Hostname: page-component-76fb5796d-x4r87 Total loading time: 0 Render date: 2024-04-25T14:41:19.830Z Has data issue: false hasContentIssue false
  • English
  • Français

How did vocal behavior “take over” the gestural communication system?

Published online by Cambridge University Press:  11 March 2014

Francisco Aboitiz
Francisco Aboitiz*
Affiliation:
Departamento de Psiquiatría, Facultad de Medicina, and Centro Interdisciplinario de Neurociencia, Pontificia Universidad Católica de Chile, Santiago, Chile, E-mail: faboitiz@puc.cl
Get access Rights & Permissions [Opens in a new window]

Abstract

In this commentary, I argue (i) that there are some peripheral homologies between the monkey and the human vocalization systems; (ii) that complex vocal learning can be achieved without need of a voluntary hand grasping circuit; and (iii) that in the monkey there are rudimentary circuits that can convey auditory information into Broca's region, via the “ventral pathway” but also via the arcuate or the superior longitudinal fasciculi.

Type
Comparing the macaque and human brain
Information
Language and Cognition , Volume 5 , Issue 2-3: Special Issue , September 2013 , pp. 167 - 176
Copyright
Copyright © UK Cognitive Linguistics Association 2013

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aboitiz, F. 2012. Gestures, vocalizations and memory in language origins. Frontiers in Evolutionary Neuroscience 4(2) doi: 10.3389/fnevo.2012.00002.Google Scholar
Aboitiz, F., Aboitiz, S. & García, R.. 2010. The phonological loop: a key innovation in human evolution. Current Anthropology 51(Suppl.S1). S55–S65.Google Scholar
Aboitiz, F. & García, R.. 1997. The evolutionary origin of the language areas in the human brain. A neuroanatomical perspective. Brain Research Reviews 25(3). 381–396.CrossRefGoogle ScholarPubMed
Aboitiz, F., García, R., Bosman, C. & Brunetti, E.. 2006. Cortical memory mechanisms and language origins. Brain and Language 98(1). 40–56.Google Scholar
Abramson, J. Z., Hernández-Lloreda, V., Call, J. & Colmenares, F.. 2012. Experimental evidence for action imitation in killer whales (Orcinus orca). Animal Cognition [Epub ahead of print Aug 9].Google Scholar
Arbib, M. A. 2010. Mirror system activity for action and language is embedded in the integration of dorsal and ventral pathways. Brain and Language 112(1). 12–24.Google Scholar
Assaneo, M. F., Nichols, J. I. & Trevisan, M. A.. 2011. The anatomy of onomatopoeia. PLoS One 6(12). e28317.Google Scholar
Beckers, G. J., Bolhuis, J. J., Okanoya, K. & Berwick, R. C.. 2012. Birdsong neurolinguistics: songbird context-free grammar claim is premature. Neuroreport 23(3). 139–145.Google Scholar
Belin, P. & Zatorre, R. J.. 2000. ‘What,’ ‘where’ and ‘how’ in auditory cortex. Nature Neuroscience 3(10). 965–966.CrossRefGoogle ScholarPubMed
Belmalih, A., Borra, E., Contini, M., Gerbella, M., Rozzi, S. & Luppino, G.. 2009. Multimodal architectonic subdivision of the rostral part (area F5) of the macaque ventral premotor cortex. Journal of Comparative Neurology 512(2). 183–217.Google Scholar
Bolhuis, J. J., Okanoya, K. & Scharff, C.. 2010. Twitter evolution: converging mechanisms in birdsong and human speech. Nature Reviews Neuroscience 11(11). 747–759.Google Scholar
Bonini, L. & Ferrari, P. F.. 2011. Evolution of mirror systems: a simple mechanism for complex cognitive functions. Annals of the New York Academy of Sciences 1225(4). 166–175.Google Scholar
Buchsbaum, B. R., Baldo, J., Okada, K., Berman, K. F., Dronkers, N., D'Esposito, M. & Hickok, G.. 2011. Conduction aphasia, sensory-motor integration, and phonological short-term memory – an aggregate analysis of lesion and fMRI data. Brain and Language 119(3). 119–128.Google Scholar
Buchsbaum, B. R. & D'Esposito, M.. 2008. The search for the phonological store: from loop to convolution. Journal of Cognitive Neuroscience 20(5). 762–778.Google Scholar
Buchsbaum, B. R., Ye, D. & D'Esposito, M.. 2011. Recency Effects in the Inferior Parietal Lobe during Verbal Recognition Memory. Front Hum Neurosci. 5(59). doi:10.3389/fnhum.2011.00059Google Scholar
Catani, M. & ffytche, D. H.. 2005. The rises and falls of disconnection syndromes. Brain 128(10). 2224–2239.Google 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(11). e26822. doi:10.1371/journal.pone.0026822CrossRefGoogle ScholarPubMed
Dick, A. S. & Tremblay, P.. 2012. Beyond the arcuate fasciculus: consensus and controversy in the connectional anatomy of language. Brain. Advance online access.Google Scholar
Ferrari, P. F., Gallese, V., Rizzolatti, G., and Fogassi, L.. 2003. Mirror neurons responding to the observation of ingestive and communicative mouth actions in the monkey ventral premotor cortex. European Journal of Neuroscience 17(8). 1703–1714.CrossRefGoogle Scholar
Fitch, W. T. & Reby, D.. 2001. The descended larynx is not uniquely human. Proceedings of the Royal Society. Biological Sciences 268(1477). 1669–1675.Google Scholar
Frey, S., Campbell, J. S. W., Pike, G. B. & Petrides, M.. 2008. Dissociating the human language pathways with high angular resolution diffusion fiber tractography. Journal of Neuroscience 28(45). 11435–11444.Google Scholar
Gentner, T. Q., Fenn, K. M., Margoliash, D. & Nusbaum, H. C.. 2006. Recursive syntactic pattern learning by songbirds. Nature 440(7088). 1204–1207.Google Scholar
Gerbella, M., Belmalih, A., Borra, E., Rozzi, S. & Luppino, G.. 2010. Cortical connections of the macaque caudal ventrolateral prefrontal areas 45A and 45B. Cerebral Cortex 20(1). 141–168.Google Scholar
Gerbella, M., Belmalih, A., Borra, E., Rozzi, S. & Luppino, G.. 2011. Cortical connections of the anterior (F5a) subdivision of the macaque ventral premotor area F5. Brain Structure and Function 216(3–4 ). 43–65.CrossRefGoogle ScholarPubMed
Ghazanfar, A. A., Takahashi, D. Y., Mathur, N. & Fitch, W. T.. 2012. Cineradiography of monkey lip-smacking reveals putative precursors of speech dynamics. Current Biology 22(13). 1176–1182.Google Scholar
Gil-da-Costa, R., Martin, A., Lopes, M. A., Muñoz, M., Fritz, J. B. & Braun, A. R.. 2006. Species-specific calls activate homologs of Broca's and Wernicke's areas in the macaque. Nature Neuroscience 9(8). 1064–1070.Google Scholar
Herman, L. M. 2002. Vocal, social, and self-imitation by bottlenosed dolphins. In: Kerstin Dautenhahn, K and Nehaniv, Chrystopher L. (eds.), Imitation in animals and artifacts, 63–108. Cambridge: MIT Press.CrossRefGoogle Scholar
Hickok, G. & Poeppel, D.. 2007. The cortical organization of speech processing. Nature Reviews Neuroscience 8(5). 393–402.Google Scholar
Horowitz, A. C. 2003. Do humans ape? Or do apes human? Imitation and intention in humans (Homo sapiens) and other animals. Journal of Comparative Psychology 117(3). 325–336.Google Scholar
Howard, M. F. & Poeppel, D.. 2012. The neuromagnetic response to spoken sentences: co-modulation of theta band amplitude and phase. Neuroimage 60(4). 2118–2127.Google Scholar
Huber, L., Range, F., Voelkl, B., Szucsich, A., Viranyi, Z. & Miklosi, A.. 2009. The evolution of imitation: what do the capacities of nonhuman animals tell us about the mechanisms of imitation? Philosohical Transactions of the Royal Society of London B Biological Sciences 364(1528). 2299–2309.Google Scholar
Jürgens, U. & Alipour, M.. 2002. A comparative study on the cortico-hypoglossal connections in primates, using biotin dextranamine. Neuroscience Letters 328(3). 245–248.Google Scholar
Mehler, J., Nespor, M., Shukla, M. & Peña, M.. 2006. Why is language unique to humans? Novartis Foundation Symposium 270. 251–292.Google Scholar
Morrill, R. J., Paukner, A., Ferrari, P. F. & Ghazanfar, A. A.. 2012. Monkey lipsmacking develops like the human speech rhythm. Developmental Science 15(4). 557–568.Google 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(10) 3743–3756.Google Scholar
Nelissen, K., Luppino, G., Vanduffel, W., Rizzolatti, G. & Orban, G. A.. 2005. Observing others: multiple action representation in the frontal lobe. Science 310(5746). 332–336.CrossRefGoogle ScholarPubMed
Petrides, M., Cadoret, G. & Mackey, S.. 2005. Orofacial somatomotor responses in the macaque monkey homologue of Broca's area. Nature 435(7046). 1235–1238.CrossRefGoogle ScholarPubMed
Petrides, M. & Pandya, D. N.. 2009. Distinct parietal and temporal pathways to the homologues of Broca's area in the monkey. PLoS Biology 7(8). e1000170. doi:10.1371/journal.pbio.1000170Google Scholar
Preuss, T. & Goldman-Rakic, P. S.. 1991. Ipsilateral cortical connections of granular frontal cortex in the strepsirhine primate Galago, with comparative comments on anthropoid primates. Journal of Comparative Neurology 310(4). 507–549.Google Scholar
Ridgway, S., Carder, D., Jeffries, M. & Todd, M.. 2012. Spontaneous human speech mimicry by a cetacean. Current Biology 22(20). R860–R861.Google Scholar
Rilling, J. K., Glasser, M. F., Preuss, T. M., Ma, X., Zhao, T., Hu, X. & Behrens, T. E. J.. 2008. The evolution of the arcuate fasciculus revealed with comparative DTI. Nature Neuroscience 11(4). 426–428.Google Scholar
Rilling, J. K., Glasser, M. F., Jbabdi, S., Andersson, J. & Preuss, T. M.. 2011. Continuity, divergence, and the evolution of brain language pathways. Frontiers in Evolutionary Neuroscience 3(11). doi:10.3389/fnevo.2011.00011Google Scholar
Rizzolatti, G. W. & Craighero, L.. 2004. The mirror-neuron system. Annual Reviews in Neuroscience 27. 169–192.Google 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(30). 12237–12241.Google Scholar
Stoeger, A. S., Mietchen, D., Oh, S., de Silva, S., Herbst, C. T., Kwon, S. & Fitch, W. T.. 2012. An asian elephant imitates human speech. Current Biology 22(22). 2144–2148.Google Scholar
Taglialatela, J. P., Reamer, L., Schapiro, S. J. & Hopkins, W. D.. 2012. Social learning of a communicative signal in captive chimpanzees. Biological Letters 8(4). 498–501.Google Scholar
Tennie, C., Call, J. & Tomasello, M.. 2012. Untrained chimpanzees (Pan troglodytes schweinfurthii ) fail to imitate novel actions. PLoS One 7(8). e41548. doi:10.1371/journal.pone.0041548Google Scholar
van Heijningen, C. A. A., de Visser, J., Zuidema, W. & ten Cate, C.. 2009. Simple rules can explain discrimination of putative recursive syntactic structures by a songbird species. Proceedings of the National Academy of Science U.S.A. 106(48). 20538–20543.CrossRefGoogle ScholarPubMed
Whiten, A., Custance, D. M., Gómez, J. C., Teixidor, P. & Bard, K. A.. 1996. Imitative learning of artificial fruit processing in children (Homo sapiens) and chimpanzees (Pan troglodytes). Journal of Comparative Psychology 110(1). 3–14.Google Scholar
Yeterian, E. H., Pandya, D. N., Tomaiuolo, F. & Petrides, M.. 2012. The cortical connectivity of the prefrontal cortex in the monkey brain. Cortex 48(1). 58–81.Google Scholar
Zentall, T. R. 2006. Imitation: definitions, evidence, and mechanisms. Animal Cognition 9(4). 335–353.Google Scholar