Cover not available
Part of
How the Brain Got Language – Towards a New Road Map
Edited by Michael A. Arbib
[Benjamins Current Topics 112] 2020
► pp. 70–85

Voice, gesture and working memory in the emergence of speech

| Pontificia Universidad Católica de Chile

Language and speech depend on a relatively well defined neural circuitry, located predominantly in the left hemisphere. In this article, I discuss the origin of the speech circuit in early humans, as an expansion of an auditory-vocal articulatory network that took place after the last common ancestor with the chimpanzee. I will attempt to converge this perspective with aspects of the Mirror System Hypothesis, particularly those related to the emergence of a meaningful grammar in human communication. Basically, the strengthening of auditory-vocal connectivity via the arcuate fasciculus and related tracts generated an expansion of working memory capacity for vocalizations, that was key for learning complex utterances. This process was concomitant with the development of a robust interface with visual working memory, both in the dorsal and ventral streams of auditory and visual processing. This enabled the bidirectional translation of sequential codes into hierarchical visual representations, through the development of a multimodal interface between both systems.

Keywords: arcuate fasciculus, working memory, laryngeal cortex, Broca’s area, vocal learning
Article outline
  • Introduction
  • Anatomy of the speech circuit
  • Grammar and semantics: Imaging studies
  • Working memory
  • From monkey to human
  • Speech origins
  • Descending control systems
  • Hand control and the mirror neuron system
  • Template construction grammar
  • Towards a new road map
  • Acknowledgements
  • References
Published online: 11 August 2020
DOI logo
https://doi.org/10.1075/bct.112.06abo
References
Aboitiz, F.
(2012) Gestures, vocalizations, and memory in language origins. Frontiers in Evolutionary Neuroscience 4, 2.Google Scholar
(2017) A Brain for Speech. A View from Evolutionary Neuroanatomy. London: Palgrave Macmillan. DOI logoGoogle Scholar
Aboitiz, F., & García, R.
(1997) The evolutionary origin of the language areas in the human brain. A neuroanatomical perspective. Brain Research Reviews 25, 381–396. DOI logoGoogle Scholar
Arbib, M. A.
(2012) How The Brain Got Language. The Mirror System Hypothesis. Oxford: Oxford University Press. DOI logoGoogle Scholar
(2016) Toward the Language-Ready Brain: Biological Evolution and Primate Comparisons. Psychonomics Bulletin Review 24, 142–150. DOI logoGoogle Scholar
(2017) Towards a computational comparative neuroprimatology: framing the language-ready brain. Physics of Life Reviews, 16, 1–54.. DOI logoGoogle Scholar
Arbib, M. A., & Caplan, D.
(1979) Neurolinguistics must be computational. Behavioral and Brain Sciences 2, 449–483. DOI logoGoogle Scholar
Baddeley, A.
(2007) Working Memory, Thought and Action. Oxford: Oxford University Press. DOI logoGoogle Scholar
(2012) Working memory: theories, models and controversies. Annual Review of Psychology 63, 1–29. DOI logoGoogle Scholar
Beauchamp, M. S.
(2015) The social mysteries of the superior temporal sulcus. Trends in Cognitive Sciences 19, 489–490. DOI logoGoogle Scholar
Binder, J. R., & Desai, R. H.
(2011) The neurobiology of semantic memory. Trends in Cognitive Sciences 15, 527–536. DOI logoGoogle Scholar
Brennan, J., Nir, Y., Hasson, U., Malach, R., Heeger, D. J., & Pylkkänen, L.
(2012) Syntactic structure building in the anterior temporal lobe during natural story listening. Brain and Language 120, 163–173. DOI logoGoogle Scholar
Caplan, D., & Waters, G. S.
(1999) Verbal working memory and sentence comprehension. Behavioral and Brain Sciences 22, 77–94. DOI logoGoogle Scholar
Catani, M., & Bambini, V.
(2014) A model for Social Communication And Language Evolution and Development (SCALED). Current Opinion in Neurobiology 28, 165–171. DOI logoGoogle Scholar
Colombo, M., D’Amato, M. R., Rodman, H. R., & Gross, C. G.
(1990) Auditory association cortex lesions impair auditory short-term memory in monkeys. Science 247, 336–338. DOI logoGoogle Scholar
Coudé, G., Ferrari, P. F., Rodà, F., Maranesi, M., Borelli, E., Veroni, V., Monti, F., Rozzi, S., & Fogassi, L.
(2011) Neurons controlling voluntary vocalization in the macaque ventral premotor cortex. PLoS One 6, e26822. DOI logoGoogle Scholar
Coudé, G. & Ferrari, P. F.
Reflections on the organization of the cortical motor system and its role in the evolution of communication in primates (this volume).
Erickson, L. C., Rauschecker, J. P., & Turkeltaub, P. E.
(2017) Meta-analytic connectivity modeling of the human superior temporal sulcus. Brain Structure and Function 222, 267–285. DOI logoGoogle Scholar
Friederici, A. D.
(2011) The brain basis of language processing: from structure to function. Physiological Reviews 91, 1357–1392. DOI logoGoogle Scholar
Fritz, J. B., Elhilali, M., Shamma, S. A.
(2005) Differential dynamic plasticity of A1 receptive fields during multiple spectral tasks. Journal of Neuroscience 25, 7623–7635 DOI logoGoogle Scholar
Fritz, J. B., Malloy, M., Mishkin, M., & Saunders, R. C.
(2016) Monkey’s short-term auditory memory nearly abolished by combined removal of the rostral superior temporal gyrus and rhinal cortices. Brain Research 1640, 289–98. DOI logoGoogle Scholar
García, R. R., Zamorano, F., & Aboitiz, F.
(2014) From imitation to meaning: circuit plasticity and the acquisition of a conventionalized semantics. Frontiers in Human Neuroscience 8, 605.Google Scholar
Goldman-Rakic, P. S.
(1995) Cellular basis of working memory. Neuron 14, 477–485. DOI logoGoogle Scholar
Griffiths, J. D., Marslen-Wilson, W. D., Stamatakis, E. A., & Tyler, L. K.
(2013) Functional organization of the neural language system: dorsal and ventral pathways are critical for syntax. Cerebral Cortex 23, 139–147. DOI logoGoogle Scholar
Gu, Z., Kalambogias, J., Yoshioka, S., Han, W., Li, Z., Kawasawa, Y. I., Pochareddy, S., Li, Z., Liu, F., Xu, X., Wijeratne, H. R. S., Ueno, M., Blatz, E., Salomone, J., Kumanogoh, A., Rasin, M. R., Gebelein, B., Weirauch, M. T., Sestan, N., Martin, J. H., & Yoshida, Y.
(2017) Control of species-dependent cortico-motoneuronal connections underlying manual dexterity. Science 357, 400–404. DOI logoGoogle Scholar
Hage, S. R., & Nieder, A.
(2016) Dual Neural Network Model for the Evolution of Speech and Language. Trends in Neuroscience 39, 813–829. DOI logoGoogle Scholar
Herculano-Houzel, S., Kaas, J. H., & de Oliveira-Souza, R.
(2016) Corticalization of motor control in humans is a consequence of brain scaling in primate evolution. Journal of Comparative Neurology 524, 448–455. DOI logoGoogle Scholar
Hickok, G.
(2017) A cortical circuit for voluntary laryngeal control: Implications for the evolution language. Psychonomics Bulletin Review 24, 56–63. DOI logoGoogle Scholar
Hickok, G., Houde, J., & Rong, F.
(2011) Sensorimotor integration in speech processing: computational basis and neural organization. Neuron 69, 407–422. DOI logoGoogle Scholar
Kumar, V., Croxson, P. L., & Simonyan, K.
(2016) Structural organization of the laryngeal motor cortical network and its implication for evolution of speech production. Journal of Neuroscience 36, 4170–4181. DOI logoGoogle Scholar
Lameira, A. R., Maddieson, I., & Zuberbühler, K.
(2014) Primate feedstock for the evolution of consonants. Trends in Cognitive Sciences 18, 60–62. DOI logoGoogle Scholar
Leighton, G. M.
(2017) Cooperative breeding influences the number and type of vocalizations in avan lineages. Proceedings of the Royal Society B 284 (1868), pii, 20171508.Google Scholar
Makuuchi, M., & Friederici, A. D.
(2013) Hierarchical functional connectivity between the core language system and the working memory system. Cortex 49, 2416–2423. DOI logoGoogle Scholar
Nelissen, K., Borra, E., Gerbella, M., Rozzi, S., Luppino, G., Vanduffel, W., Rizzolatti, G., & Orban, G. A.
(2011) Action observation circuits in the macaque monkey cortex. Journal of Neuroscience 31, 3743–3756. DOI logoGoogle Scholar
Nelson, M. J., El Karoui, I., Giber, K., Yang, X., Cohen, L., Koopman, H., Cash, S. S., Naccache, L., Hale, J. T., Pallier, C., & Dehaene, S.
(2017) Neurophysiological dynamics of phrase-structure building during sentence processing. Proceedings of the National Academy of Science U.S.A. 114, E3669–E3678 DOI logoGoogle Scholar
Neubert, F. X., Mars, R. B., Thomas, A. G., Sallet, J., & Rushworth, M. F.
(2014) Comparison of human ventral frontal cortex areas for cognitive control and language with areas in monkey frontal cortex. Neuron 81, 700–713. DOI logoGoogle Scholar
Okada, K., Matchin, W., & Hickok, G.
(2018) Neural evidence for predictive coding in auditory cortex during speech production. Psychonomics Bulletin Reviews 25, 423–430. DOI logoGoogle Scholar
Petrides, M.
(2014) Neuroanatomy of Language Regions of the Human Brain. New York: Academic Press.Google Scholar
Plakke, B., & Romanski, L. M.
(2016) Neural circuits in auditory and audiovisual memory. Brain Research 1640, 278–288. DOI logoGoogle Scholar
Putt, S. S., Wijeakumar, S., Franciscus, R. G., Spencer, J. P.
(2017) The functional brain networks that underlie Early Stone Age tool manufacture. Nature Human Behaviour, 1, 1–8. DOI logoGoogle Scholar
Rauschecker, J. P.
(2012) Ventral and dorsal streams in the evolution of speech and language. Frontiers in Evolutionary Neuroscience 4, 7.Google Scholar
(2017) Where, When, and How: Are they all sensorimotor? Towards a unified view of the dorsal pathway in vision and audition. Cortex [Epub ahead of print]Google Scholar
Rilling, J. K.
(2014) Comparative primate neurobiology and the evolution of brain language systems. Current Opinion in Neurobiology 28, 10–14. DOI logoGoogle Scholar
Rilling, J. K., Glasser, M. F., Jbabdi, S., Andersson, J., & Preuss, T. M.
(2012) Continuity, divergence, and the evolution of brain language pathways. Frontiers in Evolutionary Neuroscience 3, 11.Google Scholar
Rilling, J. K., Glasser, M. F., Preuss, T. M., Ma, X., Zhao, T., Hu, X., & Behrens, T. E.
(2008) The evolution of the arcuate fasciculus revealed with comparative DTI. Nature Neuroscience 11, 426–428. DOI logoGoogle Scholar
Rizzolatti, G., & Arbib, M. A.
(1998) Language within our grasp. Trends in Neuroscience 21, 188–194. DOI logoGoogle Scholar
Romanski, L. M., Tian, B., Fritz, J., Mishkin, M., Goldman-Rakic, P. S., & Rauschecker, J. P.
(1999) Dual streams of auditory afferents target multiple domains in the primate prefrontal cortex. Nature Neuroscience 2, 1131–1136. DOI logoGoogle Scholar
Romanski, L. M.
(2007) Representation and integration of auditory and visual stimuli in the primate ventral lateral prefrontal cortex. Cerebral Cortex 17, Suppl 1: i61–i69. DOI logoGoogle Scholar
Schomers, M. R., Garagnani, M., & Pulvermüller, F.
(2017) Neurocomputational Consequences of Evolutionary Connectivity Changes in Perisylvian Language Cortex. Journal of Neuroscience 37, 3045–3055. DOI logoGoogle Scholar
Scott, B. H., Mishkin, M., & Yin, P.
(2012) Monkeys have a limited form of short-term memory in audition. Proceedings of the National Academy of Science U.S.A. 109, 12237–12241. DOI logoGoogle Scholar
(2014) Neural correlates of auditory short-term memory in rostral superior temporal cortex. Current Biology 24, 2767–2775. DOI logoGoogle Scholar
Stivers, T., Enfield, N. J., Brown, P., Englert, C., Hayashi, M., Heinemann, T., Hoymann, G., Rossano, F., de Ruiter, J. P., Yoon, K. E., & Levinson, S. C.
(2009) Universals and cultural variation in turn-taking in conversation. Proceedings of the National Academy of Science U.S.A. 106, 10587–10592. DOI logoGoogle Scholar
Skeide, M. A., & Friederici, A. D.
(2016) The ontogeny of the cortical language network. Nature Reviews Neuroscience 17, 323–332. DOI logoGoogle Scholar
Tremblay, P., & Dick, A. S.
(2016), Broca and Wernicke are dead, or moving past the classic model of language neurobiology. Brain and Language 162, 60–71. DOI logoGoogle Scholar
Tyler, L. K., Shafto, M. A., Randall, B., Wright, P., Marslen-Wilson, W. D., & Stamatakis, E. A.
(2010) Preserving syntactic processing across the adult life span: the modulation of the frontotemporal language system in the context of age-related atrophy. Cerebral Cortex 20, 352–364. DOI logoGoogle Scholar
Tyler, L. K., Marslen-Wilson, W. D., Randall, B., Wright, P., Devereux, B. J., Zhuang, J., Papoutsi, M., & Stamatakis, E. A.
(2011) Left inferior frontal cortex and syntax: function, structure and behaviour in patients with left hemisphere damage. Brain 134, 415–431. DOI logoGoogle Scholar
Wilson, B., & Petkov, P. I.
From evolutionarily conesrved frontal regions for sequence processing to human innovations in syntax (this volume).
Yamamoto, K., & Sakai, K. L.
(2016) The dorsal rather than ventral pathway better reflects individual syntactic abilities in second language. Frontiers in Human Neuroscience 10, 295. DOI logoGoogle Scholar
Yeatman, J. D., Dougherty, R. F., Rykhlevskaia, E., Sherbondy, A. J., Deutsch, G. K., Wandell, B. A., & Ben-Shachar, M.
(2011) Anatomical properties of the arcuate fasciculus predict phonological and reading skills in children. Journal of Cognitive Neuroscience 23, 3304–3317. DOI logoGoogle Scholar
Cited by

Cited by 1 other publications

Michon, Maëva, José Zamorano-Abramson & Francisco Aboitiz
2022. Faces and Voices Processing in Human and Primate Brains: Rhythmic and Multimodal Mechanisms Underlying the Evolution and Development of Speech. Frontiers in Psychology 13 DOI logo

This list is based on CrossRef data as of 15 april 2024. Please note that it may not be complete. Sources presented here have been supplied by the respective publishers. Any errors therein should be reported to them.