Commentary on Arbib

Word Count:
Abstract: 98
Main text: 402
References: 239
Total text: 797

Are non-speech vocalizations direct predecessors of human speech?

Andreas Rogalewski^a, Andreas Jansen^a, Ann-Freya Foerster^b, Stefan Knecht^a,c, and Caterina Breitenstein^a,c

^aDepartment of Neurology, University of Muenster, 48129 Muenster, Germany; ^bInstitute of Radiology and Nuclear Medicine, Ruhr-University of Bochum, 44789 Bochum, Germany; ^cInterdisciplinary Center of Clinical Research Muenster, 48129 Muenster, Germany

rogalewski@uni-muenster.de
anjan@uni-muenster.de
ann-freya@gmx.de
knecht@uni-muenster.de
caterina.breitenstein@uni-muenster.de

http://neurologie.uni-muenster.de/ger/mitarbeiter/rogalewski/

Abstract: We would like to add evidence for Arbib’s claim that the emergence of protospeech was not a direct transition from non-speech vocalizations to speech, but involved an intermediate stage of “manual speech gestures”. Our conclusion is based on the observations that non-speech vocal sounds – which are also existent in non human species – do not activate the premotor cortex of the language-dominant hemisphere in humans. However, linguistic-prosodic intonation contours having a speech-like structure do. This shows that only vocalizations with a linguistic component – even though lacking semantic and syntactic information - are closely linked to the manual gesture system.

The precise mechanisms of how language may have evolved are largely unknown. Based on the motor theory of speech (Liberman & Mattingly 1985), it has been proposed that language may have evolved from manual gestures along several stages, from a mirror system for grasping to a manual based communication system, to proto-speech, and finally to today’s speech and language (Arbib 2000; Corballis 2002). Arbib argues that speech did not evolve directly from a closed repertoire of alarm calls and other species-specific vocalizations, which are also exhibited by nonhuman primates. He suggests that protolanguage might build upon existing vocalizations to achieve an intermediate stage of “manual speech gestures”.

There are several lines of evidence supporting Arbib’s view. One line stems from functional imaging studies on brain correlates of linguistic and non-linguistic vocalizations in humans. Listening to speech stimuli activated a superior portion of ventral premotor cortices bilaterally (Wilson et al. 2004), indicating a close functional link between the manual gesture system and speech. Listening to vocal expressions of emotions (Morris et al, 1999) and other nonspeech vocalizations, like laughing, crying, moaning etc. (Belin et al., 2002), did not activate the “mirror neuron system” or precentral motor areas. This pattern of functional connectivity suggests that evolution did indeed proceed from non-speech vocalizations to manual gestures and from there to protospeech.

Another line of evidence stems from our own laboratory. Using transcranial magnetic stimulation (TMS) we showed that linguistic tasks, like speaking, covert reading, and listening to speech, bilaterally activate the hand motor system (Floel et al. 2003). In a subsequent combined fMRI and TMS study, we examined whether presentation of the sentence intonation contours in isolation, without additional semantic and syntactic information, suffices to activate the action-perception system. The results show that listening to variable prosodic sentence contours activated the hand motor cortex to a similar extent as listening to sentences with complete syntactical and semantic information (Rogalewski et al. 2003; Knecht et al. 2004). This implies a joint neural system for the processing of manual and linguistic-prosodic gestures. Together with the above cited data from other laboratories, this indicates that only vocalizations with a linguistic component – and not nonspeech vocalizations - are functionally linked with the manual gesture system. This is in agreement with Arbib’s proposal that language evolution proceeded from species-specific vocalizations first to manual gestures, and then from manual gestures to speech vocalizations and to a full-blown language system.

References

Arbib, M.A. (2000) The mirror system, imitation, and the evolution of language. In Nehanio, C. & Dautenhahn, K. (Eds.). Imitation in Animals and Artefacts. MIT Press, Cambridge, MA:229-280.

Belin, P., Zatorre, R.J. & Ahad, P. (2002) Human temporal-lobe response to vocal sounds. Cognitive Brain Research 13:17-26.

Corballis, M.C. (2002) From Hand to Mouth: the Origins of Language. Princeton University Press, Priceton.

Floel, A., Ellger, T., Breitenstein, C. & Knecht, S. (2003) Language perception activates the hand motor cortex: implications for motor theories of speech perception. European Journal of Neuroscience 18:704-08.

Liberman, A. M. & Mattingly, I. G. (1985) The motor theory of speech perception revised. Cognition 21:1-36.

Knecht, S., Rogalewski, A., Jansen, A., Floel, A., Foerster, A.F., Deppe, M. & Breitenstein, C. (2004) From mouth to hand: Melody of speech activates the cortical representation of the right hand. Submitted for publication.

Morris, J.S., Scott, S.K. & Dolan (1999) Saying it with feeling: neural responses to emotional vocalizations. Neuropsychologia 37:1155-1163.

Rogalewski, A., Breitenstein, C., Floel, A & Knecht, S. (2003) Prosody in spoken language activates the hand motor system: A TMS study. NeuroImage 19(2):S59.

Wilson, S. M., Saygin, A. P., Sereno, M. I., & Iacoboni, M. (2004) Listening to speech activates motor areas involved in speech production. Nat Neurosci, 7, 701-702.

Acknowledgements

Supported by the NRW Nachwuchsgruppenförderung (awarded to Stefan Knecht), by the Stiftung Neuromedizin/Neuromedical Foundation, Muenster, Germany, and by the Interdisciplinary Center of Clinical Research Muenster, Muenster, Germany.