return refers to an increased difficulty of orienting to a location to which attention has previously been directed. This possibly ensures that fixations are less likely to return to a previous point of high salience (Klein, 1988).
The second form of control, which may operate together with the first, is referred to as search selection in Figure 1 and promotes saccades to particular visual features wherever in the visual field they may occur. Search selection is assumed to operate within the visual processing areas of the brain. If search selection is not active, then the visual input to level 2 is a general visual map. Search selection allows selected features to have preferential access to Level 2.
The final factor operative at level 4 has been denoted intrinsic salience. It seems plausible to suggest that visual contours and areas of the visual field of high contrast are intrinsically salient. We suggest also that long and medium term learning and adaptive processes may also modify the salience of visual information. For example, Beauvillain et al. (1996) have shown that unusual orthographic patterns can attract saccades during reading. Also carry-over effects have been noted in experiments on visual search which suggest that the target item used in an earlier search retains salience when the task changes to require a different search target (Maljkovic & Nakayama, 1994; Findlay, 1997)
We identify two routes whereby higher level influences can affect the WHEN pathway. The first concerns temporal preparation. We suggest that disengagement at level 2 can be promoted by suitable temporal preparation such as is produced by warning signals or predictable timing of the target onset. The second descending route is from ongoing cognitive and perceptual processing. When engaged in a complex perceptual activity, such as text reading, the saccadic system must be able to sequence movements to enable visual information uptake to occur smoothly. Too brief a fixation would not allow visual information to be taken in adequately while too long a fixation would be time consuming. Remarkably, human visual scanning seems to be able to control this balance very effectively. We suggest that this is because the level 2 fixate centre can be influenced directly and rapidly from centres of cognitive processing.
In this section we describe specific work which we wish to acknowledge as having influenced our thinking.
The idea of separate control for the temporal and spatial decision in connection with saccades emerged in the late 1970s. Becker & Jürgens (1979), in a classic paper, proposed a model in which a triggering process controlled the occurrence of a saccade as well as the choice of direction while a separate computational process determined its amplitude. Our model can in some ways be regarded as an extension of their thinking. Workers of a more cognitive persuasion (Rayner & McConkie, 1976) also noticed that in tasks such as reading, there appeared to be separate control of temporal parameters (fixation duration) and spatial parameters (saccade size).
The emphasis on competitive interaction in saccade generation can be found in much physiological thinking (see next sect.) and has also been promoted by Carpenter (1981; Carpenter & Williams, 1995). The potential of a distributed spatial code has long been recognised (Erickson, 1968; McIlwain, 1976) and has formed one of the distinctive features of modern neural network theory. The suggestion that the goal for visual attention capture might be determined by the point of highest salience on a map representation of visual space has been frequently suggested in the context of visual attention and visual search (Koch & Ullman, 1985; Treisman & Sato, 1990; Henderson, 1992; Wolfe, 1994).
Our discussion of the direct effects of visual stimulation has, we believe, some original features although we acknowledge the similarity with concepts such as the ‘ocular disengagement’ of Tam & Stelmach (1993). We also sense a convergence with work on visual attention in human experimental psychology (Egeth & Yantis, 1997) which has also recognised the compelling nature of sudden visual onsets (Jonides & Yantis, 1988). It is possible that a somewhat more sophisticated novelty detection system operates than simple detection of transients (Nakayama & Mackeben, 1989; Yantis & Hillstrom, 1994) but this additional detail will not be developed further here.
The discussion of spatial selection and search selection owes much to current work in visual attention and search as well as some specific suggestions (e.g. Kowler, 1990) by oculomotor workers. Ideas about covert visual attention have included spotlight and zoom-lens models (Posner & Cohen, 1984; Posner & Petersen, 1990; Eriksen & St James, 1986). Work in visual search has shown how excitatory and inhibitory processes could achieve search filtering (Schall & Hanes, 1993; Desimone & Duncan, 1995). A specific suggestion that has close affinity to ours is that of Duncan (1995) who has used the term competitive interaction to describe how visual search might occur. Competitive interaction works within feature maps to select a desired feature as well as across spatial maps to enable object selection and has obvious similarities with our competitive inhibition.
The immediate saccadic pre-motor circuitry in the brainstem has been investigated in considerable detail and our level of understanding is high. Convenient summaries are given by Fuchs et al. (1985), Wurtz & Goldberg (1989) and Moschovakis & Highstein (1994). Level 1 of our model is explicitly based on brainstem processes. For our purposes, the essential programming feature is the flip-flop like switching between pause cells and burst cells in the brain stem. Pause cells, or omnipause cells, normally fire at a high rate but cease activity for the duration of each saccade made (the pause of activity precedes the actual saccadic movement by 5 - 15 ms). Burst cells show just the opposite pattern of activity; their rate of firing increases dramatically during appropriate saccades. The omnipause cells show no specificity and cease firing for each saccade made, whereas the activity of the burst cells is coded in terms of the spatial metrics of the saccade. To account for this specificity difference, it is necessary to postulate at least two descending pathways, one carrying spatially coded information and the other acting merely to convey a trigger signal. The WHERE and WHEN terminology appear to have been first introduced by oculomotor neurophysiologists (Van Gisbergen et al. 1981).
The above brief account enormously simplifies the brain stem system, ignoring a) the neural integrator circuit which ensures the eye is held stable in the new position following the end of the saccade, b) the separation of the burst cell regions for horizontal movement and for vertical movement, c) the routing circuitry which ensures the correct muscle pairs of each eye are given appropriate signals, d) the feedback pathways (see sect. 3.3.1) to enable accurate saccades to be made to visual and remembered targets, e) long term adaptive processes maintaining the accuracy of the system.
Recent work of Munoz, Wurtz and collaborators (Munoz & Guitton, 1991, Munoz & Wurtz, 1992, 1993a,b; Wurtz, 1996) has achieved a major breakthrough in our understanding of the neurophysiology of saccade control. Their work has concerned the rostral pole region of the superior colliculus which carries the representation of the fovea in the visual and motor maps and appears to be directly connected to the omnipause neurons of the brain cell (Paré & Guitton, 1994). Munoz and collaborators have shown that the term ‘fixation centre’ can be used appropriately to describe the function of the region in both cat and monkey. In monkeys, cells in the region are active whenever the animal is fixating and pause during saccadic eye movements (Munoz & Wurtz, 1993a). The region is GABA sensitive (Munoz & Wurtz, 1993b). Injection of the GABA agonist muscimol into the region increases saccadic activity, leading to difficulties in maintaining fixation and reducing the latency of target elicited saccades. Conversely, injection of the GABA antagonist bicuculline into the region has the opposite effects and saccade latencies are increased. Munoz & Wurtz (1993b) suggest that the evidence supports a push-pull relationship between the cells in the fixation region of the rostral pole and the cells in the remainder of the deep layers of the colliculus, known to code saccade metrics as a ‘motor map’. Their stated hypothesis is that "activation of fixation related cells of the rostral superior colliculus is necessary to maintain visual fixation; whereas a pause in the discharge of these cells is a prerequisite for the initiation of a saccade". This viewpoint is reinforced by the demonstration that, when monkeys are tested in the gap paradigm (sect. 4.1.1), fixation cell activity is attenuated during the gap period with activity in buildup neurons increasing in reciprocal fashion (Dorris & Munoz, 1995; Dorris, Paré & Munoz, 1997).
An issue that is as yet unresolved is the spatial size of the fixation centre. As described by Munoz & Wurtz (1992, 1993a), the centre was located in the rostral pole of the colliculus, corresponding to about the central 2 degrees of the visual field. However, other work (Gandhi & Keller, 1997) has reported that cells with the appropriate properties for fixation neurons can be found in a more extensive region of the colliculus (extending over at least the central 10 degrees). A further puzzle relates to the issue of whether the fixation centre operates as a single unified system. The collicular fixation system shows a degree of directional (left/right) specificity that we have not included (see sect. 4.7).
We thus believe that there is strong evidence that the fixation system in the superior colliculus operates in a way which is compatible with the fixate system of our level 2. However, we do not wish to imply that our model shows total physiological isomorphism with this system. In particular, we wish to leave open the possibility that the fixate system may be more widely distributed than the collicular fixation system. Neurons with similar properties to those of the collicular fixation system are also found in parietal and frontal cortex (Sakata, Shibutani & Kawano, 1980; Hyvarinen, 1982; Goldberg & Segraves, 1989) and a direct pathway exists between the frontal eye fields and the oculomotor centres (Segraves, 1992). Hanes & Schall (1996) recently reported an impressive correlation between rate of activity in frontal eye field neurons and saccade latencies. We have chosen a different terminology (fixate rather than fixation) from that used by most physiologists to make clear that our model is functional rather than physiological.
Distributed coding is a notable feature of the superior colliculus. Visual cells have large and overlapping receptive fields and moreover the colliculus is a layered structure in which field size increases systematically with depth (Sparks, 1986; Sparks and Hartwich-Young, 1989). As a consequence, any particular point in the collicular motor map can be stimulated by visual input from a wide region of visual space and stimulation from a punctate peripheral source generates activity over a wide region of the colliculus. The potential importance of this distributed coding for the conversion of the spatial visual code to a suitable oculomotor code was first appreciated by McIlwain (1976) and has been the basis of subsequent physiological work and quantitative modelling (Lee et al. 1988, Van Gisbergen, 1989, McIlwain, 1991, Wurtz, 1996).
In sect. 2.2.3, we make the further suggestion that processes of competitive interaction operate within the salience map to promote the selection of a unique saccade goal. We believe a plausible physiological substrate for this conflict resolution involves the system of reciprocal inhibitory connections between different regions within each colliculus (intra-collicular inhibition) and further inhibitory cross connections between the colliculi (inter-collicular inhibition). Early work in cats found evidence for both forms of inhibition (Sprague, 1966; Rizzolatti et al. 1974) and similar findings were later reported in the monkey (Wurtz et al. 1980). Koch & Ullman (1985) showed how a neural network to determine the locus of maximum salience might be implemented in this way.
More recently, a number of physiological studies (reviewed in Desimone & Duncan, 1995) have shown how the processes of target selection for the oculomotor system might work at the detailed level through a similar interplay of excitation and inhibition. For example, Schlag-Rey et al. (1992) have considered how target selection might occur in a situation demanding conflict resolution. They showed, in monkeys, that electrical stimulation of the frontal eye fields, of a strength to potentially evoke a saccade, has a dual effect on neurons in intermediate layers of the superior colliculus. In regions whose movement fields correspond to the direction of the elicited saccade, excitation occurred. However, in other regions, an inhibition of neural activity was found. Schlag-Rey et al. noted that surround inhibition in the colliculus plays an important role and suggested that the inhibitory effects arose through collicular cross-connections.
Moreover this principle can extend to search selection (Duncan, 1995). Schall & Hanes (1993) studied responses of frontal eye field neurons in monkeys performing a simple colour search task. Neurons responsive to the spatial region of the target showed an activation enhancement around 50 ms prior to the monkey making a saccade to it. Conversely neurons responsive to neighbouring regions where there was a distractor stimulus of the wrong colour showed a marked diminution of activity prior to the saccade. A similar result for cells in infero-temporal cortex has been reported by Chelazzi et al. (1993). Furthermore, these spatial patterns of enhanced and diminished activity are maintained during periods in which the animal is required to delay responding, thus forming a short term spatial memory (Glimcher & Sparks, 1992; Chelazzi et al. 1993).
In this section we consider some points of contact between our framework and other work in saccade modelling from an oculomotor standpoint.
Twenty years ago, Robinson (1975) suggested a model of saccade generation that was very influential in subsequent thinking. There were two novel aspects to this model. Robinson argued first that, although saccadic eye movements were ballistic from an overall functional standpoint, the neural mechanisms generating saccades employed a feedback process driven by some internal representation of the movement goal. His second suggestion was that the movement goal consisted of a representation of the target position in head centred, rather than eye centred, space.
There has been strong support for Robinson’s first postulate. Under some conditions, the trajectories of saccades show the existence of a corrective process operative during the movement generation (Zee et al. 1976; Jürgens et al. 1981). Furthermore, Mays & Sparks (1980) showed that if, during the course of preparation of a visually elicited saccade, a movement of the eye was induced by electrical stimulation of the superior colliculus, then the visually elicited saccade showed compensation for the perturbation, even though the visual target was no longer visible. These and other results show that during the process of saccade generation, some reference signal about the saccade goal is available.
The second part of Robinson’s suggestion has received less support. Although considerable effort has been devoted to discovering a signal in neural centres devoted to saccadic eye movements in which the coding is not oculocentric, no compelling evidence for such a signal has emerged (Moschovakis & Highstein, 1994). Furthermore, more subtle tests looking for effects relating to saccadic eye movements which might suggest evidence of a signal specific to target position have also given negative results (Rohrer & Sparks, 1993). Andersen et al. (1985) discovered cells in the posterior parietal cortex whose responses were modulated by eye position. In principle, such cells could be used to obtain a head centred representation of the target (Zipser & Andersen, 1988). Such a representation is of undoubted importance in visually co-ordinated behaviour but is not necessarily involved in the generation of visually elicited saccades.
We have not included the feedback process in our model since at a functional level, our model merely requires the conversion of a spatial signal into an appropriate motor command signal. Several current suggestions exist about how this could be accomplished without using a head or body centred co-ordinate system (Van Opstal & Van Gisbergen, 1989; Moschovakis & Highstein, 1994; Arai et al. 1994). An alternative approach suggests that the feedback process operates on motor error (Sparks, 1986). Motor output uniquely codes eye position (Wurtz & Goldberg, 1989) and thus motor error is equivalent to eye position error. Moschovakis & Highstein (1994) have suggested a feedback control process working on eye position error that is compatible with current physiology. This approach has the advantage that the stored representation involved in the feedback loop is interpretable as the memory of desired eye position to acquire the target. It has been previously suggested (Droulez & Berthoz, 1990, 1991) that the results of Mays & Sparks (1980) could be interpreted in terms of visual or oculomotor memory.
In our model, saccade production requires the opening of gates in the WHEN pathway to allow the control signals to be generated for the eye muscles. These gates must be opened for a period that corresponds, at least roughly, to the duration of the saccade. If the input signal changed during the period the gate is open, the motor output would be influenced by the change and saccade trajectories would vary in a manner reflecting this changing stimulation rather than being stereotyped for saccades of a given size.
Several studies have examined saccade trajectories to discover whether a changing saccade goal can result in on-line modification of saccade trajectory. Large saccades (40 deg) recorded in a double step paradigm frequently show trajectory shifts in which the saccade goal appears to be updated during the course of the trajectory (Van Gisbergen et al. 1987a). However, with only very rare exceptions, smaller saccades (up to 10 degrees) show no major systematic variability of trajectory (Hou & Fender, 1979; Findlay & Harris, 1984) although detailed analysis reveals small but systematic effects of higher processes on trajectories (Rizzolatti et al., 1994). This suggests that for the small saccades typical of everyday viewing, the system operates with a unique spatial goal and thus circumvents the problems of dynamic update. In the next section we make a speculative suggestion about how this could be achieved.
We have proposed in sect. 2.2.3 that the metrics of the saccade are determined by the location of a peak in the salience map. We argue that this takes place through a winner-take-all process within the underlying salience map. Koch & Ullman (1985) demonstrated the computational plausibility of such a process and there is currently considerable interest among workers in computational vision for implementing such networks (Tsotsos et al, 1995). We recognise that our own suggestions for implementation are relatively sketchy but believe that they provide an account which will eventually yield to full quantitative modelling.
We propose that a winner-take-all process selects the salience peak at a particular instant in time so that, when this selection occurs, the saccade is directed to the location on the salience map represented by the peak. We suggest that the metrics are based on the location of the activity peak rather than on integrated neural activity. This requires an implicit ‘sample and hold’ process quite similar to that of the classic early model of Young & Stark (1963) except that the signal sampled arises from the salience map rather than the direct retinal input. Once the location of the activity peak is selected, a non-linear triggering process occurs which results in a fixed and stereotyped burst of activity localised at this peak.
An attractive feature of this proposal is that it can also achieve the solution of a further problem that has taxed modellers of the saccadic system. The problem is that of ensuring the response is characteristic only of the location of the target and independent of other target characteristics, in particular stimulus intensity. This may be termed the normalization problem. In one of the most fully formulated models of saccade metrics using distributed processing, Van Gisbergen et al. (1987b) showed quantitatively how saccade metrics could be accurately generated. Their model used linear vector addition over a stimulated region of a hypothetical collicular map. Nevertheless, this model was unable to explain such phenomena as the global effect (sect. 4.2.2), essentially because metrics were calculated on the basis of a vector sum of input activity. A subsequent modification (Van Opstal & Van Gisbergen, 1989; cf. Lee et al. 1988) overcame these deficiencies by introducing non-linear lateral spatial interactions to provide normalization; our proposal is an alternative non-linear solution of the normalization problem.
We believe this suggestion is plausible in the light of recent discoveries about collicular processing. Munoz & Wurtz (1995a,b) have reported two categories of cell, build up cells and burst cells, involved at the level of the collicular map. Buildup cells and burst cells were located throughout the collicular map apart from at the rostral pole where the fixation cells form a rostral extension of the buildup cells. Buildup cells showed a gradual rise in activity following the onset of a peripheral saccade target which was reciprocally related to activity in fixation cells; buildup cell activity increased as fixation cell activity decreased. In contrast burst cells showed a sudden burst of activity just before saccade onset. Burst cell activity extended over a region of the colliculus, the location of which, but not the extent of which, depended on the saccade size. Burst cell activity did not spread spatially from this region. Munoz and Wurtz suggest that the buildup cells are involved in the "preparation to make a saccade" while burst cells may encode the metrics of the desired movement (see also Wurtz, 1996).
We suggest that the processing in the buildup cells leads to the selection of an unequivocal activity peak, perhaps by competitive inhibition between different potential peaks. The burst cells only operate once a peak has emerged and, in addition, operate subsequently in an all or none manner to give a stereotyped burst in a restricted region of the map around the selected peak. Such a process could give a solution to the normalization problem since the burst would depend only on the location of the peak and not on its other characteristics. This suggestion is obviously speculative at present but does not seem to exceed the bounds of neurophysiological plausibility.
This section reviews experimental studies of human saccadic movements and suggests how the data can be explained using the model. Sects. 4.1 and 4.2 consider a number of experimental findings obtained with the target elicited saccade paradigm. Sects. 4.3 to 4.5 deal with saccades where higher level influences play more of a role. Sect. 4.6. relates our work to attentional theory and in conclusion Sect. 4.7 considers some results from eye movement studies in the neuropsychological disorder of hemispatial neglect as an example of how the model might be applied. In this section, we also contrast predictions of our model with other extant models (see particularly sects. 4.1.3, 4.2.2, 4.4.1, 4.5.1 and 4.6)
The gap effect describes how visual events at the fixation location have a substantial effect on saccade latency. In particular, if a fixated stimulus disappears slightly before the target appears, saccades have very short latencies. The effect is robust and is independent of advance knowledge of the location of the saccade target (Kingstone & Klein, 1993; Walker et al. 1995). The effect shows that some of the processing for a saccade can occur with no foreknowledge of whereabouts it will be directed. It thus supports in a general way the proposal of parallel processing in WHEN and WHERE streams. The first report of this effect was by Saslow (1967a) who varied the point in time of fixation point offset, relative to the onset of a saccade target. When the fixation disappeared 100 - 200 ms before the target onset (leaving a gap period with no stimulation visible), latencies to the onset of the target were much shorter than if the fixation point remained until target onset. If the fixation point remained on after target onset (overlap) latencies were further lengthened to become about 100 ms longer than in the gap condition.
Ross & Ross (1980, 1981) suggested that the fixation point offset might provide a warning signal giving temporal information about the appearance of the target. As shown in earlier work (Cohen & Ross, 1977), saccadic latencies can be reduced by temporal warning signals. Ross & Ross reasoned that any event at the fixation point (such as brightening or change) might also reduce saccade latencies. They showed this to be the case. Nevertheless, the latency reduction was considerably stronger when the fixation point was extinguished. Moreover, visual onsets at fixation simultaneous with, or slightly following, the target onset produced a substantial latency increase. They concluded that the gap effect resulted from two components, a warning signal effect and an effect specific to visual offset. Several recent studies (Reuter-Lorenz et al. 1991, 1995; Kingstone & Klein, 1993; Forbes & Klein, 1996) have confirmed the suggestion that the gap effect has two components. The warning signal like component effect is also found with manual reactions (Tam & Stelmach, 1993) whereas the second effect is specific to saccade generation. This second effect has been called variously fixation offset, fixation release, fixation disengagement or ocular disengagement.
In our model, the critical stage in determining saccade release is the resolution of the fixate/move conflict at level 2. The gap manipulation affects this conflict via two routes. Visual events at the fixation point have direct access (level 3) to the fixate system. Offset of a stimulus at the fixation point automatically reduces activity in the fixate centre and renders saccade triggering more likely. The second route involves the temporal preparation stage at level 4.
Paradigms involving double stimuli have been very revealing in studies of saccades. If two stimuli are presented simultaneously in reasonably close proximity, the primary effects are on saccade metrics (sect. 4.2.2). However, if two widely separated simultaneous stimuli are presented, the saccade lands accurately on one of them but its latency is prolonged. The effect was first observed by Lévy-Schoen (1969) in a study attempting to establish what rules governed the choice of stimulus fixated under these circumstances. Lévy-Schoen (1969) presented two simultaneous targets and found that an accurate saccade was made to one or the other, with various biases influencing the one likely to be fixated, the strongest being proximity to the fovea (Lévy-Schoen, 1969, 1974; Findlay 1980). The latencies of these saccades were greater than to control single targets, a finding, which has been replicated in several studies (Findlay, 1983; Weber & Fischer, 1994)
Walker et al. (1995) showed that the latency increase occurs whether or not the subject has prior knowledge of target location. Moreover the effect is temporally specific to simultaneous or near simultaneous stimulation (less than 100 ms offset between the two stimuli). Rafal et al. (1990) studied responses to bilateral target presentation in a group of patients with homonymous hemianopia as well as in a control group of normal subjects. They reported bilateral target slowing in the case when the bilateral distractor occurred in the blind temporal hemifield of the hemianopes but not when it was in the blind nasal hemifield. In contrast to the studies reviewed above, they reported no effect in control subjects. However, Figure 3 in their paper shows a small latency increase for bilateral presentations, albeit possibly non-significant, in the control subjects.
The above studies exclusively used two targets located on the horizontal axis and often at equal eccentricity. We have recently (Walker et al. 1997) examined the effects of distractor stimuli in different positions of the visual field. Our results show that the effect is a very widespread phenomenon and is neither specific to distractors on the opposite axis to, nor to those at the same eccentricity as, the saccade target. Visual onset of a distractor results in a latency increase at any location remote from the target, including remote locations in the same visual field as the target. Moreover, the latency increase is dependent in a systematic way on the location of the remote distractor, being greatest when this is at the fixation point and reducing monotonically as the distractor is positioned more eccentrically. This pattern of results strongly implicates the non-specific fixate system. If the effect depended on interactions within the salience map, then its magnitude would be expected to depend on the distance between distractor and target.
When the distractor is positioned at the fixation point, its effect is readily explicable in terms of direct activation of the fixate system (sect. 4.1.1). We suggest that the onset of a remote distractor at other locations also affects the fixate system. This postulate requires that the fixate system is accessed by stimulation from an extended central region of the visual field, a suggestion compatible with some physiological evidence from the collicular fixation system (Gandhi & Keller, 1997). We suggest that events in the near visual periphery (out to at least 10 degrees) directly influence the fixate system with a strength of connection that depends on the degree of eccentricity. This direct influence increases activity in the fixate centre and thus slows the triggering process.
Fischer & Boch (1983) used the gap paradigm with trained monkeys and observed that target directed saccades with extremely short latencies (80-100 ms) were frequently produced. They introduced the term express saccade to describe these movements, and later reported them in human subjects (Fischer & Ramsperger, 1984). Subsequent work has elaborated their properties and the conditions under which they occur (Fischer & Weber, 1993). A striking finding is that under some circumstances, there is a marked bimodality in the latencies with a short latency ‘express’ population and a longer latency ‘regular’ population (Jüttner & Wolf, 1992; Nothdurft & Parlitz, 1993), although this bimodality has not been always found (Reuter-Lorenz et al, 1991; Wenban-Smith & Findlay, 1991).
We have already discussed in sect. 4.1.1. how saccades with short latencies might arise when the fixate system is disengaged. We believe our model might also account for bimodality in saccade distributions. Critical to our explanation is the spatially extended fixation region discussed in sect. 4.1.2. A consequence of this is that a peripheral visual target will affect both the move system and the fixate system. We suggest that, if the fixate system is already in a state of disengagement it is possible that the triggering can occur immediately as a result of the increased stimulation in the move system. Such a state of disengagement would be likely in paradigms where target occurrence was highly predictable, and also with trained subjects. These situations are indeed ones which render express saccades frequent (Fischer & Weber, 1993; Paré and Munoz, 1996). However if immediate triggering does not occur, the fixate system activation builds up through the direct pathway (level 3) and an extra time consuming period is needed to overcome this target generated activation. During this period the system is refractory and saccades are less likely to be triggered.
According to this account express saccades should be rendered more likely in conditions in which the move system is activated by the target rather than fixate system. Hence it would be expected that express saccades should be more common with more eccentric stimuli since activation of the fixate system increases with proximity to the fovea (sect. 4.1.2). Exactly this finding was made by Weber et al. (1992). They showed that express saccades occurred frequently when targets were at 4 degrees eccentricity but their frequency decreased for targets at smaller eccentricities, being absent at eccentricities below 1.5 degrees. Their account of this phenomenon is quite similar to the one presented here.
The earliest theoretical accounts of express saccades (Fischer, 1987) suggested separate anatomical pathways and a quantitative model recently formulated by Fischer et al. (1995) envisages that saccades are produced purely by the build up of excitation to some threshold level. In contrast to our model, no role is assigned to inhibition. Other recent work has given more emphasis to processes such as attentional disengagement (Fischer & Weber, 1993: Fischer et al. 1995) and gating of the fixation system (Cavegn, 1996). This treatment in terms of processes is closer to our own thinking although we argue in sect. 4.6 against the specific idea of attentional disengagement. Recent physiological work directed to understanding the neural substrate of express saccades (Edelman & Keller, 1996; Paré & Munoz, 1996; Dorris, Paré & Munoz, 1997) supports an account in terms of fixation system activation although Dorris et al argue that, in addition, oculomotor preparation (involvement of the spatial selection system) is a requirement for express saccades to occur.
The 'anti-saccade paradigm' is one in which saccades are voluntarily directed away from a peripheral target. Hallett (1978) developed this technique and reported that anti-saccades were characterised by longer latencies than reflexive saccades and showed more variable primary amplitude. On some trials subjects were found to erroneously make saccades to the target (‘pro-saccade’ errors). It was found that the latency of anti-saccades was related to the latency of reflexive saccades (Hallett & Adams, 1980), which was attributed to the sum of a constant delay (neural impulses) and a variable 'goal redefinition' process. The goal redefinition process cancelled the primary reflexive saccade, and if it was delayed then a reflexive 'error' saccade would result. Although this account is appealing it should be noted that a clear relationship between reflexive and anti-saccade latency has not always been observed (Guitton et al. 1985).
A number of studies have examined the facilitatory effects of the gap condition on reflexive and anti-saccade latencies. Although Reuter-Lorenz et al. (1991) failed to find a reduced latency for anti-saccades in a gap condition, a latency reduction has been reported in subsequent studies (Fischer & Weber, 1992; Reuter-Lorenz et al. 1995). However the magnitude of the gap effect is greater for reflexive saccades than for anti-saccades (Reuter-Lorenz et al. 1995; Forbes & Klein, 1996). Such a finding is consistent with the two component explanation of the gap effect discussed in sect. 4.1.1. Anti-saccades only benefit from the non-visual (warning signal) component since the suppression of the central fixation system necessary to prevent release of a reflexive saccade renders ineffective the activity reduction through fixation point offset.
Anti-saccades involve the voluntary inhibition of a reflexive saccade and the cognitive manipulation of the spatial parameters to produce a saccade in the opposite direction. In our model, the ability to voluntarily suppress a saccade can be performed by the level 5 voluntary decision process connected to the central fixation system. This route enables reflexive saccades to be cancelled. The cognitive control over saccade metrics in Hallett's goal redefinition process must also depend on Level 5 processes. These might work through controlling spatial selection but could also use search selection processes, the search target being a region of absence of stimulation.
Damage to the human frontal cortex is known to increase the number of pro-saccade errors made in the anti-saccade task (Guitton et al 1985). One explanation of this increase in reflexive pro-saccades is that the timing of the cancellation signal is altered. Anti-saccade errors would be more likely to occur if the time taken for the voluntary inhibition was increased. If the level 3 operations are completed before the cancellation signal is produced then a reflexive saccade would result). A recent alternative account has related anti-saccade errors to so-called 'executive processes' such as working memory that are thought to be functions of the frontal lobe. Support for this view has come from a study by Roberts et al. who showed studied anti-saccade performance in normal subjects when performing a concurrent working memory task (Roberts, Hager, & Heron, 1994). They found that pro-saccade error rates were greatest when the task with the highest working memory load was performed. Further support of a link between working memory processes and anti-saccade error rates has been provided by a recent single case study of a patient with frontal lobe damage (Walker, Husain, Hodgson, & Kennard, in press). The patient was unable to suppress his reflexive glances in the anti-saccade task and was found also to be impaired on tests of working memory and executive function (which involved the temporary suppression of a response). This suggests a link between higher level (level 5) processes and the generation of signals to suppress potent responses. Damage to this system can result in deficits both in working memory and in the anti-saccade paradigm.
In our model, we follow the suggestion of Becker & Jürgens (1979) that the metrics of the saccade are programmed separately and subsequent to the decision to trigger a saccade. Following triggering, a saccade is made to the point of greatest salience in the salience map of the move system. Our model also incorporates the idea that the salience map codes spatial locations in a distributed way. Sects. 4.2.1 and 4.2.2 show how the model explains results from the two step and two target paradigms.
In the two step situation, a subject is required to track a target, which moves in steps. On some trials, two steps occur in rapid succession so that the second step occurs whilst the subject is preparing the response to the first step. In this situation a variety of types of eye movement behaviour can occur. The subject may accurately track both steps with two separate saccades. The subject may make just one saccade to the final position of the target. The subject may also make a first saccadic response to an intermediate position between the two positions of the target with a second saccade to the final target position. Becker & Jürgens (1979) demonstrated that the critical parameter in determining the type of response made was the time interval between the second step and the commencement of the first saccade. This interval, which they denoted by the term D, can be seen as the time available for the information from the second target step to modify the response to the first target step.
If D is small, there is no perturbing effect of the second step and the response goes to the first target position. Likewise if D is large, the response goes to the second target position. However Becker & Jürgens showed that there is an intermediate range of D values in which saccades of intermediate amplitude occur. If the positions of the two target steps are both in the same direction from fixation (e.g. both on the right at 5 deg and 10 deg), then a range of intermediate positions occur. The saccades show a characteristic amplitude transition function (ATF), with the average amplitude showing a systematic dependence on the value of D. If the target positions are more distant or if they are opposite sides of the fovea, then such a transition function is absent, or only minimally present (Ottes et al. 1984). The pattern found in these cases is of a set of saccades towards the position of the first target for small values of D and a set towards the second position for large values of D. There is an intermediate range of D values for which no saccades are found. This suggests that a finite time is required to cancel the saccade in course of preparation to the first target position and reprogram one to the second position. Becker & Jürgens used these results to develop their model of saccade control.
Subsequent work has confirmed this basic pattern and has extended investigations to remove the restriction to the horizontal meridian. If two steps occur between positions, which differ in direction from the fixation point with each having the same eccentricity, then similar transition functions can occur. If the two directions fall within a sector subtending less than about 45 deg from the fixation point, a range of intermediate saccade directions occur in a systematic transition function (Findlay & Harris, 1984; Ottes et al. 1984). This result holds even if the steps take the target across a horizontal or vertical meridian so requiring a change in direction of one component of the saccade.
Our model follows the ideas of Becker & Jürgens (1979) in explaining double step results in terms of spatial and temporal integration of visual information within the salience map. Our model treats the triggering stage as entirely non-spatial whereas in the original Becker & Jürgens model, this stage also produced the direction decision for the saccade. To account for the additional delays when the second target step takes the target to a position across the fovea (the pulse overshoot condition), we suggest that under these circumstances the second step operates as a remote distractor, producing direct activation in the fixate system, as discussed in sect. 4.1.2. The magnitude of the extra delay in the pulse overshoot condition is comparable with that found in the remote distractor effect. In the pulse-undershoot configuration, the second step is in a neighbouring position, producing input into the part of the move system, which is already activated.
A critical question in saccade programming is whether direction and amplitude are in some sense programmed separately. Becker & Jürgens (1979) argued for separate programming because of the extra delays found when the second step of a double step stimulus required a direction reversal. However, in view of the subsequent findings, it may be that other factors than the direction reversal per se contribute to the extra delay and in a subsequent review Becker (1989) was more cautious. Aslin & Shea (1987) carried out work with the double step paradigm and found transition functions for both amplitude and direction. They also investigated situations in which the second step modified both amplitude and direction. They found transition functions but with differences in their time course and argued that direction and amplitude are separately programmed. It should be noted that the time course differences, although clear-cut, are relatively small and also the time relationships are not systematic. In some cases, the changes in amplitude preceded the changes in direction, and in other cases the reverse order occurred. Further discussion of this issue occurs in sect. 4.4.1.
Another elaboration from the single target case is the study of saccades when more than one lone target is presented. If two stimuli are in reasonably close proximity in the visual field, a frequent finding is that the first saccade made to them goes to some intermediate location. This was first reported by Coren & Hoenig (1972) for voluntary saccades. It was later found to be a very characteristic feature of target elicited saccades (Findlay, 1981b, 1982; Deubel et al. 1984; Ottes et al. 1984). The result has been termed the centre of gravity or global effect. The saccade landing point is influenced by the relative visual properties of the two stimuli, such as size, luminance or spatial frequency (Findlay, 1982; Deubel et al, 1984; Findlay et al. 1993), suggesting that it results from spatial integration within the visual pathways.
He & Kowler (1989) pointed out that the global effect can be modulated by higher level factors such as expectancies (He & Kowler, 1989) and suggested that the effect might be entirely due to high level strategies. However, we believe a more appropriate interpretation is that of Ottes et al. (1985) who suggested that the global effect represents a default option for the saccadic system, which can be modified by higher level strategies but is manifest when no such influences are present. In our model the effect is a consequence of the distributed spatial coding in the salience map and pathways leading to it. The integration process occurs over all signals, which are feeding into the salience map in any particular situation. Thus for example, global effects are seen in visual search when targets are present in neighbouring locations (Findlay, 1997; Findlay & Gilchrist, 1997).
Saccadic latencies show strong effects of prior information. As discussed in 4.1, if accurate estimation of the time of the occurrence of the target can be made, latencies are shorter than in conditions of temporal uncertainty. These effects seem particularly powerful and the latency difference may be as large as 100 ms (Michard et al. 1974; Cohen & Ross, 1977). In our model, these effects are subsumed under the heading of Temporal Preparation. This powerful temporal preparation process has been little investigated. Becker, Hoehne, Iwase & Kornhuber (1972), in a study of event-related potentials, showed that saccades are accompanied by a pre-motor positivity in a similar manner to that found with voluntary hand movements.
It has been repeatedly demonstrated that the decision about when a saccade should be made is directly related to the information being processed foveally. As reviewed for example in Rayner (1995), the relationship is indeed reliable enough to have given rise to a substantial body of work in which fixation durations are used as an indicator of processing load. A particularly clear-cut demonstration of the effect of foveal information processing load occurred in the study of Gould (1973). Gould used a task of memory search, in which letters were scanned and a decision required whether or not the letters were members of a memorised target set. He found a substantial effect of memory set size on fixation durations. In this study the immediate visual stimulus was unaltered but its informational load was varied. This variation in informational load had a clear effect on fixation duration. Another example showing the effect of information load is the study by Zingale & Kowler (1987). They showed that, if a subject is required to execute a preplanned sequence of saccades, the latency for the first saccade increases with the length of the sequence.
The ability to direct the eyes voluntarily to a particular location is so familiar that its formal incorporation into a model of the saccadic system is unlikely to be questioned. Our proposal is that spatial selection operates by selection of a localised region within the topographically mapped WHERE system. This follows the idea of Kowler (1990) that saccade metric selection is based on spatial integration of information within some selected region of the visual field. This suggestion appears to offer an approach to the way that cognitive and sensory influences can be combined. The selected region forms a window with the non-selected region outside subject to inhibition in the salience map so that visual stimulation is less effective, possibly to the extent of being totally gated out. The distributed nature of the spatial processing within the maps sets a limit to the minimum size region of visual space which can be selected and to the accuracy with which saccades can be made. Thus Kowler & Blaser (1995) showed that the precision of saccades to simple targets is very little affected by target size over a wide range of sizes.
In the parallel processing account, spatial selection operates in the WHERE pathway and thus would be expected to produce an influence on saccade latencies only through modification of the fixate/move equilibrium. A strong prediction of the model is that the effects of such selection on latencies will then be small. This section examines the relevant evidence.
A number of studies have failed to find any effect of the number of potential target locations on saccade latencies (Saslow, 1967b; Megaw & Armstrong, 1973; Heywood & Churcher, 1980). This result contrasts strongly with the well-known increase in latency for manual choice reaction times as the number of choices is increased. Several studies have looked at the question of whether prior knowledge of likely target position affects latency. Michard et al. (1974) found that prior knowledge of target position led to latencies, which were about 40 ms shorter than when the target could appear in four alternative positions. It should be noted however that the targets eccentricities used in this study were rather large (20 and 40 deg). Megaw & Armstrong (1973) found an advantage of about 18 ms for the pre-specification of target direction. In contrast, Walker et al. (1995) found very small benefits for attentional precueing in comparison with a no precueing condition although precueing did result in costs, i.e. increased latencies to targets at uncued locations.
Abrams & Jonides (1988) developed a model of saccadic eye movement programming based on a study of precueing. Their model differs from ours in several respects and thus the supporting evidence is examined in some detail here. Abrams and Jonides used a precueing paradigm in which subjects were given various types of advance information about the possible location or locations of a saccade target. The influence of this prior information on the latency for target elicited saccades was measured. Four target locations were used, two on the left of fixation and two on the right at 3 deg and 6 deg eccentricity respectively. They were particularly concerned with the comparisons between precueing which specified direction (2 targets on the same side precued), amplitude (2 targets with the same eccentricity on left and right) and the mixed condition (2 targets but with neither direction nor amplitude uniquely specified). They found that the mixed condition resulted in latencies, which were about 13 ms slower than if a single factor (direction or amplitude) was precued. This finding was used to argue for a model in which direction and amplitude are programmed separately, although not necessarily in a fixed serial order. Although the conclusions are logical given the framework adopted, some critical points can be made. Firstly the saccades in this study showed an abnormally high error rate (20 - 25 %). Secondly although the mixed condition resulted in saccades which were slower than in the single dimension cueing conditions, nevertheless mixed precueing produced saccades which were about 30 ms faster than with no precueing, a puzzling result if components are separately programmed.
In general there are small but reliable effects of prior spatial knowledge on saccade latencies. We do not feel that these are of sufficient magnitude to undermine the model we have proposed but rather that they indicate that processes within the WHERE stream can contribute to a small extent to the latency of saccades. Indeed we have suggested in sect. 2.2.3 that a set of conflict resolution processes occurs within the move centre. As we have indicated in the previous section, we believe it is misguided to think of saccade programming as a matter of parameter specification in a discrete way. We wish to place much more emphasis on location specification in a representational map of visual or motor space. Although at the brain stem level (sect. 3.2.1) saccadic eye movements are programmed in terms of muscular components, we are sceptical that this level is cognitively penetrable.
If both spatial and temporal predictability are high, then anticipatory saccades often occur. Saccades, which are initiated before the target appears, are clearly anticipatory, rather than target-elicited. There is good reason to suppose also that any saccade with latency less than about 80 ms from target onset remains anticipatory with a quite abrupt transition at that time to stimulus driven saccades. There are measurable differences in amplitude and in trajectory between the two types (Findlay, 1981a; Smit & Van Gisbergen, 1989). Moreover if two possible target positions exist, then saccades with latency less than 80 ms go to either position indiscriminately (Wenban-Smith & Findlay, 1991) whereas saccades with longer latencies are almost invariably target directed.
In visual search, saccadic eye movements are subject to cognitive control. A particular target is selected from a number of distractors, which differ from the target on some visual characteristic. Recent experimental work, both with humans and with monkeys, has considerably elucidated these search processes.
We envisage search selection as a natural mode of operation of the various retinotopically mapped areas, which map in turn onto the salience map in the move centre. The salience map may be activated in an excitatory manner by stimulus properties appropriate for the search target and in an inhibitory manner by other stimulus properties. The distributed nature of the salience map representation places limits on such a process. In an experiment by Ottes et al. (1985) subjects were presented with one red and one green stimulus and the instruction was to saccade to the target of a particular colour. The task proved simple if the targets were in very different regions of the visual field, but if the targets were within the spatial averaging regions (sect. 2.2.4) then it was only possible to direct the first saccade to the target if its latency was abnormally prolonged; in other cases spatial averaging saccades occurred.
Search selection thus operates through competitive interactions, which can occur at various levels in the multiple different visual areas (see sect. 3.2.4.). This view is elaborated elsewhere (Desimone & Duncan, 1995; Findlay, 1997). In principle, the search selection processes in our model allow complex information to affect saccade landing position providing the processing of the information can be achieved rapidly enough to modify the salience map (sect. 4.5.1). The role of covert attention in the search process is discussed briefly in the sect. 4.6.
An important issue to consider in the high level control of saccades is what type of information can influence saccades, in particular the relationship between saccade processes and visual object recognition. We do not feel that there is enough firm knowledge about visual processing speeds to provide more than tentative answers to such questions. It is possible that only relatively simple information can be made available with sufficient rapidity. In a recent study (Findlay & Gilchrist, 1997) we have shown that shape information (square versus circle) is available to influence long latency saccades in a search task but not short latency ones. This result shows the critical importance of processing speeds. These temporal constraints may also be accompanied by constraints resulting from the pattern of neural connectivity. For example, it might be expected that processes in the dorsal cortical stream would be able to influence saccades more readily than processes in the ventral stream as a consequence of the more direct connectivity from the parietal cortex.
Similar considerations will apply in text reading. A controversial issue in reading research has been whether high level cognitive factors can influence saccade landing positions. There seems little doubt that low level visual factors are the primary determiners of landing position but evidence is accumulating for higher level effects. Several studies have examined saccades to an isolated word target presented in parafoveal vision. If the saccades have short latencies, integration of purely visual information characteristic of the global effect is seen and the global effect is thought to play some part in determining eye fixation positions in reading continuous text (Vitu, 1991). The saccades are influenced by visual factors such as relative contrast of letters (Beauvillain et al. 1996). If the initiation of the saccade is delayed, a more accurate saccade can occur to any desired position within the word (Coëffé & O’Regan, 1987). Furthermore careful analysis has demonstrated that some linguistic factors such as unusual orthographic patterns (Beauvillain et al. 1996) can influence saccade landing positions.
We have suggested that transient visual information is processed automatically (Level 3). In the situation of saccades to targets with transient onset, the onset transient will provide the dominant input to the salience map. However if the subject delays a saccade, the saccade target may be more precisely selected (Ottes et al. 1985; Lemij & Collewijn, 1989; Findlay, 1997), reflecting the dynamic nature of the salience map. Also any new transient stimulation arriving during a fixation will influence the subsequent saccade and such influences are reliably found (Reingold & Stampe, 1997).
A theory of saccade programming is necessarily a theory of attentional deployment. However, in the discussion so far, little explicit reference has been made to attention. Much traditional theorising in the area of attention was predicated on the supposition of resource limitations or limited capacity. We have not found it necessary to make use of such concepts in our theory, although the time consuming processes of competitive interaction do limit the speed with which saccadic eye movements can occur. Our model follows the admonishments of Allport (1993) who argued that there are a multiplicity of attentional mechanisms and workers should adopt goals in domain specific areas.
Studies of costs and benefits in reaction times and in visual performance have repeatedly shown that a selective advantage can be conferred on restricted ‘attended’ areas of the visual periphery when the eyes are held stationary. This covert visual attention contrasts with the overt attentional deployment by means of eye movements. Space limitations preclude a full discussion of the relationship between covert and overt attention (for recent work see Rizzolatti et al. 1994; Walker et al. 1995; Findlay & Walker, 1996) but our proposal of spatial selection has affinities with both spotlight and zoom lens models of spatial attention while additionally introducing the constraints imposed by distributed processing. We have argued that visual transient information has privileged access to the eye movement control system. In a similar way, most theorists of visual attention accept that attention is captured in a reflexive, or exogenous way, by peripheral events (Egeth & Yantis, 1997). We believe there are close general affinities between our work and that derived from more traditional attentional viewpoints although we note below some specific contentious points.
An early theory of visual search (Treisman & Gelade, 1980) emphasized scanning with covert attention, assigning minimal role to eye movements. Our model in contrast has no role for an internal attentional scanning process. Indeed our model would be invalidated if it could be demonstrated that a fast covert attentional scan over a number of locations was possible in the preparation period before a saccadic movement. However, recent estimations of the rate of covert attentional scanning have given estimates which are at least as slow as those of overt eye movements (Sperling & Weichselgartner, 1995; Ward, Duncan & Shapiro, 1996; Findlay, 1997). As elaborated elsewhere (Findlay & Gilchrist, 1998), saccadic eye movements are rapid, easy to produce, and serve to direct the high resolution foveal region to the location of interest. We question whether covert attention plays any role in normal visual scanning.
An influential attention theory, which has relevance to oculomotor control, has been developed by Posner and colleagues (Posner & Peterson, 1990). As described by Posner et al. (1984), "One can consider the act of orienting attention toward the target in terms of three mental operations: disengaging from the current focus of attention, moving attention to the location of the target and engaging the target". This theory was first formulated from consideration of neuropsychological deficits. We argue that, at least as applied to saccadic eye movements, the concept is flawed. In our model, processes equivalent to disengagement and attentional allocation both occur but we entirely reject the idea that the same process in involved in each case, in other words the idea that whatever is disengaged is the same as what is moved. In our view, disengagement occurs in the channel, which is not spatially specific and so is not connected with the spatial aspect of attentional allocation. In support of this position, the magnitude of the gap effect is not affected by attentional manipulations (sect. 4.1.1)
Henderson (1992, 1993) has advanced an attentional based model to account for saccades during reading and scene scanning. According to this model, attention is initially allocated to the stimulus at the point of fixation. When the foveal stimulus is processed, attention is reallocated to some location in the periphery and the system begins to program a saccade to this new location. Thus attentional movements are primary and eye movements are secondary. This model recognises that perceptual and cognitive processing both affect saccade release and subsequent work (Henderson & Ferreira, 1993) has confirmed an earlier finding by Lévy-Schoen (1981) that only foveal, and not peripheral processing, has this effect. Henderson gives the following account of attentional allocation. "First, a pre-attentive map of likely stimulus locations is made available to the attention allocation system. Second, stimulus locations are weighted so that attention is allocated to the stimulus location with largest weight." This has evident similarities with the salience peak selection described in sect. 2.2.3. While Henderson’s model has some parallels with our own, we are unclear what is gained by using attentional terminology since the properties assigned to attention mimic closely those of the eye itself (unique pointing direction; rapid movement from direction to the next).
Space precludes any full discussion of the effects of brain damage on eye movements. However we do discuss here results from individuals with unilateral neglect because we believe our model has the potential to throw some light on the attentional deficit present in this condition.
One consequence of unilateral parietal damage is visual neglect and visual extinction. These conditions are characterised by a failure to detect stimuli and objects located in the contralesional side of space. In addition to extinction and neglect selective impairments in eye movement control are also observed in both monkey (Lynch & McClaren, 1989) and man (Girotti et al. 1983) following parietal lesions. The manifestations of extinction and neglect may be dissociated from the eye movement disorders and are typically regarded as reflecting higher level disorders of visual attention (Posner et al. 1984, 1987) and visual awareness (Bisiach et al. 1979).
The eye movement deficits observed in patients with neglect have the following characteristics. Neglect patients are known to be generally able to make saccades following a verbal command (De Renzi, 1982). Considering visually elicited saccades, there may, in the most severe cases, be a failure to initiate a saccade to a contralesional visual stimulus; if contralesional saccades are made these are of long latency and the amplitude hypometric (Girotti, et al., 1983; Ishiai et al. 1987; Walker & Findlay, 1996; Walker et al. 1991). Patterns of small contralesional multi-stepping saccades are also observed to locate stimuli in the contralesional hemifield (Meienberg et al. 1986). In the monkey a less severe deficit is observed whereby the animal can make saccades to a contralesional stimulus, but if two targets appear simultaneously in both hemifields then an ipsilesional saccade is always made (Lynch & McClaren, 1989).
We have examined the saccades made by patients with unilateral parietal damage and visual neglect under fixation gap and overlap conditions (Walker & Findlay, 1996). All of the patients showed the normal latency reduction (gap effect) for ipsilesional saccades but none showed the normal latency increase (remote distractor effect) when a distractor appeared in their contralesional visual field. Two of the patients did not have a visual field defect and so the lack of a remote distractor latency increase cannot be attributed to a low level sensory loss explanation. We also noted that neglect patients made more contralesional saccades under the gap condition than in the overlap condition (Walker & Findlay, 1996; Walker et al. 1991). Although the increase in numbers of contralesional saccades in the gap condition appears consistent with Posner's deficit of attentional disengagement hypothesis we have cautioned against this conclusion. A consistent finding in both studies was that patients also made more ipsilesional saccades in the gap condition than in the overlap condition. Furthermore, the amplitude of the contralesional saccades remained hypometric in the gap condition and a pattern of multistepping indicative of a search strategy was also observed. Thus, the increase in contralesional saccades shown by some patients may be interpreted as reflecting an increase in a non-spatial attention caused by warning signal effects of fixation offset.
The saccadic abnormality observed in neglect can be accounted for in terms of our model with one extra assumption that at some level the spatial channels for L and R saccades are separate. Unilateral brain damage appears to result in an imbalance in the system which affects the level 3 automated processes in the spatial channel on the same side as the brain damage. More specifically it is proposed that the ipsilesional automatic peripheral detection processes (involved in orienting to contralesional stimuli) remain permanently under activated. The consequence of this under activation is two fold; firstly the salience map involved in coding saccade metrics remains permanently depressed making it unlikely that a peak will occur on the contralesional side and that a contralesional movement will be generated. Any contralesional saccades that are made will be hypometric and of long latency although such saccades are not precluded.
A further consequence of the unilateral under activation of the peripheral detection processes is a low level of activation in the fixate system following the onset of a stimulus in the contralesional hemifield. When two targets appear simultaneously in both hemifields the system will be biased to making a saccade in the ipsilesional direction by the intact movement channel. The latency of ipsilesional saccades will not be increased under bilateral target conditions due to the lack of automatic inhibitory effects which would normally be produced by the connection to the fixate system. As the response of the ipsilesional movement channel remains under activated there is little activation of the fixate system following a contralesional input.
In this article we have presented a framework for the understanding of the generation of individual saccadic eye movements. We have shown how this framework is consistent with known brain processes and have shown how certain robust experimental results can be accommodated into the framework. In various subsections of Section 4, we have highlighted points of difference between our framework and those used by other workers.
We hope our presentation serves both to review past work and to provide pointers for future directions. We have concentrated on studies analysing visually elicited saccades since a wealth of data has been obtained from these studies for which we believe are well accounted for the lower levels in our hierarchy. Our discussion of the upper levels of the hierarchy is more sketchy but we expect understanding of the processes involved at these levels to develop rapidly. At the detailed level of neural computation, plausible accounts of spatial and search selection have been discussed and we expect these to become integrated with our increasing knowledge of the multiple cortical processing streams involved in visual analysis and saccade generation.
Work on this paper was started during a visit made by the authors to the Max-Planck Institute of Psychological Research, Munich. We are grateful to the Max-Planck foundation for financial support. We are also grateful for the constructive comments of H Collewijn, D Munoz, A Wertheim and other anonymous referees.
Abrams, R. A. & Jonides, J. (1988) Programming saccadic eye movements. Journal of Experimental Psychology, Human Perception and Performance, 14, 428-443.
Allport, D. A. (1993) Attention and control: have we been asking the wrong questions? A critical review of twenty-five years. In: Attention and Performance XIV, eds. D. E. Meyer & S. Kornblum. MIT Press.
Andersen, R. A., Essick, G. K. & Siegel, R. M. (1985) Encoding of spatial location by posterior parietal neurons. Science, 230, 456-458.
Arai, K., Keller, E. L. & Edelman, J. A. (1994) Two-dimensional model of the primate saccadic system. Neural Networks, 7, 1115-1135.
Aslin, R. N. & Shea, S. L. (1987) The amplitude and angle of saccades to double-step target displacements. Vision Research, 27, 1925-1942, 1987.
Beauvillain, C., Doré, K. & Baudoin, V. (1996) The ‘centre of gravity’ of words: evidence for an effect of the word initial letters. Vision Research, 36, 589-603.
Becker, W. (1989) Metrics. In: The neurobiology of saccadic eye movements, eds. R. H. Wurtz & M. E. Goldberg. Elsevier.
Becker, W. & Jürgens, R. (1979) An analysis of the saccadic system by means of double step stimuli. Vision Research, 19, 967-983.
Becker, W. Hoehne, O. Iwase, K. & Kornhuber, H. H. (1972) Bereitschaftspotential, prämotorische Positivierung und andere Hirnpotentiale bei sakkadische Augenbewegungen. Vision Research, 12, 421-436.
Bisiach, E., Luzzatti, C., & Perani, D. (1979) Unilateral neglect, representational schema and consciousness. Brain, 102, 609-618.
Bridgeman, B., van der Heijden, A. H. C. & Velichkowsky, B. M. (1994) A theory of visual stability across saccadic eye movements. Behavioral and Brain Sciences, 17, 247-292.
Carpenter, R. H. S. (1981) Oculomotor procrastination. In: Eye movements, cognition and visual perception, eds. D. F. Fisher, R. A. Monty & J. W. Senders. Lawrence Erlbaum.
Carpenter, R. H. S. & Williams, M. L. L. (1995) Neural computation of log likelihood in control of saccadic eye movements. Nature, 377, 59-62.
Cavegn, D. (1996) Bilateral interactions in saccade programming. Experimental Brain Research, 109, 312-332.
Chelazzi, L., Muller, E. K., Duncan, J. & Desimone, R. (1993) A neural basis for visual search in inferior temporal cortex. Nature, 363, 345-347.
Coëffé, C. & O'Regan, J. K. (1987) Reducing the influence of non-target stimuli on saccade accuracy: predictability and latency effects. Vision Research, 27, 227-240.
Cohen, M. E. & Ross, L. E. (1977) Saccade latency in children and adults: effects of warning signals and target eccentricity. Journal of Experimental Child Psychology, 23, 539-549.
Coren, S. & Hoenig, P. (1972) Effect of non-target stimuli on the length of voluntary saccades. Perceptual and Motor Skills, 34, 499-508.
De Renzi, E. (1982) Disorders of space exploration and cognition. Wiley.
Desimone, R. & Duncan, J. (1995) Neural mechanisms of selective attention. Annual Review of Neuroscience, 18, 193-222.
Deubel, H. (1987) Adaptivity of gain and direction in oblique saccades. In: Eye movements: from physiology to cognition, eds. J. K. O'Regan & A. Lévy-Schoen. Elsevier/North Holland.
Deubel, H. (1995) Selective adaptation of reactive and volitional saccadic eye movements. Vision Research, 35, 3529-3540.
Deubel, H., Wolf, W. & Hauske, M. (1984) The evaluation of the oculomotor error signal. In: Theoretical and Applied Aspects of Oculomotor Research, eds. A. G. Gale & F. W. Johnson. Elsevier.
Dorris, M. C., Paré, M. & Munoz, D. P. (1997). Neuronal activity in monkey superior colliculus related to the initiation of saccadic eye movements. Journal of Neuroscience, 17, 8566-8579.
Droulez, J. & Berthoz, A. (1990) The concept of dynamic memory in sensorimotor control. In: Motor control: concepts and issues, eds. D. R. Humphrey & H. J. Freund. Wiley.
Droulez, J. & Berthoz, A. (1991) A neural network model of sensoritopic maps with predictive short-term memory properties. Proceedings of the National Academy of Sciences, U. S. A., 88, 9653-9657.
Duncan, J. (1995) Cooperating brain systems in perception and action. In : Attention and Performance XV, eds. T. Inui & J. L. McClelland. MIT Press.
Edelman, J. A, & Keller, E. L. (1996) Activity of visuomotor burst neurons in the superior colliculus accompanying express saccades. Journal of Neurophysiology, 76, 908-926.
Egeth, H. E. & Yantis, S. (1997) Visual attention : control, representation and time course. Annual Review of Psychology, 48, 269-297.
Enright, J. T. (1984) Changes in vergence mediated by saccades. Journal of Physiology, London. 350, 9-31.
Enright, J. T. (1992) The remarkable saccades of asymmetric vergence. Vision Research, 32, 2261-2276.
Erickson, R. P. (1968) Stimulus coding in topographic and non-topographic afferent modalities: on the significance of the activity of individual sensory neurons. Psychological Review, 75, 447-465.
Eriksen, C. W. & St James, J. D. (1986) Visual attention within and around the field of focal attention: a zoom lens model. Perception and Psychophysics, 40, 225-240.
Erkelens, C. J., Steinman, R. M. & Collewijn, H. (1989) Ocular vergence under natural conditions. II Gaze shifts between real targets differing in distance and direction. Proceedings of the Royal Society, London, 236B, 441-465.
Findlay, J. M. (1980) The visual stimulus for saccadic eye movements in human observers. Perception, 9, 7-20.
Findlay, J. M. (1981a) Spatial and temporal factors in the predictive generation of saccadic eye movements. Vision Research, 21, 347-354.
Findlay, J. M. (1981b) Local and global influences on saccadic eye movements. In: Eye Movements, Cognition and Visual Perception, eds. D. F. Fisher, R. A. Monty & J. W. Senders. Lawrence Erlbaum.
Findlay, J. M. (1982) Global processing for saccadic eye movements. Vision Research, 22, 1033-1045.
Findlay, J. M. (1983) Visual information for saccadic eye movements. In: Spatially oriented behavior, eds. A. Hein & M. Jeannerod. Springer-Verlag.
Findlay, J. M. (1987) Visual computation and saccadic eye movements. Spatial Vision, 2, 175-189.
Findlay, J. M. (1997) Saccade target selection during visual search. Vision Research, 37, 617-631.
Findlay, J. M. & Harris, L. R. (1984) Small saccades to double stepped targets moving in two dimensions. In: Theoretical and Applied Aspects of Oculomotor Research, eds. A. G. Gale & F. W. Johnson. Elsevier.
Findlay, J. M. & Gilchrist, I. D. (1997) Spatial scale and saccade programming, Perception, 26, 1159-1167.
Findlay, J. M. & Gilchrist, I. D, (1998) Eye guidance during visual search. In: Eye guidance while reading and while watching dynamic scenes, ed. G. Underwood. Elsevier
Findlay, J. M. & Walker, R. (1996) Visual attention and saccadic eye movements in normal human subjects and in patients with unilateral neglect. In: Visual Attention and Cognition. Advances in Psychology, Volume 116, eds. W. Zangemeister, H. S. Stiehl & C. Freska. North-Holland.
Findlay, J. M., Brogan, D. & Wenban-Smith, M. (1993) The visual signal for saccadic eye movements emphasizes visual boundaries. Perception and Psychophysics, 53, 633-641.
Fischer, B. (1987) The preparation of visually guided saccades. Reviews of Physiology, Biochemistry and Pharmacology, 106, 1-35.
Fischer, B. & Boch, R. (1983) Saccadic eye movements after extremely short reaction times in the monkey. Brain Research, 260, 21-26.
Fischer, B. & Ramsperger, E. (1984) Human express saccades: extremely short reaction times of goal directed eye movements. Experimental Brain Research, 57, 191-195.
Fischer, B. & Weber, H. (1992) Characteristics of "anti" saccades in man. Experimental Brain Research, 89, 415-424.
Fischer, B. & Weber, H. (1993) Express saccades and visual attention. Behavioral and Brain Sciences, 16, 553-610.
Fischer, B., Gezeck, S. & Huber, W. (1995) The three-loop model: a neural network for the generation of saccadic reaction times. Biological Cybernetics, 72, 185-196.
Forbes, K. & Klein, R. (1996) The magnitude of the fixation offset effect with endogenously and exogenously controlled saccade. Journal of Cognitive Neuroscience, 8, 344-352.
Fuchs, A. F., Kaneko, C. R. S. & Scudder, C. A. (1985) Brainstem control of saccadic eye movements. Annual Review of Neuroscience, 8, 307-337.
Gandhi, N. J. & Keller, E. L. (1997) Spatial distribution and discharge characteristics of superior colliculus neurons antidromically activated from the omnipause region in the monkey. Journal of Neurophysiology, 78, 2221-2225.
Girotti, F., Casazza, M., Musicco, M. & Avanzini, G. (1983) Oculomotor disorders in cortical lesions in man: the role of unilateral neglect. Neuropsychologia, 5, 543-553.
Glimcher, P. W. & Sparks, D. L. (1992) Movement selection in advance of action in the superior colliculus. Nature, 355, 542-545.
Glimcher, P. W. & Sparks, D. L. (1993) Representation of averaging saccades in the superior colliculus of the monkey. Experimental Brain Research, 95, 429-435.
Goldberg, M. E. & Segraves, M. A. (1989) The visual and frontal cortices. In : The neurobiology of saccadic eye movements, eds. R. H. Wurtz & M. E. Goldberg. Elsevier.
Gould, J. D. (1973) Eye movements during visual search and memory search. Journal of Experimental Psychology, 98, 184-195.
Guitton, D., Buchtel, H. A. & Douglas, R. M. (1985) Frontal lobe lesions in man cause difficulties in suppressing reflexive glances and in generation of goal directed saccades. Experimental Brain Research, 58, 455-472.
Hallett, P. E. (1978) Primary and secondary saccades to goals defined by instructions. Vision Research, 18, 1279-1296.
Hallett, P. E. & Adams, W. D. (1980) The predictability of saccadic latency in a novel oculomotor task. Vision Research, 20, 329-339.
Hanes, D. P. & Schall, J. D. (1996) Neural control of voluntary movement initiation. Science, 274, 427-430.
He, P. & Kowler, E. (1989) The role of location probability in the programming of saccades : implications for "center-of-gravity" tendencies. Vision Research, 29, 1165-1181.
Henderson, J. M. (1992) Visual attention and eye movement control during reading and picture viewing. In : Eye movements and visual cognition : scene perception and reading, ed. K. Rayner. Springer-Verlag.
Henderson, J. M. (1993) Visual attention and saccadic eye movements. In: Perception and Cognition. Advances in eye movement research, eds. G. d’Ydewalle & J. Van Rensbergen. Elsevier.
Henderson, J. M. & Ferreira, F. (1993) Eye movement control during reading : fixational measures reflect foveal but not parafoveal processing difficulty. Canadian Journal of Experimental Psychology - Revue Canadienne de Psychologie Expérimentale, 47, 201-221.
Heywood, S. & Churcher, J. (1980) Structure of the visual array and saccadic latency : implications for oculomotor control. Quarterly Journal of Experimental Psychology, 32, 335-341.
Hinton, G. E., McClelland, J. L. & Rumelhart, D. E. (1986) Distributed representations. In : Explorations in the microstructure of cognition, eds. D. E. Rumelhart, J. L. McClelland & the PDP Research Group. MIT Press.
Hou, R. L. & Fender, D. H. (1979) Processing of direction and magnitude information by the saccadic system. Vision Research, 19, 1421-1426.
Hyvarinen, J. (1982) Posterior parietal lobe of the primate brain. Physiological Reviews, 62, 1060-1129.
Ishiai, S., Furukawa, T., & Tsukagoshi, H. (1987) Eye-fixation patterns in homonymous hemianopia and unilateral spatial neglect. Neuropsychologia, 25, 675-679.
Jonides, J. & Yantis, S. (1988) Uniqueness of abrupt visual onset in capturing attention. Perception and Psychophysics, 43, 346-354.
Jürgens, R., Becker, W. & Kornhuber, H. H. (1981) Natural and drug-induced variations of velocity and duration of human saccadic eye movements: evidence for a control of the neural pulse generator by local feedback. Biological Cybernetics, 39, 87-96.
Jüttner, M. & Wolf, W. (1992) Occurrence of human express saccades depends on stimulus uncertainty and stimulus sequence. Experimental Brain Research, 68, 115-121.
Kingstone, A. & Klein, R. M. (1993) Visual offset facilitates saccade latency : does pre-disengagement of attention mediate this gap effect? Journal of Experimental Psychology, Human Perception and Performance, 19, 251-265.
Klein, R. M. (1988) Inhibitory tagging facilitates visual search. Nature, 324, 430-431.
Koch, C. & Ullman, S. (1985) Shifts in visual attention : towards the underlying circuitry. Human Neurobiology, 4, 219-227.
Kowler, E. (1990) The role of visual and cognitive processes in the control of eye movement. In: Eye Movements and their role in visual and cognitive processes, ed. E. Kowler. Elsevier/North-Holland.
Kowler, E. & Blaser, E. (1995) The accuracy and precision of saccades to small and large targets. Vision Research, 35, 1741-1754.
Lambert, A, J, & Sumich, A, J, (1996). Spatial orienting controlled without awareness: a semantically based implicit learning effect. Quarterly Journal of Experimental Psychology, 49A, 490-518.
Lee, C., Rohrer, W. H. & Sparks, D. L. (1988) Population coding of saccadic eye movements by neurons in the superior colliculus. Nature, 332, 357-360.
Lemij, H. G. & Collewijn, H. (1989) Differences in accuracy of human saccades between stationary and jumping targets. Vision Research, 29, 1737-1748.
Lévy-Schoen, A. (1969) Détermination et latence de la réponse oculomotrice à deux stimulus. L'Année Psychologique, 69, 373-392.
Lévy-Schoen, A. (1974) Le champ d'activité du regard : données expérimentales. L'Année Psychologique, 74, 43-66.
Lévy-Schoen, A. (1981) Flexible and or rigid control of visual scanning behaviour. In: Eye movements: cognition and visual perception, eds. D. F. Fisher, R. A. Monty & J. W. Senders. Lawrence Erlbaum.
Lynch, J. C., & McLaren, J. W. (1989) Deficits of visual attention and saccadic eye movements after lesions of parietooccipital cortex in monkeys. Journal of Neurophysiology, 61, 74-90.
Maljkovic, V. & Nakayama, K. (1994) Priming of pop-out 1. Role of features. Memory and Cognition, 22, 657-672.
Mays, L. E. & Sparks, D. L. (1980) Saccades are spatially, not retinotopically, coded. Science, 208, 1163-1165.
McIlwain, J. T. (1976) Large receptive fields and spatial transformations in the visual system. In: International Review of Physiology, Volume 10: Neurophysiology II, ed. R. Porter.
McIlwain, J. T. (1991) Distributed coding in the superior colliculus : a review. Visual Neuroscience, 6, 3-13.
Megaw, E. D. & Armstrong, W. (1973) Individual and simultaneous tracking of a step input by the normal saccadic eye movement and manual control system. Journal of Experimental Psychology, 100, 18-28.
Meienberg, O., Harrer, M. & Wehren, C. (1986) Oculographic diagnosis of hemineglect in patients with homonymous hemianopia. Journal of Neurology, 233, 97-101.
Michard, A., Têtard, C. & Lévy-Schoen, A. (1974) Attente du signal et temps de réaction oculomoteur. L'Année Psychologique, 74, 387-402.
Moschovakis, A. E. & Highstein, S. M. (1994) The anatomy and physiology of primate neurons the control rapid eye movements. Annual Review of Neuroscience, 17, 465-488.
Munoz, D. P. & Guitton, D. (1991) Control of orienting gaze shifts by the tectoreticulospinal system in the head free cat. II Sustained discharges during motor preparation and fixation. Journal of Neurophysiology, 66, 1624-1641.
Munoz, D. P. & Wurtz, R. H. (1992) Role of the rostral superior colliculus in active visual fixation and execution of express saccades. Journal of Neurophysiology, 67,1000-1002.
Munoz, D. P. & Wurtz, R. H. (1993a) Fixation cells in monkey superior colliculus. I. Characteristics of cell discharge. Journal of Neurophysiology, 70, 559-575.
Munoz, D. P. & Wurtz, R. H. (1993b) Fixation cells in monkey superior colliculus. II. Reversible activation and deactivation. Journal of Neurophysiology, 70, 576-589.
Munoz, D. P. & Wurtz, R. H. (1995a) Saccade-related activity in monkey superior colliculus. I. Characteristics of burst and build-up cells. Journal of Neurophysiology, 73, 2313-2333.
Munoz, D. P. & Wurtz, R. H. (1995b) Saccade-related activity in monkey superior colliculus. II. Spread of activity during saccades. Journal of Neurophysiology, 73, 2334-2348.
Nakayama, K. & Mackeben, M. (1989) Sustained and transient components of focal visual attention. Vision Research, 29, 1631-1647.
Norman, D. A. & Draper, S. W. eds. (1986) User centred system design. New perspectives on human-computer interaction. Lawrence Erlbaum.
Nothdurft, H. C. & Parlitz, D. (1993) Absence of express saccades to texture or motion defined targets. Vision Research, 33, 1367-1383.
Ottes, F. P., Van Gisbergen, J. A. M. & Eggermont, J. J. (1984) Metrics of saccadic responses to double stimuli : two different modes. Vision Research, 24, 1169-1179.
Ottes, F. P., Van Gisbergen, J. A. M. & Eggermont, J. J. (1985) Latency dependence of colour-based target vs. nontarget discrimination by the saccadic system. Vision Research, 25, 849-862.
Paré, M. & Guitton, D. (1994) The fixation area of cat superior colliculus : effects of electrical stimulation and direct connection with brainstem omnipause neurons, Experimental Brain Research, 101, 109-122.
Paré, M. & Munoz, D. P. (1996) Saccadic reaction time in the monkey: advanced preparation of oculomotor programs is primarily responsible for express saccade occurrence. Journal of Neurophysiology, 76, 3666-3681.
Posner, M. I. & Cohen, Y. (1984) Components of visual orienting. In: Attention & Performance X, eds. H. Bouma & D. G. Bowhuis. Lawrence Erlbaum.
Posner, M. I. & Petersen, S. E. (1990) The attention system of the human brain. Annual Review of Neuroscience, 13, 25-42.
Posner, M. I., Walker, J. A., Friedrich, F. J. & Rafal, R. D. (1984) Effects of parietal lobe injury on covert orienting of visual attention. Journal of Neuroscience, 4, 1863-1874.
Posner, M. I., Walker, J. A., Friedrich, F. A., & Rafal, R. D. (1987) How do the parietal lobes direct covert attention? Neuropsychologia, 25, 135-145.
Rafal, R. D., Calabresi, P. A., Brennan, C.W. & Sciolto, T. K. (1989) Saccade preparation inhibits reorienting to recently attended locations. Journal of Experimental Psychology, Human Perception and Performance, 15, 673-685.
Rafal, R. D., Smith, J., Krantz, J., Cohen, A. & Brennan, C. (1990) Extrageniculate vision in the hemianopic human : saccade inhibition by signals in the blind fields. Science, 250, 118-120.
Rayner, K. (1995) Eye movements and cognitive processes in reading, visual search, and scene perception. In : Eye movement research : mechanisms, processes and applications, eds. J. M. Findlay, R. Walker & R. W Kentridge. North Holland.
Rayner, K. & McConkie, G. (1976) What guides a reader's eye movements? Vision Research, 16, 829-837.
Reingold, E. & Stampe, D .(1997). Transient saccadic inhibition during reading. Poster, Ninth European Conference on Eye Movements, Ulm
Reuter-Lorenz, P. A., Hughes, H. C. & Fendrich, R. (1991) The reduction of saccadic latency by prior offset of the fixation point : an analysis of the gap effect. Perception and Psychophysics, 49, 167-175.
Reuter-Lorenz, P. A., Oonk, H. M., Barnes, L. L. & Hughes, H. C. (1995) Effects of warning signals and fixation point offsets on the latencies of pro- versus antisaccades : implications for an interpretation of the gap effect. Experimental Brain Research, 103, 287-293.
Rizzolatti, G., Camarda, R., Grupp, L. A. & Pisa, M. (1974) Inhibitory effects of remote visual stimuli on visual responses of cat superior colliculus: spatial and temporal factors. Journal of Neurophysiology, 37, 1262-1275.
Rizzolatti, G., Riggio, L. & Sheliga, B. M. (1994) Space and selective attention. In: Attention and Performance XV, eds. C. Umiltà & M. Moscovitch. MIT Press.
Roberts, R. J., Hager, L. D., & Heron, C. (1994) Prefrontal cognitive processes: working memory and inhibition in the antisaccade task. Journal of Experimental Psychology: General, 123, 374-393.
Robinson, D. A. (1975) Oculomotor control signals. In: Basic mechanisms of ocular motility and their clinical applications, eds. G. Lennestrand & P. Bach-y-Rita. Pergamon Press.
Rohrer, W. H. & Sparks, D. L. (1993) Express saccades: the effects of spatial and temporal uncertainty. Vision Research, 33, 2447-2460.
Ross, L. E. & Ross, S. M. (1980) Saccade latency and warning signals : stimulus onset, offset and change as warning events. Perception and Psychophysics, 27, 251-257
Ross, S. M. & Ross, L. E. (1981) Saccade latency and warning signals : effects of auditory and visual offset and onset. Perception and Psychophysics, 29, 429-437.
Sakata, H., Shibutani, H. & Kawano, K. (1980) Spatial properties of visual fixation neurons in posterior parietal association cortex of the monkey. Journal of Neurophysiology, 43, 1654-1672.
Saslow, M. G. (1967a) Effects of components of displacement-step stimuli upon latency for saccadic eye movement. Journal of the Optical Society of America, 57, 1024-1029.
Saslow, M. G. (1967b) Latency for saccadic eye movement. Journal of the Optical Society of America, 57, 1030-1033.
Schall, J. D. (1995) Neural basis of saccade target selection. Reviews in the Neurosciences, 6, 63-85.
Schall, J. D. & Hanes, D. P. (1993) Neural basis of target selection in frontal eye field during visual search. Nature, 366, 467-469.
Schlag-Rey, M., Schlag, J. & Dassonville, P. (1992) How the frontal eye fields impose a saccade goal on superior colliculus neurons. Journal of Neurophysiology, 67, 1003-1005.
Segraves, M. A. (1992) Activity of monkey frontal eye field neurons projecting to oculomotor regions of the pons. Journal of Neurophysiology, 69, 1880-1889.
Smit, A. C. & Van Gisbergen J, A. M. (1989) A short-latency transition in saccade dynamics during square-wave tracking and its significance for the differentiation of visually guided and predictive saccades. Experimental Brain Research, 76, 64-74.
Sparks, D. L. (1986) The neural translation of sensory signals into commands for the control of saccadic eye movements : the role of the superior colliculus. Physiological Review, 66, 118-171.
Sparks D L and Hartwich-Young R (1989). The deep layers of the superior colliculus. In : The neurobiology of saccadic eye movements, eds. R. H. Wurtz & M. E. Goldberg. Elsevier.
Sparks, D. L. & Mays, L. E. (1990) Signal transformations required for the generation of saccadic eye movements. Annual Review of Neuroscience, 13, 309-336.
Sperling, G. S. & Weichselgartner, E. (1995) Episodic theory of the dynamics of spatial attention. Psychological Review, 102, 503-532.
Sprague, J. M. (1966) Interaction of cortex and superior colliculus in the mediation of visually guided behavior in the cat. Science, 153, 1544-1547.
Tam, W. J. & Stelmach, L. B. (1993) Viewing behavior : ocular and attentional disengagement. Perception and Psychophysics, 54, 211-222.
Treisman, A. & Gelade, G. (1980) A feature integration theory of attention. Cognitive Psychology, 12, 97-136.
Treisman, A. & Sato, S. (1990) Conjunction search revisited. Journal of Experimental Psychology, Human Perception and Performance, 16, 459-478.
Tsotsos, J. K., Culhane, S. M., Wai, W. Y. K., Lai, Y., Davis, N. & Nuflo, F. (1995). Modeling visual attention via selective tuning. Artificial Intelligence, 78, 507-545.
Van Gisbergen, J. A. M. (1989) Models. In : The neurobiology of saccadic eye movements, eds. R. H. Wurtz & M. E. Goldberg. Elsevier.
Van Gisbergen, J. A. M., Gielen, S., Cox, H., Bruijns, J. & Kleine Schaars, H. (1981) Relation between metrics of saccades and stimulus trajectory in visual target tracking; implications for models of the saccadic system. In: Progress in Oculomotor Research, eds. A. F. Fuchs & W. Becker. Elsevier/North Holland,.
Van Gisbergen, J. A. M., Van Opstal, A. J. & Roebroek, J. G. H. (1987a) Stimulus induced midflight modification of saccade trajectories. In: Eye movements : from physiology to cognition, eds. J. K. O’Regan & A. Lévy-Schoen. North-Holland,.
Van Gisbergen, J. A. M., Van Opstal, A. J. & Tax, A. A. M. (1987b) Collicular ensemble coding of saccades based on vector summation. Neuroscience, 21, 541-555.
Van Opstal, A. J. & Van Gisbergen, J. A. M. (1989) A nonlinear model for collicular spatial interactions underlying the metrical properties of electrically elicited saccades. Biological Cybernetics, 60, 171-183.
Vitu, F. (1991) The existence of a centre of gravity effect during reading. Vision Research, 31, 1289-1313.
Walker, R. & Findlay, J. M. (1996) Saccadic eye movement programming in unilateral neglect. Neuropsychologia, 34, 493-508.
Walker, R., Deubel, H. & Findlay, J. M. (1997) The effect of remote distractors on saccade programming : evidence for an extended fixation zone. Journal of Neurophysiology , 78, 1108-1119.
Walker, R., Kentridge, R. W. & Findlay, J. M. (1995) Independent contributions of the orienting of attention, fixation offset and bilateral stimulation on human saccadic latencies. Experimental Brain Research, 103, 294-310.
Walker, R., Findlay, J. M., Young, A. W., & Welch, J. (1991) Disentangling neglect and hemianopia. Neuropsychologia, 29, 1019-1027.
Walker, R., Husain, M., Hodgson, T., & Kennard, C. (in press) Saccadic eye movements and working memory deficits following damage to human prefrontal cortex. Neuropsychologia.
Ward, R., Duncan, J. & Shapiro, K. (1996) The slow time course of visual attention, Cognitive Psychology, 30, 79-109.
Weber, H. & Fischer, B. (1994) Differential effects of non-target stimuli on the occurrence of express saccades in man. Vision Research, 34, 1883-1891.
Weber, H., Aiple, F., Fischer, B. & Latanov, A. (1992) Dead zone for express saccades. Experimental Brain Research, 89, 214-222.
Wenban-Smith, M. G. & Findlay, J. M. (1991) Express saccades : is there a separate population in humans ? Experimental Brain Research, 87, 218-222.
Wolfe, J. M. (1994) Guided search 2.0. A revised model of visual search. Psychonomic Bulletin and Review, 1, 202-228.
Wurtz, R. H. (1996) Vision for the control of movement. Investigative Ophthalmology and Visual Science, 37, 2131-2145.
Wurtz, R. H. & Goldberg, M. E. eds. (1989) The neurobiology of saccadic eye movements. Reviews of Oculomotor Research Volume 3. Elsevier.
Wurtz, R. H., Richmond, B. S. & Judge, S. J. (1980) Vision during saccadic eye movements. III. Visual interactions in monkey superior colliculus. Journal of Neurophysiology, 43, 1161-1181.
Yantis, S. & Hillstrom, A. P. (1994) Stimulus driven attentional capture: evidence from equiluminant visual objects. Journal of Experimental Psychology, Human Perception and Performance, 20, 95-107.
Young , L. R .& Stark, L. R. (1963) Variable feedback experiments testing a sampled data model for eye tracking movements. IEEE Transactions of the Professional Technical Group on Human Factors in Electronics, HFE-4, 38-51.
Zee, D. S., Cook, J. D., Optican, L. M., Ross, D. A. & King Engel, W. (1976) Slow saccades in spinocerebellar degeneration. Archives of Neurology, 33, 243-251.
Zingale, C. M. & Kowler, E. (1987) Planning sequences of saccades. Vision Research, 27, 1327-1341.
Zipser, D. & Andersen, R. A. (1988) A back-propagation programmed network that simulates response properties of a subset of posterior parietal neurons. Nature, 331, 679-684.