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Pavlovian Feed-Forward Mechanisms in the Control of Social Behavior

Abstract

The conceptual and investigative tools that are brought to bear on the analysis of social behavior are expanded by integrating biological theory, control systems theory, and Pavlovian conditioning. Biological theory has focused on the costs and benefits of social behavior from ecological and evolutionary perspectives. In contrast, control systems theory is concerned with how machines achieve a particular goal or purpose. The accurate operation of a system often requires feed-forward mechanisms that adjust system performance in anticipation of future inputs. Pavlovian conditioning is ideally suited to serve this function in behavioral systems. Pavlovian mechanisms have been demonstrated in various aspects of sexual behavior, maternal lactation, and infant suckling. Pavlovian conditioning of agonistic behavior has been also reported, and Pavlovian processes may be similarly involved in social play and social grooming. In addition, several lines of evidence indicate that Pavlovian conditioning can increase the efficiency and effectiveness of social interactions, thereby improving the cost/benefit ratio. The proposed integrative approach serves to extend Pavlovian concepts beyond the traditional domain of discrete secretory and other physiological reflexes to complex real-world behavioral interactions and helps apply abstract laboratory analyses of the mechanisms of associative learning to the daily challenges animals face as they interact with one another in their natural environment.

Keywords

social behavior, biological theory, control theory, feed-forward mechanisms, learning theory, Pavlovian conditioning, aggression, sexual behavior, nursing and lactation, social play, social grooming

1. Introduction

Many of the things that animals do, they do together. This makes the analysis of social behavior a central problem in behavioral science. Our goal in this paper is to expand the conceptual and investigative tools that are used in the analysis of social behavior by integrating three different theoretical perspectives: biological theory, control systems theory, and learning theory (in the form of Pavlovian conditioning). We discuss how the integration of these three perspectives provides insights into important proximate mechanisms of social behavior that serve to increase the efficiency and effectiveness of social interactions.

The three theoretical approaches addressed in this paper have developed pretty much independently of one another, and two of the three (control theory and learning theory) have had little to say about social behavior. The biological approach has focused on ecological and genetic factors that shape social behavior but has largely ignored the role of learning or learned associations. Control systems theory developed as a discipline in engineering, and although it has been used in the analysis of some biological systems (e.g., McFarland 1971), it has not been extended to social behavior. Pavlovian conditioning theory originated in investigations of digestive physiology and since then has been applied to a variety of other areas including cardiovascular and immune functioning, placebo effects, substance abuse, ingestive behavior, and language and memory (Hollis 1997; Turkkan 1989). However, most of the research on Pavlovian conditioning has focused on the behavior of individual organisms in socially isolated laboratory settings.

Biological theories are concerned with the costs and benefits of group living, from ecological and evolutionary perspectives. An important assumption of the biological approach has been that animals engage in social interactions because such interactions bring them ecological and genetic benefits. What might be the proximate mechanisms that shape social behavior in accordance with cost/benefit considerations? We suggest that control systems theory can be used to answer that question. Control systems theory is concerned with the analysis of how machines are designed to achieve a particular goal or purpose. A particularly effective way to reduce errors in the operation of a system involves detecting the errors and then using that information to adjust the future operations of the system. However, time lags in feedback mechanisms can seriously compromise the functioning of the system. Such time lags are especially likely in biological or behavioral systems. We will describe how Pavlovian feed-forward mechanisms can facilitate efficient performance by reducing time lags in biobehavioral systems.

Pavlovian conditioning is concerned with the formation of associations. The concept of associations has been for psychology what the concept of gravity has been for physics. It is the glue that holds experience together, helping to organize sequences of behavior. Although the concept of associations dates back to at least Aristotle, the modern era in the study of associations began with Ebbinghaus, Thorndike, and Pavlov, who for the first time investigated the characteristics of associations using empirical methods. In contrast to Pavlov’s early emphasis on the conditioning of glandular physiological responses, more recent studies have extended the applicability of Pavlovian conditioning to skeletal response systems (e.g., Hearst & Jenkins 1974; Holland 1984; Timberlake et al. 1982; Tomie et al. 1989). We contend that Pavlovian concepts can be further extended to the analysis of social behavior. We will illustrate this claim by describing how Pavlovian mechanisms are involved in a number of prominent forms of social behavior (agonistic behavior, sexual behavior, lactation and nursing, play behavior, and social grooming) and how these Pavlovian mechanisms may facilitate efficient performance.

2. Biological Approaches to Social Behavior

Animal social behavior traditionally has been studied within the context of ecological and biological perspectives. These analyses have focused on the environmental and/or genetic factors associated with the formation and behavior of animal groups. Wilson (1975) defined an animal group as a "set of organisms, belonging to the same species, that remain together for a period of time interacting with one another to a distinctly greater degree than with other conspecifics" (p.585). Some defining characteristics of animal groups are limited membership, intragroup communication, enduring relationships and cooperation between group members, and periods of synchronous activity (Daeg 1980). A fundamental assumption has been that for groups to form, the current and/or historical benefits of social living have to exceed any costs or disadvantages.

2.1. Theories of Group Formation. Theoretical approaches to animal social behavior can be arranged into three broad, non-mutually exclusive categories (Slobodchikoff & Shields 1988). Ecologically-based theories focus on the impact of environmental challenges on the development and maintenance of social groupings (Crook 1964, 1966, 1970; Lack 1968). Genetically-based theories use concepts such as indirect selection and inclusive fitness to explain how social living can be adaptive (Hamilton 1964; Trivers 1985). Finally, phylogenetic hypotheses suggest that explanations of social behavior should consider the natural history of a species, because the conditions that historically promoted group living may not be operating currently (Wilson 1975).

2.1.1. Ecological Theories. Traditionally, ecologically based considerations of animal social behavior have used the comparative method to evaluate and make predictions about which types of environmental pressures favor animal groupings. This theoretical perspective suggests that the forces of natural selection have endowed animals with the ability to adapt to changes in the ecological landscape (Wrangham & Rubenstein 1986). Thus, animal groups occur because they allow individuals to better utilize or acquire certain essential or centralized resources (Crook 1972; Alexander 1974; Slobodchikoff 1984; Wittenberger & Hunt 1985).

The benefits most often associated with group living are increased foraging efficiency and improved predator defense and avoidance (Alexander 1974). Additional benefits that may accrue to group-living individuals include access to a greater array of reproductive options (Alexander 1974), protection from aggressive conspecifics (Wrangham & Rubenstein 1986), and improved thermoregulation (Wittenberger 1981). For social groups to be adaptive these advantages must outweigh the costs associated with group living (Alexander 1974; Wrangham & Rubenstein 1986).

Although the benefits that result from living in groups vary across and within species, Alexander (1974, p. 328) described the costs of sociality as "automatic and universal." Invariably, group living increases the rate of exposure to parasites and disease, and increases the level of competition for mates and for survival needs such as food and shelter (Alexander 1974). Less common costs include being more conspicuous to prey, greater risk of inbreeding, and the potential for misdirected parental care (Alexander 1974, Grier & Burk 1992).

Once animal groupings occur, the overall social organization is heavily influenced by intra-specific variables (e.g., sex and age) that affect the degree to which individuals can compete for the available resources (Wrangham & Rubenstein 1986). In larger groups, this competition often results in a stratification of the group with some animals coming to hold more favored positions while others are relegated to less privileged roles. As a result, the costs and benefits associated with social living will tend to vary between individuals and/or subsets of individuals (Alexander 1974; Dunbar 1988; Rubenstein 1975, Wrangham & Rubenstein 1986). For some group members, the costs will be greater and may include ultimate costs such as fewer or no opportunities for reproduction. For other animals, the benefits will be enhanced and may include assistance in territory and/or nest defense and in rearing of young. Thus, in addition to consideration of the factors that bring animals together, it is also important to consider how sociality is experienced at the level of the individual, and the means by which individuals can reduce the ratio of costs to benefits inherent to group living.

2.1.2. Genetic-Based Theories. Genetically-based theories also examine the evolution of social behavior from a cost/benefit perspective. However, in genetic analyses, the costs and benefits of social behavior are measured in terms of an individual’s total genetic contribution to the next generation. This total contribution includes shared genes supplied by kin. From the perspective of the group-living individual, costly forms of social behavior are those that tend to decrease the number or likelihood of personal reproductive opportunities.

A cost/benefit approach was used by Hamilton (1964) to describe the four possible outcomes of animal interaction: cooperation (when both animals benefit as a direct result of the interaction), altruism (when the animal performing the behavior loses so that the other may gain), selfishness (when an animal benefits from an altruistic act), and spite (when both animals incur a net loss). Darwin was the first of many evolutionary theorists to recognize the challenge posed by examples of cooperative and altruistic behavior (Darwin, 1859). Altruistic behavior seems paradoxical from a genetic perspective because the genes of selfish individuals should proliferate at the expense of less selfish individuals. As a result, genetically-based considerations of social behavior have often sought to explain how selection processes can favor the evolution of cooperative and unselfish forms of behavior.

A prominent explanation, provided by Hamilton (1964), suggested that animals are more likely to participate in costly forms of social behavior if those activities result in fitness benefits for themselves or a related individual. According to this view, there are two distinct evolutionary processes: direct and indirect selection (Brown & Brown 1981; Brown 1987). Direct selection operates on the variability between individuals in terms of offspring production and survival. Indirect selection operates on the variability between individuals with regard to the reproductive success of relatives. Because related individuals possess common genes, unselfish and cooperative behaviors that serve to enhance a relative’s reproductive success increase the unselfish individual’s genetic representation in the next generation. Hamilton (1964) coined the term "inclusive fitness" to describe the additive effect of these two processes on an animal’s genetic representation in the next generation. Thus, the most successful animals in terms of inclusive fitness leave many offspring and/or assist relatives and their offspring. However, because assistance provided to relatives often comes at the expense of personal reproductive pursuits, measures of inclusive fitness for some social animals are dominated by the indirect selection component.

Hamilton (1964) drew upon these concepts to develop a formula that has come to be known as "Hamilton’s rule". Hamilton’s formula is used to compare the effects of altruistic versus selfish behavioral strategies on an individual’s inclusive fitness. The evolution of altruism will be favored in situations where altruistic strategies produce higher inclusive fitness values. This general idea has been used to explain seemingly altruistic behaviors such as helping behavior in pied kingfishers (Reyer 1984), alarm-calling in Belding’s ground squirrels (Sherman 1977; 1985), and the sterile worker castes of eusocial insects (Hamilton 1964).

In more cognitively advanced species, altruistic forms of behavior may also be maintained by "reciprocal altruism" (Trivers 1971). Reciprocal altruism is essentially a delayed form of cooperation. It occurs when one animal assists another in one context and is then assisted by the same individual at a later time. Reciprocal altruism does not work in evolutionary terms if there are numerous cheaters. However, as suggested by Axelrod and Hamilton (1981), in long-lived animals that possess a memory for prior social encounters and outcomes, the advantages gained from isolated cheating episodes may be outweighed by the fitness costs accumulated during a lifetime of social interactions. Although reports of reciprocal altruism are rare, on a number of occasions, Packer (1977) observed male olive baboons form cooperative pairs to displace a dominant male. Reciprocity is possible in this species because baboons can recognize individuals and are capable of associating acts with outcome.

2.1.3. Phylogenetic Theories. Phylogenetic hypotheses focus on the evolutionary history of social species or groups. Phylogenetic hypotheses are considered when ecological and genetic cost/benefit considerations fail to provide a satisfactory explanation for a particular group structure (Slobodchikoff & Shields 1988) and/or when the focus of interest is on the historical factors or evolutionary origins of particular forms of social behavior. According to this view, a species’ current social schema may no longer be adaptive but simply a remnant of past evolutionary pressures (Wilson 1975).

2.2 The Experience of Individuals in a Social Context

Most biological treatments of animal social behavior have focused on the conditions that promote or maintain group living, without devoting much attention to the social experience of the individual. However, at some point all analyses of social behavior must consider the consequences of a social lifestyle for the individual participants. The account developed in this article focuses on the day-to-day social experience of group-living individuals as they encounter, assist, and compete with various group members. Fundamental to this approach is the idea that Pavlovian processes can provide a mechanism that adds predictability to an animal’s social experience.

An individual’s social experience is determined, in part, by the types of relationships it establishes with other group members. Social relationships, by definition, are associated with predictable behavioral exchanges (Scott 1977). The costs associated with social interaction decline as the participants become more familiar with each other. As Dunbar (1988) noted, an individual’s social behavior is "a consequence both of behavioral strategies learned by experience and of the extent to which its cognitive capacities allow it to hypothesize and extrapolate about the future behavior of the world in which it lives" (p. 183). Pavlovian conditioning allows animals to anticipate how social encounters and outcomes will unfold, and thereby contributes to the predictability of social interactions. Anticipating the outcome is especially important when the interaction is with dominant or territory-holding individuals. Because the fitness costs of social behavior can be severe in these cases, the ability to predict the outcome of the interaction should be especially helpful.

In general, a major cost of social living for individuals is increased competition for resources such as food, water, territories, and mates. Some individuals are more successful in competing for resources than others. Thus, the social pressures, opportunities, and rewards associated with group living will tend to vary between individuals and result in a social milieu unique to each group member (Alexander 1974; Dunbar 1988; Rubenstein 1975; Wrangham & Rubenstein 1986). Animals relegated to lesser social positions are forced to make the best of a bad situation. Animals of higher status reap more of the benefits inherent to group living. However, regardless of an animal’s social status or role, all animals approach social competition with the same mandate, to minimize costs relative to benefits.

3. Control Systems Theory and Pavlovian Feed-Forward Mechanisms

As we have seen, biological theories have traditionally emphasized the ultimate evolutionary factors that encourage group living. The theories have had less to say about the proximate environmental factors that are responsible for the shape and form of a particular individual’s social responses. Inanimate stimuli and stimuli provided by another animal elicit social responses and enable experienced animals to predict the occurrence, and in some cases the outcome, of impending social encounters. This ability to predict is invaluable because it enables anticipatory reactions and helps to fine tune and increase the efficiency of social interactions.

Living organisms, however, are not the only systems that benefit from foreknowledge. Engineers have long recognized that predictive functions are often necessary components in the design and proper functioning of mechanistic systems. Powerful methods have been developed in engineering for the analysis of how predictive functions facilitate system performance. In this section we review relevant aspects of systems theory and describe how those concepts, together with Pavlovian feed-forward mechanisms, can be used to analyze how predictive functions enable animals to utilize environmental resources more efficiently. The resulting model incorporates both evolutionary and environmental factors in the shaping of animal social behavior.

Systems engineering originally developed as a specialty in electrical engineering. Since then, similarities have been recognized between biological and electronic control systems, and this has led to explorations of the relationships between engineering and biology (Rosenblueth et al. 1943). The application of control theory to biological problems is based on the assumption that useful analogies can be drawn between the mechanisms of living and nonliving systems (McFarland 1971). Engineering applications of control theory are used to improve the operation of a machine that has been created to accomplish a specific purpose. Control system analysis is most useful when the machine under investigation consists of a complex interaction of multiple components, and when these components have a propensity to vary under changing environmental conditions. Social interactions also involve multiple components that vary with changing circumstances. This parallel encouraged us to explore the application of control systems theory to the analysis of social behavior.

In engineering, a system is considered to be a collection of interacting components that provides a specified system response (Dorf 1992). The system’s activities are determined by the characteristics of the individual components and by the machinery that connects those components (Vaidhyanathan 1993). Control mechanisms are necessary when a system’s output varies outside acceptable operating levels. While some behavioral variability in living systems is inevitable (and probably advantageous), excessive variability can reduce the efficiency with which animals utilize important resources in their environment. Behavioral variability is especially likely when two or more organisms interact. Therefore, biological control mechanisms that monitor and control behavioral responses may be especially important in a social context. Functionally, such control mechanisms would reduce unnecessary energy expenditure and increase the probability that an animal engages in social behaviors previously found to improve the utilization of environmental resources.

3.1. Closed Loop Feedback Control. Two fundamental types of control systems have been identified: closed-loop systems which contain feedback mechanisms, and open-loop systems which operate without feedback. Open-loop systems do not have the capacity to adjust their mode of operation. This lack of adjustment prohibits open-loop systems from compensating for errors that may occur during system functioning. Closed-loop systems, in contrast, are more effective in producing a specified output. System regulation is accomplished by tracking the output of the system and using that information to change how the system responds to future inputs (Dunderstadt et al. 1982).

Four essential components are needed to accomplish feedback regulation in nonliving systems: a transducer or controller, a monitor, a comparator, and a set of instructions that represent the appropriate or desired system performance. [Note that these are functional components. In actual control systems, many physical elements are typically required to accomplish each of these separate tasks.] The transducer is responsible for receiving the system’s input and transforming that input into the system’s output. Transducers, however, are susceptible to errors. Thus, the remaining components are needed to properly execute the transduction process. The monitor tracks the system’s output and sends this information to the comparator. The comparator then measures the actual output against a desired output value. Changes to the transducer are then undertaken to compensate for any discrepancies between the two. In this way, feedback regulation provides error control and enables the system to maintain desired operating levels.

3.2. Time Lags and Instability. Delays invariably occur between the output of a system and subsequent adjustments. Such time lags in feedback regulation can substantially reduce the effectiveness of the control mechanism and under extreme conditions may actually cause the system to malfunction. The destabilizing effects of a time lag depend on the duration of the lag and the strength or intensity of the feedback control correction (Dworkin 1993).

Consider, for example, the effects of a delay in the operation of a simple thermostat that regulates room temperature by turning on either a heating unit or a cooling unit. If the thermostat operates with a substantial time lag, it will permit the room to get too hot before activating the cooling unit. Likewise, it will permit the room to get too cold before activating the heating unit. Thus, time lags will cause increased oscillations in room temperature. Oscillation problems become especially troublesome if the feedback correction is particularly strong, for instance, if very hot air is introduced to correct for a drop in temperature and very cold air is introduced to correct for a rise in temperature. Under these conditions, delayed feedback will exacerbate the destabilizing effects of temperature fluctuations. As this example illustrates, time lags can seriously compromise the effectiveness of feedback regulation (Kalmus 1966).

3.3. Feed-Forward Mechanisms as Solutions to Time Lags. Effective mechanisms have been developed to overcome the destabilizing effects that time lags have on feedback control. Engineers have found that oscillation problems are reduced when systems contain mechanisms capable of predicting their own output errors. Such mechanisms provide regulatory systems with feed-forward control (Box & Jenkins 1970).

Accurate prediction of a future event can only be based on how similar events took place in the past. For example, a weather forecaster predicts rain not on the basis of clairvoyance but on the basis of patterns of prior meteorological events. Thus, accurate prediction or feed-forward mechanisms are possible only with the existence of some kind of memory. Memory allows feed-forward mechanisms to anticipate output errors that have occurred in the past under similar circumstances. Through feed-forward mechanisms, a system can be "corrected" before an output error actually occurs. In principle feed-forward mechanisms are more useful than feed-back mechanisms because they can reduce the destabilizing effects of time lags in feed-back regulation and because they can adjust system functioning to prevent error.

3.4. Biological Control Mechanisms. Feedback and feed-forward control have been used in explanations of a variety of different biological functions. One early application concerned the control of body movements in the fly. Holst and Mittelstaedt (1950; Mittelstaedt 1954, cited in Kalmus 1966) proposed a model of movement control in which sensory feedback from efferent organs was compared to a template of the intended movement. From this comparison, new efferent signals could be adjusted to correct for previous inaccuracies. In humans, the cerebellum appears to be involved in processing teleceptive and proprioceptive feedback in the feedforward control of muscle activation, motor learning, and posture (Smith 1996). Other recent examples of motor control systems include a neural network model with feedforward and feedback loops for the neuromuscular control of human arm movements (Stroeve 1997), and a neural network model of locomotor control in the lamprey (Jung, Kiemel & Cohen 1996; see also Jordan 1996).

Feedback control was also an integral part of Sokolov’s (1963) theory of habituation, and was applied by Baerends (1970) to explain incubation behavior in birds. In incubation, sensory feedback from sitting on a clutch of eggs is compared to an internal target value, and this comparison is then used to increase or decrease future incubation responses. Feedback and feed-forward regulation has also been frequently used in analyses of feeding and drinking. The traditional view explained feeding and drinking in terms of feedback mechanisms that tracked fluctuations in physiological parameters that were considered indices of nutritional status (McFarland 1971). However, more recently investigators have become convinced that feed-forward mechanisms based on learning are more important and more useful in the control of feeding and drinking than feed-back mechanisms (e.g., Ramsay et al. 1996).

The recent popularity of research utilizing simulated neural networks has encouraged a resurgent interest in systems theory and the concepts of feedforward and feedback control. For instance, Berger, Bassett, and Orr (1991) proposed a multi-layered neural network that describes the modulatory connections among hippocampus, basal ganglia and cerebellum involved in the modification of learned behavior. Schmajuk and DiCarlo (1992; see also Schmajuk & Moore 1988) proposed a real-time multilayered neural network of Pavlovian conditioning. Computer simulations of the model correctly predict the effects of cortical and hippocampal lesions, as well as hippocampal and medial septal activity during classical conditioning paradigms including acquisition of delay and trace conditioning, extinction, blocking, discrimination acquisition, discrimination reversal, and generalization. Errors in the network’s output are fed back to a hidden unit layer via a biologically plausible backpropagation procedure (see also Gluck & Meyers 1993; Schmajuk 1997).

3.4.1. Distinctive Features of Biological Control Systems. Although there are many functional similarities between the feedback control observed in living and nonliving systems, there are some important differences as well. For example, unlike nonliving systems, the control mechanisms of living systems must perform in the context of physiological constraints and other limiting metabolic factors. While nonliving systems function regardless of mechanistic redundancy or cumbersome system components, living systems are forced to accomplish feedback regulation using biological mechanisms pruned by environmental adaptations.

Living and nonliving control systems also differ with respect to the nature of the instructional component that dictates desired system performance. In a nonliving system, the instructions regulating the system’s output are designed by the system’s engineer to fit the demands of a specific task or environment. In contrast, the "instructions" that regulate a living system’s "output" are shaped by the forces of natural selection (Rosen 1967). In this way, biological instructional codes actually evolve in response to the specific environmental demands living systems encounter. In nonliving systems, the system’s instructions are designed to fit the environment. In living systems, specific environmental demands dictate the "design" of the instructions.

What might be the nature of the evolved instructional codes with respect to social interactions? As we have seen, traditional theories of social behavior have in common the assumption that there are specific costs and benefits associated with each particular social response. If this is true, natural selection should favor organisms that possess the biological mechanisms necessary to (a) calculate the cost/benefit ratio associated with a given social response, and (b) evaluate the calculated ratio to ensure that it is as low as possible under the extant environmental conditions. In essence, natural selection is presumed to favor individuals who are behaviorally predisposed to minimize the costs and maximize the benefits of group living. The instructional code for the regulation of social responses, therefore, should contain information necessary for organisms to seek lower cost/benefit ratios.

3.4.2. The Feedback Control of Behavior. How the concept of feedback control may be applied to the regulation of behavior is illustrated in Figure 1. Each square in the figure represents a separate system component, and the solid arrows indicate how the components are functionally connected. Inputs and outputs are depicted without squares, and open arrows show the input and output projections. Biologically important sensory input (an unconditioned stimulus or US) is initially relayed to a stimulus/response actuator. Here sensory input gives rise to behavioral output (the unconditioned response or UR). The monitor component tracks the system’s output and calculates the cost/benefit (C/B) ratio associated with the current output response. The calculated cost/benefit ratio is then sent to the comparator which also receives input from the ratio instructions component. Here the calculated ratio from the monitor is evaluated with respect to the system’s instructional code which, as outlined above, specifies the attainment of the lowest possible cost/benefit ratio. Based on this analysis, necessary and appropriate changes to the stimulus/response actuator are undertaken so that subsequent output responses result in lower cost/benefit ratios. The extent to which the transducer needs adjustment is a function of how much the calculated cost/benefit ratio can be improved (lowered) under the extant environmental conditions.

Figure 1. A closed-loop feedback control system for the regulation of behavior. Each square represents a separate system comnponent, and the solid arrows indicate how the components are functionally connected. System input and output is depicted without squares. Open arrows show the input and output projections. The stimulus/response actuator translates sensory input (unconditioned stimuli - US) into behavioral output (unconditioned responses - UR). The remaining components provide feedback control. They enable the system to track and evaluate the cost/benefit ratio associated with the current output response. This information is then used to adjust the stimulus/response actuator so that future behavioral outputs result in lower cost/benefit ratios.

3.4.3. The Feed-Forward Control of Behavior. As we have seen, a time lag between system output and subsequent transduction adjustments is detrimental to the functioning of nonliving feedback control mechanisms. Time lags are no less troublesome with respect to the feedback regulation of biological control systems, especially biological systems whose reaction speed is restricted by physiological constraints (Vaidhyanathan 1993). Further, speeding up biological feedback mechanisms may require evolutionary adaptations that are too complicated or metabolically too costly to develop. Thus, like mechanistic control systems, living organisms rely on the feed-forward control provided by memory processes.

Figure 2 shows a feed-forward mechanism added to the feedback control system depicted in Figure 1. The modified system contains a memory component that receives sensory input as well as input from the monitor and comparator components. This enables the system to remember previously encountered stimuli, the calculated cost/benefit ratio associated with the behavioral responses to those stimuli, and any compensatory adjustments that may have been made.

Incoming stimuli can now activate information previously logged in memory. Activated memories are compared to the ratio instructions, and this is used to undertake anticipatory adjustments that modify imminent behavioral outputs. Thus, memories are used to anticipate the behavioral output so that adjustments to the stimulus/response actuator are made before mistakes occur&endash; before unconditioned responses susceptible to time lag errors are performed. The anticipatory adjustments permit more efficient and effective changes in the stimulus/response actuator than would normally occur without feed-forward control.

Figure 2. A control system for the regulation of behavior that includes a feed-forward mechanism to reduce the adverse effects of time lags in feed-back regulation. Feed-forward control is gained with the addition of a memory module which stores previously experienced sensory input as well as previous comparisons and adjustments made through feedback control. The system is able to anticipate imminent behavioral output so that adjustments to the stimulus/response actuator can be undertaken before behavioral mistakes are made. This allows the system to operate more efficiently and effectively under the extant environmental conditions.

3.4.4. Pavlovian Conditioning and Feed-Forward Control. One of the most versatile and ubiquitous biological feed-forward mechanisms is Pavlovian conditioning (Hershberger 1990; Hollis 1997; Turkkan 1989). Pavlovian conditioning provides a way for animals to track the causal texture of their environment. It enables organisms to form representations of contingent relations between the events they encounter and to respond in anticipation of biologically important stimuli.

Pavlovian conditioning can result in either excitatory or inhibitory learning (Rescorla 1969). However, for the sake of simplicity, we will focus primarily on conditioned excitation. The feed-forward character of conditioned excitation is obvious when a dog salivates in response to a conditioned stimulus that usually precedes the presentation of meat powder (Pavlov 1927). The adaptive value of this type of anticipatory conditioned responding was recognized from the outset of studies of Pavlovian conditioning. Culler (1938) expressed the idea eloquently when he noted that without anticipatory conditioned responding, an organism would

"be forced to wait in every case for the [unconditioned] stimulus to arrive before beginning to meet it. The veil of the future would hang just before his eyes. Nature began long ago to push back the veil. Foresight proved to posses high survival value, and conditioning is the means by which foresight is achieved" (p. 136).

More recently, Hollis (1982, 1997) suggested that the feed-forward control made possible by Pavlovian conditioning is the primary basis for the adaptive value of excitatory conditioned responding. According to Hollis (1982), "the biological function of classically conditioned responding . . . is to enable the animal to optimize interaction with the forthcoming biologically important event" [the unconditioned stimulus] (p. 3). By being able to anticipate an unconditioned stimulus, the animal is better able to respond to it in a highly beneficial fashion.

Feed-forward Pavlovian control has been investigated extensively in physiological systems, the traditional domain of Pavlovian conditioning. A major reason for invoking Pavlovian conditioning here was to reduce time lags in feedback regulation. Dworkin (1993), for example, argued that "the conditioned reflex can be a powerful mechanism for eliminating intrinsic lags" and augmenting the effectiveness of a physiological feedback loop (p. 48). Others have suggested that Pavlovian feed-forward mechanisms effectively reduce the need for feedback regulation (Ramsay et al. 1996; Seeley et al. 1997). According to this latter perspective, it is maladaptive to rely on feedback mechanisms when feed-forward mechanisms eliminate, or at least substantially reduce, the chances of errors occurring in the first place.

Figure 3 shows how the ability to form associations augments feed-forward control. The addition of Pavlovian conditioning to the control system is accomplished by supplementing the memory component depicted in Figure 2 with an associator component. The associator receives sensory input from both a conditioned stimulus (CS) and an unconditioned stimulus (US) and forms an association between them. The resulting CS-US association enables subsequent CS encounters to activate a representation of the US. The conditioned properties of the CS are retained in memory and can be also activated in the future through the presentation of the CS by itself .

Figure 3. A behavioral control system that includes a Pavlovian feed-forward mechanism. An associator (located inside the memory component) receives sensory input in the form of conditioned and unconditioned stimuli (CS and US) and establishes an association between them. The memory component retains a representation of the association (CS-US) so that future CS presentations can activate feed-forward adjustments to the system in anticipation of the forthcoming US.

In excitatory conditioning situations, the CS typically occurs before the US. Therefore, once the CS has become conditioned and capable of activating the memory component, feed-forward control begins when the animal first perceives the CS. Thus, feed-forward control begins prior to presentation of the US. Once conditioned and registered in memory, CSs (and the US memories they activate) provide a means of anticipating necessary adjustments to the stimulus/response actuator. These "conditioned anticipatory adjustments" serve to prime the system in preparation for the forthcoming US.

4. Pavlovian Feed-Forward Mechanisms in Social Behavior

Pavlovian conditioning involves the establishment of an association between a conditioned and an unconditioned stimulus. Pavlovian conditioning readily occurs in situations where a CS reliably precedes a US. Rabbits come to blink in response to a tone that precedes mild irritation of the eye (Gormezano 1966), rats become fearful of a tone that precedes foot-shock (Kamin 1965), and hungry pigeons come to approach and peck a spot of light that reliably precedes access to grain (Brown & Jenkins 1968). Thus, Pavlovian conditioning occurs in situations where two events are experienced in a predictable order.

Social situations may be also viewed as involving predictable event sequences. A social sequence begins with fairly innocuous stimuli experienced when two animals are at a distance and just starting to take notice of one another and ends when they are close together and engaged in vigorous behavioral exchange. As an animal experiences the stimulus sequence on a number of occasions, it may learn to anticipate the terminal behavioral exchange on the basis of early cues that are predictive of the social encounter. Each participant in a recurrent social interaction can learn to predict how the interaction is likely to play out. For the sake of simplicity, we will focus on one participant at a time.

We assume that the stimuli encountered during the vigorous social exchange at the end of a social sequence are potential USs. The stimuli encountered at the beginning of the social sequence are potential CSs. The CSs may be physical or behavioral cues provided by the other animal at a distance, or environmental cues correlated with the appearance of a conspecific. As Demarest (1992) has noted, "learning about cues in the environment that predict the location of another animal is important because it may provide a mechanism for enhancing social behavior" (p. 150).

The concepts of Pavlovian conditioning may be applied to a variety of different forms of social behavior. In this section we discuss how Pavlovian concepts may be applied to the analysis of agonistic behavior, sexual behavior, suckling and lactation, play behavior, and social grooming. In some of these cases, considerable evidence has already been obtained on the role of Pavlovian conditioning. In other cases, the evidence is less extensive and therefore our discussion is more speculative.

4.1. Agonistic Behavior. Agonisitic behavior is a form of social behavior that results from intraspecific competition for desired resources such as food items, living space, resting sites, status positions, and sexual partners (Poole 1985). Agonistic behavior is also exhibited by territorial species as a means of defending one or more of these resources from neighboring territory holders or other intruders. By definition a territory is "any defended area" (Noble 1939). This defense is accomplished by display, threat, or attack (Brown 1975). Territoriality is very common among bird species, and to a lesser degree is also seen in fish and mammals (Brown 1975). Territories are classified as serving mating, nesting, or more general purposes (Brown 1975; Daeg 1980).

For those territorial species in which successful territory and nest defense is highly correlated with reproductive success (Brown 1975), the ability to predict and prepare for combat should pay fitness benefits. Animals that can predict when a conspecific will invade their territory on the basis of an antecedent environmental cue should be more successful in warding off the invasion with an effective defensive display or fighting posture than animals that encounter an intruder unexpectedly. Thus, Pavlovian feed-forward mechanisms should enhance the effectiveness of territorial defense.

The conditioning of agonistic behavior has been explored in two species of Anabantid fish, the blue gourami (Trichogaster trichopterus) and the Siamese fighting fish (Betta splendens), and in the three-spined stickleback (Gasterosteus aculeatus). Despite some species specializations, these fish exhibit a similar form of territorial and reproductive behavior. In general, males establish and defend territories during the breeding season before the arrival of females. Females choose one or more males, and lay caches of eggs in nests the males have built. The territory-holding males then fertilize the eggs and defend the nest. Reproductive success is thus highly dependent on the ability of males to acquire and defend a nest site from satellite males in search of a territory or a cache of eggs to fertilize. When the territory boundary is breached, males confront the invader with species-typical aggressive displays and threats. If the intruder does not withdraw, a fight ensues. The fight generally comes to a quick conclusion when one of the combatants adopts a submissive posture and flees.

In studies of the conditioning of agonistic behavior, the unconditioned stimulus has been an encounter with an intruding male. Studies with Siamese fighting fish and three-spined sticklebacks have used the presentation of the male subject’s mirror image to simulate an intruder (Jenkins & Rowland 1996; Thompson & Sturm 1965). Studies with the blue gourami have used visual access to another male as the US (Hollis 1990). In the native environment of the fish, the CS for agonistic conditioning may be provided by cues of the intruder at a distance or inanimate environmental events correlated with the intruder’s appearance. In the first laboratory study of agonistic conditioning, a brief electric shock was used as the CS (Adler & Hogan 1963). In subsequent experiments, visual and spatial cues served as conditioned stimuli.

Thompson and Sturm (1965) reported successful conditioning of four components of the aggressive display of Siamese fighting fish to a red or a green light CS. The conditioned responses included fin erection, undulating movements, gill cover erection, and frontal approach to the CS. Thompson and Sturm used a standard classical conditioning method in which the CS shortly preceded the US and conditioning trials were administered according to a preset schedule regardless of the subjects’ behavior. However, they only tested four subjects.

Subsequent experiments with Betta splendens focused on the frontal approach response and included larger numbers of participants. In addition, a new method was developed in which the fish encountered the CS and US by swimming into one of two tunnels (Bronstein 1986a, 1986b). With this procedure, exposures to the CS and US were determined by the behavior of the subjects. Perhaps because of the lack of experimental control over CS and US presentations, the procedure has yielded inconsistent results (Bronstein 1986a, 1986b, 1988; Demarest 1992).

Mirror-image stimulation as the US has been used more successfully in studies with male sticklebacks. Jenkins and Rowland (1996) recently demonstrated the conditioning of both approach and zigzag movements in this species. Sticklebacks have been noted to attack intruders on the basis of the red coloration of rival males (Tinbergen 1951). To see if this predisposition would influence the course of Pavlovian conditioning, Jenkins and Rowland compared red and green lights as cues in the conditioning of two groups of male sticklebacks. For one group, presentations of the red light (CS+) were paired with visual access to a "rival" male, and presentations of the green light (CS-) occurred without the US; for the other group, the green light served as the CS+ and the red light served as the CS-. The CS+ came to elicit significantly more approach and zig-zag movements than the CS- in each group. The conditioned agonistic behavior was robust and slow to extinguish. Furthermore, there was no difference in conditioned responding as a function of which colored light served as the CS+. Thus, despite their biological predisposition, stickleback males are not constrained to respond only to red as a predictor of potential conflict. These results are especially noteworthy because early ethologists believed that the aggressive displays of sticklebacks were primarily unconditioned and independent of experiential influences (Tinbergen 1951).

The classical conditioning of agonistic behavior has been investigated most extensively in studies with the blue gourami (Hollis 1984, 1990). In this research, males were first socially isolated and permitted to establish a territory. One group of subjects then received 15 conditioning trials a day for 24 days in which a 10-second red light CS was followed by 15 seconds of visual access to a rival male. A control group received the CS and US in an unpaired fashion. Males in the paired group came to show a defensive frontal display to the red light in anticipation of viewing the potential rival. Thus, the red-light CS acquired stimulus control over the species-typical aggressive posture previously elicited only by the rival male. This opportunity to anticipate the rival male also resulted in better resource defense during a post-conditioning test trial in which exposure to the CS was followed by removal of the barrier that separated the subject’s territory from the territory of the adjacent male. During the test trial, subjects in the paired group delivered more bites and tail-beatings to the adjacent male than subjects in the control group. Thus, Pavlovian conditioning acted as a feed-forward mechanism that increased defensive behavior.

The relative inefficiency of the males in the control group to mount a successful defense suggests a potential conditioned inhibition effect. Just as the light cue predicted the presence of competition for the paired males, the same cue may have predicted "no competition" for the males in the unpaired group. Consistent with this interpretation, inhibitory conditioning of aggression was confirmed in a subsequent experiment by Hollis et al. (1984).

The opportunity to anticipate the presentation of a rival allows male gouramis to meet the competition more effectively. A CS associated with a territorial intruder increases the aggressive tendencies of males and enables them to exhibit the frontal display response more quickly. Even if the rapid recruitment of the display does not ensure triumph, it may provide a preliminary advantage in territorial defense. Evidence suggests that early success in aggressive encounters can have long-term beneficial consequences. Hollis et al. (1995) tested blue gourami males twice, once right after Pavlovian conditioning and again three days later. During the first test, a majority of the males that were conditioned to anticipate the presentation of a rival successfully defended their territory, as in previous studies. Interestingly, however, the males that won their first contest were also more likely to win their second contest. This outcome was particularly noteworthy because the second contest involved a different rival male and was unsignalled for both combatants. Thus, there was a significant positive carryover effect between the two contests. Changes in androgen levels as a result of victory may have contributed to this carryover effect (Hollis et al. 1995).

4.2. Sexual Behavior. Sexual behavior contributes directly to reproductive fitness but is fraught with risks and uncertainty. Successful sexual interaction involves a delicate interplay between a male and a female in which the actions of one participant have to be carefully coordinated with the actions of its partner. An incorrect move can result in an aggressive reaction from either the potential sexual partner or another conspecific in the area. Given the sensitive and risky nature of sexual behavior, this is an area in which Pavlovian feed-forward mechanisms may be especially useful. Pavlovian mechanisms have been examined in several species, and evidence of the functional utility of such learning has been obtained as well.

4.2.1. Sexual Conditioning in the Domesticated Quail. Sexual Pavlovian conditioning has been investigated most extensively in male domesticated quail (Coturnix japonica). In the first such study, Farris (1967) reported that male Japanese quail come to perform a courtship response (strut and toe-walking) to an auditory conditioned stimulus that signals the opportunity to copulate with a female. More extensive observations in subsequent studies with visual conditioned stimuli failed to replicate this result (e.g., Domjan et al. 1986) but showed that male quail come to approach and remain near the CS. This conditioned approach response is similar to the phenomenon of sign tracking that has been extensively documented in studies with laboratory rats and pigeons conditioned with food (Hearst & Jenkins 1974; Tomie et al. 1989). Just as animals come to approach and manipulate a localized CS that is paired with food, male quail come to approach (and sometimes manipulate) a CS paired with copulatory opportunity. The approach behavior is acquired even if a control procedure is used in which the US is omitted on trials when the response occurs (Crawford & Domjan 1993). This finding indicates that the approach behavior is a Pavlovian conditioned response and does not have to be instrumentally reinforced by access to the female. Another important feature of the response is that it is directed at the CS rather than the US. The conditioned approach response occurs even if the CS is presented nearly 1 meter away from where the female is released on the conditioning trials, and moving the CS to different locations after training does not disrupt the CS tracking behavior (Burns & Domjan 1996).

Because the sexual conditioned approach response is acquired quickly and reliably, it has enabled the exploration of numerous learning phenomena in the sexual behavior system. Phenomena that have been demonstrated include acquisition and extinction (Domjan et al. 1986; Holloway & Domjan 1993a), stimulus discrimination learning (Domjan et al. 1988), blocking (Köksal et al. 1994), second-order conditioning (Crawford & Domjan 1995), trace conditioning (Akins & Domjan 1996; Burns & Domjan 1996), conditioned inhibition (Crawford & Domjan 1996), and the effects of US devaluation (Hilliard & Domjan 1995; Holloway & Domjan 1993b).

Approach to a brief stimulus that signals copulatory opportunity is analogous to focal search behavior in foraging for food&endash; search behavior limited to a specific area where the US is likely to be found. This type of conditioned response is observed when the CS-US interval used during the conditioning trials is of moderate duration. If the CS-US interval is increased substantially (from 1 min to 20 min, for example), nondirected locomotion rather than focal search develops as the conditioned response (Akins et al. 1994). This nondirected locomotor behavior is analogous to general search behavior in foraging for food. General search behavior tends to predominate when the US is expected but not imminently (Timberlake & Lucas 1989).

Under other circumstances, the sexual conditioned response may include attempts to copulate with the conditioned stimulus. This occurs if a very short CS-US interval is used and the CS is an object that male quail can grab, mount, and contact with their cloaca. The conditioning of copulatory behavior is also facilitated by incorporating into the CS some of the species typical features of a female quail. This can be done, for example, by adding a taxidermically prepared head and some of the plumage of a female to the CS object (Cusato & Domjan 1998; Domjan et al. 1992b).

Contextual cues can also serve as conditioned stimuli in Pavlovian sexual conditioning. However, the mode of action of conditioned contextual cues differs a bit from the mode of action of discrete, localizable stimuli. As has been found in more conventional learning paradigms (e.g., Bouton & Swartzentruber 1986; Grahame et al. 1990 ), contextual cues can "set the occasion" for the signal value of discrete conditioned stimuli (Domjan et al. 1992a). Conditioned contextual cues also increase the responsiveness of males to female cues. Males spend more time near a window through which they can see females if they are tested in a sexually conditioned context rather than a nonsexual context (Domjan et al. 1992a). They are also more likely to approach and copulate with a terrycloth object that includes a taxidermically prepared head and neck of a female in a context that has become associated with copulatory opportunity (Domjan et al. 1989). Such context-induced responsivity to female cues is particularly interesting because it is evident after a single conditioning trial (Hilliard et al. 1997).

4.2.2. Sexual Conditioning in the Fruit Fly. A sexual learning effect that appears to involve Pavlovian conditioning has also been observed in the fruit fly (Drosophila melanogaster). However, in this case the phenomenon results in the suppression rather than facilitation of male courtship behavior. Recently-mated female drosophila secrete a pheromone that acts as an unconditioned stimulus that inhibits male courtship behavior (Tompkins & Hall 1981; Tompkins et al. 1983). Experience of the inhibitory pheromone in connection with other features of a female fly results in suppression of courtship directed at virgin females (Siegel & Hall 1979). The conditioned stimulus can also be provided by a mutant male. Presentation of the inhibitory pheromone in combination with exposure to mutant males results in suppression of courtship directed at mutant males (Tompkins et al. 1983). For the conditioning effect to occur, the CS and US have to be presented at the same time. Following one with the other does not produce the effect. Exposure to the inhibitory pheromone by itself (a US-alone control procedure) or exposure to a virgin female without the pheromone (a CS-alone control procedure) also fails to result in courtship suppression (Tompkins et al. 1983).

4.2.3. Sexual Conditioning in a Fish Species. Sexual conditioning has also been investigated in a fish species, the blue gourami (Trichogaster trichopterus) (Hollis et al. 1989). In this study, the conditioned stimulus was the presentation of a red light, and the unconditioned stimulus was visual access to a female. For one group of males, each presentation of the CS was followed immediately by the US. For another group, the CS and US presentations occurred unpaired. As training progressed, subjects in the paired group came to perform an anticipatory frontal display when the CS was presented and showed significantly more courtship appeasement responses when they were given access to a female.

4.2.4. Sexual Conditioning in Small Mammals. A sexual conditioning effect has been identified in the house mouse that involves ultrasound vocalizations in males in response to the odor of female urine (Dizinno et al. 1978). Female urine appears to have two components (Sipos et al. 1992). One is an unstable volatile substance that elicits ultrasound vocalizations in male mice as an unconditioned response. This volatile component quickly becomes degraded after the urine is voided and loses its effectiveness. The second component of female urine is stable over a longer period and is less volatile, but it does not elicit male ultrasound vocalizations unconditionally. Rather, the stable component of the urine comes to elicit vocalizations by virtue of being associated with the unstable component.

Conditioning of male ultrasound vocalizations typically has been accomplished by having males copulate with a female and thereby encounter both the CS and US features of the female urine (Dizinno et al. 1978). Studies with females that presumably provided different scents (hypophysectomized females vs. normal females) have indicated that the learning can be specific to the odor that is encountered during copulatory experience (Maggio et al. 1983). Evidence is also available indicating that conditioned vocalizations can come to be elicited to some extent by arbitrary odors encountered during copulation (Nyby et al. 1978).

Sexual conditioning has been investigated in laboratory rats by placing males in a distinctive plastic tub for 10 minutes before moving them to a copulation arena in which they encountered a sexually receptive female (Zamble et al. 1985). After as few as 8 conditioning trials, exposure to the conditioned stimulus reduces the latency of males to ejaculate when they are allowed to copulate with a female. Zamble and his associates have demonstrated numerous conditioning phenomena in this paradigm, including acquisition, extinction, latent inhibition, and second-order conditioning (Zamble et al 1985; Zamble et al. 1986; see also Cutmore & Zamble 1988).

Sexual conditioning effects have also been demonstrated in male Mongolian gerbils (Meriones unguiculatus) that have established a pair-bond. In these studies a compound olfactory/spatial cue served as the CS. The CS was paired with access to the subject’s pair-mate during the post-partum estrus period of the female (Villarreal & Domjan 1997). Conditioning decreased the latency to approached the CS and increased time spent near it.

4.2.5. Sexual Conditioning of Females. Much less evidence is available on the sexual conditioning of females than males. Hollis et al. (1989) observed conditioned frontal displays in both male and female gourami. However, only the conditioned males showed increased courtship appeasement responses during a mating test conducted after the conditioning trials. In studies with Japanese quail, Gutiérrez and Domjan (1997) found that females are much less likely than males to approach and remain near a CS that is paired with the presentation of a sexual partner. In contrast to this result, both female and male Mongolian gerbils have been found to approach and remain near a sexually conditioned olfactory/spatial CS (Villarreal & Domjan 1997). The comparable results obtained with male and female gerbils may be related to the fact that unlike Japanese quail, gerbils form pair bonds. However, other alternatives also require careful consideration (see Villarreal & Domjan 1997, for a more detailed discussion).

Sexual experience has also been found to influence the sexual behavior of female rats and mice. Oldenburger, Everitt, and de Jonge (1992) found that female rats develop a preference for a distinctive compartment in which they previously copulated with males. Caroum and Bronson (1971) reported that the preference of female mice for male preputial gland extract is increased by copulatory experience with males.

4.2.6. The Feed-Forward Character of Sexual Conditioning. If Pavlovian sexual conditioning acts as a feed-forward mechanism to optimize responses to the unconditioned stimulus, then conditioning should facilitate copulatory interactions between males and females. Several different lines of evidence support this prediction. As was noted above, Zamble et al. (1985; see also Zamble et al. 1986) reported that male rats achieve ejaculation faster when given a chance to copulate with a female after exposure to a sexually conditioned stimulus. In related observations, Domjan et al. (1986) reported that sexually conditioned male quail initiated copulation faster after exposure to the CS than subjects in a control group for whom the CS was not predictive of copulatory opportunity.

Sexual conditioning can also facilitate how females interact with males. A prominent aspect of sexual receptivity in female quail is squatting in response to the presence of a male (Noble 1972). Gutiérrez and Domjan (1997) found that the presentation of a sexual CS increases the duration of squatting. This outcome demonstrates that, as with males, a Pavlovian sexual CS facilitates the sexual behavior of female quail.

A sexually conditioned stimulus can also influence the outcome of sexual competition. Gutiérrez and Domjan (1996) tested pairs of male quail in a 72 m² outdoor aviary. A female was released at one end of the aviary after presentation of a localized auditory cue. The auditory cue was a sexually conditioned stimulus for one of the males but not the other. The point of interest was whether the male that copulated with the female first was the one that received the sexual CS on that trial. The results indicated that this was indeed the case. In 15 of 17 competition trials, the winner was the male that could anticipate release of the female because of the sexually conditioned CS.

In studies with blue gourami fish, Hollis et al. (1989) found that exposure to a conditioned sexual stimulus reduces aggressive displays and facilitates the emergence of courtship behavior when the male is permitted to interact with a female. The facilitation of courtship and sexual behavior is highly persistent and is manifest in decreased aggression, increased nest building, decreased latency to spawn, and increased clasping (Hollis et al. 1997). In addition, and most importantly, following exposure to a sexually conditioned stimulus, gouramis produce far more offspring than they do if their sexual interactions are not signaled by a CS (Hollis et al. 1997).

Other evidence indicates that exposure to a sexually conditioned stimulus can facilitate physiological reflexes related to reproduction. Graham and Desjardins (1980) demonstrated that a sexually conditioned stimulus triggers the release of leuteinizing hormone and testosterone in rats. Exposure to a sexually conditioned stimulus has been also observed to stimulate the release of sperm in quail (Domjan et al. 1998). Male quail that were exposed to a sexually conditioned stimulus released greater volumes of semen and greater numbers of spermatozoa than control subjects. However, conditioning did not alter other aspects of the sperm, such as their motility, concentration, and viability.

4.3. Conditioned Maternal and Infant Behavior. Variations in infant survival are directly related to maternal responsiveness (Fleming et al. 1996), which is often a function of experience. For example, exposure to pup cues increases the maternal responsiveness of female mice (Noirot 1972). In addition, maternal experience has been shown to improve pup retrieval behavior (Carlier & Noirot 1965; Fleming & Rosenblatt 1974).

4.3.1. Conditioning of Maternal Behavior. The conditioning of maternal behavior has been explored extensively in sheep and rats. Parental behavior in sheep involves special problems because adult females and their suckling young form flocks in which newborn lambs can easily come in contact with nursing females that are not their mother. Nursing females that accept alien young might not have sufficient milk for their own offspring, thus reducing their reproductive fitness (Holmes 1990). Females rapidly learn the unique olfactory features of their own offspring. The learning appears to take place during parturition, and is facilitated by the mother moving away from the herd just before a lamb is born.

The mother is highly responsive to the amniotic fluid that is ejected during the birth process, continually sniffing and licking it, as well as the ground with which the fluid comes in contact. When the lamb is born, the mother vigorously licks the lamb until it is clean of amniotic fluid. This seems to be critical to accepting the lamb for nursing. Washing neonates (which presumably reduces the odor of the amniotic fluid) reduces maternal licking behavior and maternal acceptance (Levy & Poindron 1987). On the other hand, maternal responsiveness can be induced by covering lambs in jackets soaked with amniotic fluid (Basiouni & Gonyou 1988).

Once maternal responsiveness has been established through contact with amniotic fluid, maternal acceptance comes to be elicited by the unique olfactory cues of only that mother’s lamb (Poindron et al. 1993), presumably because these cues have become associated with the amniotic fluid. Studies attempting to identify the exact source and composition of these olfactory cues (Alexander 1978; Alexander & Stevens 1982), and attempts to disrupt the development of responsiveness to a lamb’s unique scent by introducing artificial odors during the learning phase (Levy et al. 1996), have not been successful. Nevertheless, the available evidence is consistent with the suggestion that individual lamb odors serve as conditioned stimuli that quickly become associated with amniotic fluid, a biologically significant stimulus inherently meaningful to parturient ewes. The individual lamb odors then control maternal acceptance. However, additional studies employing unpaired controls need to be undertaken to substantiate this interpretation.

Olfactory associative learning has also been implicated in the maternal behavior of rats. Bauer (1993) investigated the malleability of preferences for nest and pup odors in first-time mothers. Rat mothers were capable of learning a novel nest odor (CS) if that odor was paired with normal odors from the mother’s original bedding (US). This novel odor was then shown to facilitate the identification of the nest, as well as pups that had been placed in the nest (see also Beach & Jaynes 1956). Further, the mothers retained the conditioned preferences through their second litter. These results clearly show that associative learning helps dams identify their nests and their offspring&endash; abilities that are highly correlated with reproductive fitness.

4.3.2. Conditioning of Maternal Neuroendocrine Responses. Maternal lactation involves milk let-down and milk ejection. Both are mediated by neuroendocrine mechanisms triggered unconditionally by suckling of the nipple (McNeilly & McNeilly 1978). Suckling causes the release of oxytocin from the posterior pituitary gland. Oxytocin (OT) then travels through the bloodstream to the breast and facilitates the movement of milk into larger mammary ducts, causing milk let-down. The milk ejection reflex, on the other hand, is controlled by prolactin release from the anterior pituitary. Evidence from sheep, rats, and humans suggests that the milk let-down reflex and the milk ejection reflex are both susceptible to Pavlovian conditioning.

Fuchs et al. (1987) measured fluctuations in plasma OT levels in ewes and found that external cues provided by lambs came to elicit OT release as a result of the association of these cues with suckling. Lambs were separated from their mothers after birth, except for periodic feedings. OT concentrations rose significantly due to actual suckling 86% of the time, indicating a clear unconditioned response. After two days of testing, OT concentrations also rose significantly from baseline levels when a lamb was introduced into its mother’s pen. The fact that OT levels increased in response to the placement of the lamb into the mother’s pen only after the external cues of the lamb had been paired with suckling suggests that this increase was a conditioned response. However, this Pavlovian interpretation must await further testing because the external lamb cues were never presented in an unpaired fashion with suckling bouts.

Exteroceptive stimuli have been found to affect prolactin release as well in a number of species (mice, rats, goats, cows, pigeons, doves). Investigations have explored the role of external pup cues in eliciting and maintaining lactation in rat mothers during different stages of nursing (see Grosvenor & Mena 1974, for a review). During the first seven days postpartum, prolactin is released primarily as an unconditioned response to suckling. However, by day 14 postpartum, prolactin release also comes to be stimulated by the visual, olfactory, and auditory cues provided by the pups that reliably precede suckling. Continued nursing from day 14 to day 21 results in broad stimulus generalization of this effect. By day 21, increases in prolactin are elicited not only by the dam’s own pups but also by cues from other lactating mother-pup pairs and general contextual cues from the animal room environment (Grosvenor & Mena 1972). In addition, a new inhibitory response to pup cues develops as the pups reach the age of weaning. By day 21, the pups have an inhibitory influence upon the action of prolactin in stimulating milk secretion (Grosvenor et al. 1977; Grosvenor & Mena 1974). Pup cues still elicit prolactin release but they also come to activate an inhibitory process that reduces the effectiveness of prolactin in stimulating milk secretion.

4.3.3. Conditioning of Lactation in Humans. Learning mechanisms also contribute to the regulation of human maternal feeding responses. Psychological factors related to the maternal milk ejection reflex were first reported by Waller (1938), who documented that milk ejection can be inhibited by embarrassment or elicited by the mother simply thinking of feeding (Jelliffe 1978). Evidence suggestive of conditioned oxytocin release was obtained by McNeilly et al. (1983), who measured oxytocin release during early and later stages of lactation (within 1 week postpartum and 4-11 weeks postpartum, respectively). OT samples were obtained from mothers in the presence of their own babies 15 min before suckling started, and at 1-min intervals during the subsequent feeding. OT levels increased in all participants as a result of infant suckling. Half of the mothers also showed OT increases upon hearing their baby cry before the start of suckling. The remaining mothers showed OT increases either while preparing to feed or after seeing the baby become restless in expectation of feeding. Consistent with a conditioning interpretation, these effects were most consistent 4-11 weeks postpartum, after numerous pairings of pre-feeding cues with suckling.

Caldeyro-Barcia (1969) was able to study conditioned milk-ejection by measuring intramammary pressure. Polyethylene tubes connected to pressure transducers were surgically implanted into the mammary ducts of lactating women. The milk-ejection reflex was then quantitatively measured in the breast opposite the one being suckled. By far the most effective means of eliciting the reflex was suckling by the infant. However, intramammary pressure also increased in response to seeing the baby or hearing the baby cry in an adjacent room (Caldeyro-Barcia 1969). This conditioned intramammary pressure response was nearly as intense as the response to actual suckling.

Further evidence that mothers can be conditioned to respond to cry stimuli was obtained by measuring changes in mammary skin temperature in response to hearing the recorded cries of a baby (Lind et al. 1971). After the cry stimulus was perceived, 85% of the lactating mothers showed significant increases in mammary skin temperature. No thermal increases were recorded in a control group of nursing mothers that were tested in the absence of the cry stimulus.

4.3.4. Conditioning of Nursing in Neonates. Learning mechanisms are also involved in regulating the nursing responses of neonates. Rat mothers elicit nipple attachment by placing amniotic fluid on their nipples (Teicher & Blass 1977; Blass 1990). Newborn pups locate the nipple by tracking the odor of the amniotic fluid. This mechanism shows considerable plasticity. Penderson and Blass (1982) injected either an artificial scent or saline into the amniotic sacs of 19-day-old rat fetuses and delivered the neonates surgically on day 21 of gestation. They then tested for nipple attachment following angiogenital stimulation of the pups in the presence of the artificial scent. Rat pups were given a choice of nipples treated or untreated with the artificial odor. Only those pups that were exposed to the artificial scent before and after parturition successfully attached to the nipples treated with this odor. Thus, nipple attachment was determined by the artificial olfactory manipulation (Fillion & Blass 1986a). The artificial scent also affected later sexual behavior. The presence of the odor on a sexually receptive female decreased the ejaculation latencies of male rats that developed a preference for the artificial scent as neonates (Fillion & Blass 1986b).

Evidence of learning in the control of suckling behavior is also evident from studies of human infants. Human infants are differentially responsive to their own mother’s odors. Specific odor cues of the mother may facilitate early mother-infant attachment (Porter et al. 1988) or may help the infants locate the nipple for feeding (Blass & Teicher 1980). Human neonates that have been breast-fed differentially prefer the odors of their own mother’s compared to the odors of unfamiliar lactating females. Bottle-fed neonates do not show such a discrimination (Cernoch & Porter 1985). Preferences for these odors likely develop as a result of the odors being paired with the unconditioned stimuli provided by suckling.

Nursing responses can also become conditioned to tactile and auditory cues. Using a sucrose solution in the mouth as the US, head-mouth orientation was successfully conditioned in infants to a number of artificial CSs including stroking of the forehead and the clicking of castanets (Blass 1990; see also Blass et al. 1984). Presenting the CS without the US after CS-US pairings resulted in crying in 6 out of 8 infant participants. This type of frustration response is similar to the distress vocalizations of rat pups when their reward expectancy has been violated (Amsel et al. 1977; Blass 1990).

4.4 Play Behavior. In contrast to the forms of social behavior reviewed in the above sections, explicit studies of Pavlovian conditioning have not been carried out with play behavior. However, the available evidence is consistent with the suggestion that Pavlovian feed-forward processes may also facilitate playful interactions.

By definition, the word "play" suggests behavior performed for reasons other than necessity. Play behavior typically occurs in pre-adults, presumably for self-stimulation or amusement. However, many examples of play behavior mimic in some way responses needed for survival. If nothing else, an animal’s play behavior increases motor activity, facilitating muscle development and coordination.

While play behavior has been documented in a variety of vertebrate species, including birds (Ortega & Bekoff 1987), it is perhaps most common in mammals, especially canids and primates (Poole 1985). The earliest forms of play are characterized by exploration and self-discovery as the young animal begins to stray from the mother and interact with the environment (Harlow & Harlow 1965). If there is a peer base, the opportunity for interaction with conspecifics becomes available to the developing animal, and this provides the opportunity for playful interactions (Poole 1985). Harlow and Harlow (1965) described the development of a "peer affectional" system in young primates that includes a stage of interactive play, followed by a stage of more aggressive play in which the juvenile learns its place in the social order.

The ubiquitous nature of play behavior among mammals suggests that it had adaptive value during the course of mammalian evolution (Poirier & Smith 1974). Baldwin and Baldwin (1977) identified at least 30 possible functions for play and exploratory behavior. Common to many of these are learning opportunities that arise from environmental and peer interactions. For instance, it has been proposed that play provides reinforcement in the form of sensory stimulation as animals seek to obtain optimum levels of arousal (Baldwin & Baldwin 1977). Consistent with this hypothesis, the opportunity to engage in social play has been successfully used as a reinforcer for maze learning in rats (Humphreys & Einon 1981), and chimps will manipulate a lever for access to a human play partner (Mason et al. 1962).

If the opportunity for social contact and play can serve as a reinforcer, then the social play partner, for our purposes, can be considered an unconditioned stimulus. This social US occurs in some context and in association with environmental and behavioral signals. These contextual and behavioral signals, through their association with the US, may acquire predictive value and come to control conditioned responses relevant to play behavior. Consistent with this scenario, social play becomes more efficient with practice (Poole 1985). In addition, Poirier and Smith (1974) noted that mammalian species with the greatest capacity for learning also show the greatest propensity for play behavior.

Juveniles may acquire preferred play partners through associative processes. Positive and negative reinforcement will become differentially associated with various peers through repeated social contact. The contextual and behavioral signals that occur in conjunction with these bouts of peer contact could become associated with the reinforcement that follows the signal. Bekoff (1974, 1975) has identified such behavioral signals in the playful interactions of canids. For instance, coyotes (Canis latrans) attempting to solicit a playful interaction often adopt a "play bow" posture, crouching on their forelegs while elevating their hindlegs. In laboratory tests, 90% of successful playful interactions were preceded by such play signals. A high correlation was also found between those signals that were successful in eliciting playful interactions and those that were actually used (Bekoff 1974). Play signals have also been shown to clarify playful intentions when the behavioral intention of the soliciting partner is relatively ambiguous (Bekoff 1995). Other signals found to be temporally correlated with play behavior include the "play pounce" and "play face" in canids (Bekoff 1975; Fox 1970) and the primate "play face" (Chevalier-Skolnikoff 1974; van Hooff 1967).

Even if playfully intended, some play behaviors have the potential of inflicting injury on the unwitting playmate (Poole 1985). Signals that precede a playful interaction may acquire predictive value and assist animals in approaching positive play experiences and avoiding negative ones with animals that are likely to respond too aggressively. Learning to predict the form of the forthcoming play episode (wrestling, chasing, pouncing, biting) may also allow young animals to better prepare for the impending interaction and engage in more complex and satisfying forms of play. Thus, learning may decrease the potential costs of finding willing and compatible play partners and increase the effectiveness of the play behavior.

4.5. Social Grooming. Another form of social behavior prominent in various species is grooming. When grooming behavior occurs in a social context it is termed mutual grooming, allogrooming, or social grooming. Social grooming is the act of cleaning a conspecific’s fur, pelage, or skin. In birds a functionally similar form of this behavior is called social preening. However, grooming as a form of social behavior has been best documented in primates (Sparks 1967; see also Bernstein & Mason 1963; Lindburg 1973; Oki & Maeda 1973; Rosenblum et al. 1966; Sade 1965; Yerkes 1933), and is believed to serve various social and group functions (Carpenter 1942; Lindburg 1973; Sade 1965; Terry 1970; Washburn & DeVore 1961; Yerkes 1933). The importance of social grooming for some primate societies is evident in the amount of time spent in daily allogrooming activities (Bernstein & Mason 1963; Lindburg 1973; Southwick 1967). The act of grooming and being groomed may have reward properties for the participants (Lindburg 1973; Marler 1965; Yerkes 1933). If social grooming is a rewarding activity, then grooming partners can be characterized as social contact USs that are potentially available for Pavlovian conditioning. In this way social grooming is similar to social play.

In Lindburg’s (1973) observations of Rhesus macaques, bouts of social grooming were among the first and last activities of the day when the groups’ food or sleep needs had been satisfied. This suggests that the environmental context in which social grooming is most commonly displayed is predictable. The predictability of social grooming suggests that it should be amenable to Pavlovian conditioning. As a regular occurrence in a common context, grooming bouts with another individual may constitute discrete learning trials. These learning episodes may promote the formation of associations between environmental stimuli and preferred grooming partners.

Allogrooming may be most rewarding when the participants can anticipate the outcome and nature of the imminent interaction. Inherent to the act of being groomed is a relaxed posture and weakened defense that, in the wrong context or with the wrong conspecific, could have negative or injurious consequences. Presumably, a certain level of confidence between grooming partners must develop before grooming can acquire the properties that make it reinforcing. Because social contact is risky when the results of close proximity are unpredictable, social animals should come equipped to associate contextual and behavioral cues with both pleasant and aversive social outcomes. These associations would serve to increase the frequency of pleasant social experiences and decrease the frequency of unpleasant ones. In this way animals can gain greater control over the costs and benefits of social interactions such as grooming. Thus, predictability would appear to be important in the formation of stable grooming relationships, and Pavlovian associations are likely to be the means by which these relationships can acquire predictive properties. Or, as Lindburg (1973) put it, "Though it has not been experimentally tested, conditioning and learning might be essential in making the grooming preferences among group members specific" (p. 143).

The degree and rate of social grooming within a primate group varies intraspecifically according to the age, status, and sex of an individual (Lindburg 1973; Oki & Maeda 1973). These individual attributes probably serve as biological constraints that, in part, determine which group members can establish amicable grooming relationships. Not every group member is considered a potential grooming partner. For instance, in matriarchal primate societies same-sex allogrooming relationships are generally the domain of adult females (Lindburg 1973; Oki & Maeda 1973). The unrelated adult males in these societies may not be capable of perceiving other males as anything other than potential aggressors because the behavioral costs of doing so are too great. Thus, individual differences, when coupled with the contextual constraints discussed above, effectively limit the range of potential CSs available for association with the act of allogrooming. This enhanced specificity increases the likelihood that for any one animal only a few select individuals, or class of individuals, will serve as USs for association with the behavioral and environmental cues available to signal satisfactory grooming interactions.

5. Conclusion

Animal social behavior has been analyzed traditionally within the context of biological perspectives that emphasize ecological and genetic benefits. Presumably evolutionary processes have shaped social behavior so as to increase its benefits relative to costs. However, the proximate mechanisms that increase the utility of social behavior have not been specified. How systems function to achieve a particular goal or purpose has been analyzed within the context of control systems theory. Those considerations have indicated that feed-forward mechanisms can significantly improve system functioning. In behavioral systems, a prominent feed-forward mechanism is Pavlovian conditioning. Therefore, we explored the role of Pavlovian conditioning in several forms of social behavior.

Pavlovian conditioning of social behavior has been investigated most extensively in studies of sexual behavior, maternal lactation, and infant suckling. However, clear demonstrations of Pavlovian conditioning are also available for agonistic behavior, and Pavlovian processes may be similarly involved in social play and social grooming. In addition, several lines of evidence indicate that associative learning can increase the efficiency and effectiveness of these social interactions. Pavlovian conditioning has been shown to improve defensive behavior in the blue gourami, an Anabantid fish. It also has been shown to facilitate courtship and reproductive behavior in the blue gourami. Other evidence indicates Pavlovian conditioning can decrease the latency of copulation and stimulate the release of sex hormones in male rats. In quail, Pavloivan conditioning has been shown to increase the sexual receptivity of both males and females, increase the success of males in sexual competition, and facilitate the release of sperm. Pavlovian conditioning also has been shown to facilitate maternal neurohormonal responses involved in milk let-down and milk secretion and improve the efficiency of infant suckling in humans. Associative processes also have been implicated in mother-infant attachment in sheep.

The available evidence encourages us to propose that all social interactions can be profitably analyzed from the perspective of Pavlovian conditioning. It is our contention that Pavlovian feed-forward mechanisms can contribute significantly to the efficiency of social behavior. We further contend that this contribution is best understood from a perspective that integrates Pavlovian processes, biological theory, and concepts from control systems theory. Based on these assumptions, we predict that all social behavior will be more efficient and effective in situations where animals are able to use cues provided by the inanimate and social environment to predict how a social interaction will unfold. Conversely, social behavior will be less effective in situations that lack relevant social conditioned stimuli.

In principle our predictions are not tautological. Pavlovian conditioning need not occur in all social situations, and the presence of a Pavlovian CS need not increase the efficiency and efficacy of all social interactions. We are not aware of data inconsistent with our predictions. However, given the diversity of animal species and the diversity of forms of animal social behavior, the available evidence of Pavlovian control of social behavior is severely limited. Much work remains to extend this approach to other species and response systems.

The extension of Pavlovian concepts to the analysis of social behavior provides a number of advantages. First, the Pavlovian perspective provides a framework for the study of proximate mechanisms of social behavior, by focusing on the stimuli that predictably occur in sequential social interactions. This emphasis on proximate mechanisms complements biological perspectives that have focused on ultimate factors that shape social behavior. Second, our extension of Pavlovian concepts helps integrate biological and learning approaches to the analysis of social behavior. This integration is achieved by using control systems theory to show that Pavlovian feed-forward mechanisms can increase the benefits of social behavior relative to its costs. Third, the use of control systems theory in combination with Pavlovian conditioning shows how memory mechanisms are involved in the shaping of effective social behavior. Fourth, the Pavlovian approach makes clear predictions about circumstances in which the efficiency and effectiveness of social behavior will be enhanced, and circumstances in which such effects will not be observed. Fifth, our analysis serves to extend Pavlovian concepts beyond the traditional domain of discrete secretory and other physiological reflexes to complex real-world behavioral interactions. This helps apply abstract laboratory analyses of the mechanisms of associative learning to the daily challenges animals face as they interact with one another in their natural environment.

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