Cover not available

Article published In: How the Brain Got Language: Towards a New Road Map
Edited by Michael A. Arbib
[Interaction Studies 19:1/2] 2018
► pp. 102–120

Get fulltext from our e-platform
JBE logo with link
PDF logo with download linkDownload PDF
authorization required

Why do we want to talk?

Evolution of neural substrates of emotion and social cognition

 | University of California, San Diego
Published online: 17 September 2018
DOI logo with link
https://doi.org/10.1075/is.17046.sem
Abstract
Cognitive and emotional processes are now known to be intertwined and thus the limbic system that underlies emotions is important for human brain evolution, including the evolution of circuits supporting language. The neural substrates of limbic functions, like motivation, attention, inhibition, evaluation, detection of emotional stimuli and others have changed over time. Even though no new, added structures are present in the human brain compared to nonhuman primates, evolution tweaks existing structural systems with possible functional implications. Empirical comparative neuroanatomical evidence is presented here in support of such changes in the limbic system, including the amygdala and the orbitofrontal cortex. Given their possible functional significance, these alterations may further enable and enhance human interest and motivation to communicate beyond what is seen in other primates living in complex social groups. The argument here is that even though emotion processing is likely needed for increased social complexity independent of language, the reason why humans want to talk may be related in part to the enhancement of socioemotional processes resulting from the reorganization and rewiring of underlying neural systems some of which are interconnected to the language areas. Neurodevelopmental disorders in humans affecting both language and sociability fuel such arguments.
Article outline
  • Introduction
  • Gestural communication, language and limbic neural substrates in human and nonhuman primates
  • Detection of the changing social environment and behavioral responses
  • Motivation, evaluation of error, modulation
  • Feelings, body and mind integration, and empathic theory of mind
  • Emotion, social cognition and language evolution
  • Towards a new road map
  • Acknowledgements
  • References
References (63)
References
Adolphs, R., (2001). The neurobiology of social cognition. Current Opinion in Neurobiology, 11(2), 231–239. Google Scholar logo with link to Google Scholar
, (2009). The Social Brain: Neural Basis of Social Knowledge. Annu Rev Psychol, 601, 693–716. Google Scholar logo with link to Google Scholar
, (2017). How should neuroscience study emotions? By distinguishing emotion states, concepts, and experiences Social Cognitive and Affective Neuroscience, 24–31. Google Scholar logo with link to Google Scholar
Allman, J., Hakeem, A., Watson, K., (2002). Two phylogenetic specializations in the human brain. Neuroscientist 8 (4), 335–346. Google Scholar logo with link to Google Scholar
Allman, J. M., Tetreault, N. A., Hakeem, A. Y., et al., (2010). The von Economo neurons in frontoinsular and anterior cingulate cortex in great apes and humans. Brain Struct. Funct. 214 (5–6), 495–517. Google Scholar logo with link to Google Scholar
Anderson, D. J., & Adolphs, R., (2014). A Framework for Studying Emotions across Species. Cell, 157(1), 187–200. Google Scholar logo with link to Google Scholar
Antonell, A., de Luis, O., Domingo-Roura, X., Pérez-Jurado, L. A., (2005): Evolutionary mechanisms shaping the genomic structure of the Williams-Beuren syndrome chromosomal region at human 7q11.23. Genome Res 151, 1179–1188. Google Scholar logo with link to Google Scholar
Arbib, M. A., (2012). How the Brain Got Language: The Mirror System Hypothesis. New York & Oxford: Oxford University Press. Google Scholar logo with link to Google Scholar
Arbib, M. A., & Bota, M., (2003). Language Evolution: Neural Homologies and Neuroinformatics. Neural Networks, 161, 1237–1260. Google Scholar logo with link to Google Scholar
Arbib, M. A., & Fellous, J. M., (2004). Emotions: from brain to robot. Trends Cogn Sci, 8(12), 554–561. Google Scholar logo with link to Google Scholar
Armstrong, E., (1980). A quantitative comparison of the hominoid thalamus: II. Limbic Nuclei anterior Principalis and Lateralis nucleus. Am. J. Phys. Anthropol. 52 (3), 43–54.Google Scholar logo with link to Google Scholar
, (1990). The limbic system and culture: an allometric analysis of the neocortex and limbic nuclei. Hum. Nat. 21, 117–136. Google Scholar logo with link to Google Scholar
Barbas, H., (2015). General Cortical and Special Prefrontal Connections: Principles from Structure to Function. (Edited by: Hyman, S. E.) Annual Review of Neuroscience 381, 269–289 Google Scholar logo with link to Google Scholar
Barger, N., Stefanacci, L., Semendeferi, K., (2007). A comparative volumetric analysis of the amygdaloid complex and basolateral division in the human and ape brain. Am. J. Phys. Anthropol. 403 (134), 392–403. Google Scholar logo with link to Google Scholar
Barger, N., Stefanacci, L., Schumann, C. M., et al., (2012). Neuronal populations in the basolateral nuclei of the amygdala are differentially increased in humans compared with apes: a stereological study. J. Comp. Neurol. 520 (13), 3035–3054. Google Scholar logo with link to Google Scholar
Barger, N., Hanson, K. L., Teffer, K., Schenker-Ahmed, N. M., Semendeferi, K., (2014). Evidence for evolutionary specialization in human limbic structures. Front. Hum. Neurosci. 81, 1–17. Google Scholar logo with link to Google Scholar
Bauernfeind, A. L., de Sousa, A. A., Avasthi, T., et al., (2013). A volumetric comparison of the insular cortex and its subregions in primates. J. Hum. Evol. 64 (4), 263–279 Google Scholar logo with link to Google Scholar
Bellugi, U., Järvinen-Pasley, A., Doyle, T., Reilly, J., & Korenberg, J., (2007). Affect, social behavior and brain in Williams syndrome. Current Directions in Psychological Science, 51, 197–208.Google Scholar logo with link to Google Scholar
Bellugi, U., Lichtenberger, L., Mills, D., Galaburda, A., Korenberg, J. R., (1999): Bridging cognition, the brain and molecular genetics: evidence from Williams syndrome. Trends Neurosci 221, 197–207. Google Scholar logo with link to Google Scholar
Belyk, Michel; Brown, Steven; Lim, Jessica; et al., (2017). Convergence of semantics and emotional expression within the IFG pars orbitalis Neuroimage. 1561, 240–248. Google Scholar logo with link to Google Scholar
Bianchi, S., Stimpson C. D., Bauernfield, A. L., Schapiro, S. J., Wallace, B. B., McArthur M. M., Bronson, E., Hopkins W. D., Semendeferi, K., Jacobs, B., Hof, P. R. and Sherwood C. C., (2013). Dendritic morphology of pyramidal neurons in the chimpanzee neocortex: regional specializations and comparison to humans. Cerebral Cortex 23(10):2429–2436 Google Scholar logo with link to Google Scholar
Bickart, K. C., Wright, C. I., Dautoff, R. J., Dickerson, B. C., Barrett, L. F., (2011). Amygdala volume and social network size in humans. Nat. Neurosci. 14 (2), 163–164. Google Scholar logo with link to Google Scholar
Chailangkarn, T., Trujillo, C. A., Freitas, B. C., Hrvoj-Mihic, B., Herai, R. H., Yu, D. X., Timothy T. Brown, Maria C. Marchetto, Cedric Bardy, Lauren McHenry, Lisa Stefanacci, Anna Järvinen, Yvonne M. Searcy, Michelle DeWitt, Wenny Wong, Philip Lai, M. Colin Ard, Kari L. Hanson, Sarah Romero, Bob Jacobs, Anders M. Dale8, Li Dai, Julie R. Korenberg, Fred H. Gage, Ursula Bellugi, Eric Halgren, Katerina Semendeferi & Alysson R. Muotri. (2016). A human neurodevelopmental model for Williams syndrome. Nature 5361, 338–343.Google Scholar logo with link to Google Scholar
Chun, C. F., T. T. Brown, Hauke Bartsch, Joshua M. Kuperman, Donald J. Hagler Jr., Andrew Schork, Yvonne Searcy, Ursula Bellugi, Eric Halgren, Anders M. Dale. (2017). Williams syndrome-specific neuroanatomical profile and its associations with behavioral features NeuroImage: Clinical. 151, 343–347. Google Scholar logo with link to Google Scholar
Craig, A. D., (2009). How do you feel now? the anterior insula and human awareness. Nat. Rev. Neurosci. 101, 59–70. Google Scholar logo with link to Google Scholar
Damasio, A. R., (1994). Descartes’ Error Grosset/Putnam, New York.Google Scholar logo with link to Google Scholar
Deaner, R. O., Isler, K., Burkart, J., & van Schaik, C., (2007). Overall brain size, and not encephalization quotient, best predicts cognitive ability across non-human primates. Brain, Behavior and Evolution, 70(2), 115–24. Google Scholar logo with link to Google Scholar
DeFelipe, J., Alonso-Nanclares, L., Arellano, J. I., (2002): Microstructure of the neocortex: comparative aspects. J Neurocytol 311, 299–316. Google Scholar logo with link to Google Scholar
Etkin, A., Egner, T., Kalisch, R., (2011). Emotional processing in anterior cingulate and medial prefrontal cortex. Trends Cogn. Sci. 15 (2), 85–93. Google Scholar logo with link to Google Scholar
Evrard, H. C., Forro, T., Logothetis, N. K., (2012). Von Economo neurons in the anterior insula of the macaque monkey. Neuron 74 (3), 482–489 Google Scholar logo with link to Google Scholar
Falk, D., (2016). Evolution of brain and culture: the neurological and cognitive journey from Australopithecus to Albert Einstein J Anthropological Sciences. 941, 99–111.Google Scholar logo with link to Google Scholar
Ferrari, P. F., Gerbella, M., Coudé, G., & Rozzi, S., (2017). Two different mirror neuron networks: The sensorimotor (hand) and limbic (face) pathways. Neuroscience 3581, 300–315. Google Scholar logo with link to Google Scholar
Hanson, K. L., Branka Hrvoj-Mihic and Katerina Semendeferi. (2014). A Dual Comparative Approach: Integrating Lines of Evidence from Human Evolutionary Neuroanatomy and Neurodevelopmental Disorders Brain Behav Evol 2014; 841, 135–155. Google Scholar logo with link to Google Scholar
Hanson, K. L., Lew C. H., Hrvoj-Mihic, B., Groeniger K. M., Halgren, E., Bellugi, U. and K. Semendeferi. (2017). Increased glia density in the caudate nucleus in Williams syndrome: implications for frontostriatal dysfunction in autism. Developmental Neurobiology, published online.Google Scholar logo with link to Google Scholar
Heimer, L. and Van Hoesen G. W., (2006). The limbic lobe and its output channels: implications for emotional functions and adaptive behavior. Neuroscience & Biobehavioral Reviews 30(2):126–147. Google Scholar logo with link to Google Scholar
Hof, P. R., Nimchinsky, E. A., Perl, D. P., Erwin, J. M., (2001). An unusual population of pyramidal neurons in the anterior cingulate cortex of hominids contains the calcium-binding protein calretinin. Neurosci. Lett. 307 (3), 139–142. Google Scholar logo with link to Google Scholar
Horton Lew, C., C. Brown, U. Bellugi, and K. Semendeferi. (2017). Neuron density is decreased in the prefrontal cortex in Williams syndrome. Autism Research 101, 99–112. Google Scholar logo with link to Google Scholar
Hrvoj-Mihic, B.; Hanson, Kari L.; Lew, Caroline H.; et al., (2017). Basal Dendritic Morphology of Cortical Pyramidal Neurons in Williams Syndrome: Prefrontal Cortex and Beyond Frontiers in Neuroscience. 111, 419. Google Scholar logo with link to Google Scholar
Hutsler, J. J., Zhang, H., (2010): Increased dendritic spine densities on cortical projection neurons in autism spectrum disorders. Brain Res 13091, 83–94. Google Scholar logo with link to Google Scholar
Iacoboni, M., Dapretto, M., (2006). The mirror neuron system and the consequences of its dysfunction. Nat. Rev. Neurosci. 7 (12), 942–951. Google Scholar logo with link to Google Scholar
Jarvinen, A., Korenberg, J., Bellugi, U., (2013). The social phenotype of Williams syndrome. Current Opinion in Neurobiology 231, 1–9. Google Scholar logo with link to Google Scholar
Krubitzer, L., Kahn, D. M., (2003). Nature versus nurture revisited: an old idea with a new twist. Progress in Neurobiology 701, 33–52. Google Scholar logo with link to Google Scholar
LeDoux, J., (1996). The Emotional Brain, Simon & Schuster.Google Scholar logo with link to Google Scholar
Lew, C. H., Semendeferi, K., (2017). Evolutionary Specializations of the Human Limbic System. In: Kaas, J. (ed.), Evolution of Nervous Systems 2e. vol. 41, pp. 277–291. Oxford: Elsevier. Google Scholar logo with link to Google Scholar
Lew, C. H., Groeniger, K. M., Bellugi, U., Stefanacci, L., Schumann, C. M., K. Semendeferi. (2017). A postmortem stereological study of the amygdala in Williams syndrome. Brain Structure and Function, published online. Google Scholar logo with link to Google Scholar
Mesulam, M. M., Mufson, E. J., (1982). Insula of the old world monkey III: efferent cortical output and comments on function. J. Comp. Neurol. 212 (1), 38–52 Google Scholar logo with link to Google Scholar
Morecraft, R. J., K. S. Stilwell-Morecraft, J. Ge, P. B. Cipolloni, D. N. Pandya. (2015). Cytoarchitecture and cortical connections of the anterior insula andadjacent frontal motor fields in the rhesus monkey Brain Research Bulletin. 1191, 52–72 Google Scholar logo with link to Google Scholar
Nimchinsky, E. A., Gilissen, E., Allman, J. M., Perl, D. P., Erwin, J. M., Hof, P. R., (1999). A neuronal morphologic type unique to humans and great apes. Proc. Natl. Acad. Sci. U.S.A. 96 (9), 5268–5273. Google Scholar logo with link to Google Scholar
Okon-Singer, H., Hendler, T., Pessoa, L., Shackman, A., (2015). The neurobiology of emotion-cognition interactions: fundamental questions and strategies for future research. Frontiers in Human Neuroscience, 91, 58. Google Scholar logo with link to Google Scholar
Pessoa, L., (2013). The Cognitive-Emotional Brain: From Interactions to Integration. Cambridge, MA: MIT Press. Google Scholar logo with link to Google Scholar
Petanjek, Z., Judas, M., Kostovic, I., Uylings, H. B. M., (2008): Lifespan alterations of basal dendritic trees of pyramidal neurons in the human prefrontal cortex: a layer-specific pattern. Cereb Cortex 181, 915–929. Google Scholar logo with link to Google Scholar
Petanjek, Z., Judas, M., Simic, G., Rasina, M. R., Uylings, H. B. M., Rakic, P., Kostovic, I., (2011): Extraordinary neoteny of synaptic spines in the human prefrontal cortex. Proc Natl Acad Sci USA 1081, 13281–13286. Google Scholar logo with link to Google Scholar
Schumann, C. M., Amaral, D. G., (2006). Stereological analysis of amygdala neuron number in autism. J. Neurosci. 26 (29), 7674–7679. Google Scholar logo with link to Google Scholar
Seeley, W. W., Carlin, D. A., Allman, J. M., et al., (2006). Early frontotemporal dementia targets neurons unique to apes and humans. Ann. Neurol. 60 (6), 660–667. Google Scholar logo with link to Google Scholar
Semendeferi, K., Armstrong, E., Schleicher, A., Zilles, K., Van Hoesen, G. W., (1998). Limbic frontal cortex in hominoids: a comparative study of area 13. Am. J. Phys. Anthropol. 106 (2), 129–155. Google Scholar logo with link to Google Scholar
, (2001). Prefrontal cortex in humans and apes: A comparative study of Area 10. Am. J. Phys. Anthropol. 1141, 224–241. Google Scholar logo with link to Google Scholar
Semendeferi, K., N. Barger, N. Schenker Brain reorganization in humans and apes. In: Human Brain Evolving. D. Broadfield, M. Yuan, N. Toth, and K. Schick (Eds) Stone Age Institute Press (4th volume). David Brown Book Company and Oxbow Books, pp.119–155 (2010).Google Scholar logo with link to Google Scholar
Stefanacci, L., Amaral, D. G., (2000). Topographic organization of cortical inputs to the lateral nucleus of the macaque monkey amygdala: a retrograde tracing study. J. Comp. Neurol. 4211, 52–79. Google Scholar logo with link to Google Scholar
Striedter, G. F., (2004). Principles of Brain Evolution Sinauer Associates. Google Scholar logo with link to Google Scholar
Von Economo, C., (1929). The Cytoarchitectonics of the Human Cerebral Cortex. Oxford University Press, Oxford, UK.Google Scholar logo with link to Google Scholar
Wicker, B., Keysers, C., Plailly, J., Royet, J. P., Gallese, V., & Rizzolatti, G., (2003). Both of us disgusted in My insula: the common neural basis of seeing and feeling disgust. Neuron, 40(3), 655–664. Google Scholar logo with link to Google Scholar
Cited by (4)

Cited by four other publications

Hertrich, Ingo, Susanne Dietrich & Hermann Ackermann
2020. The Margins of the Language Network in the Brain. Frontiers in Communication 5 DOI logo
Petanjek, Zdravko, Dora Sedmak, Domagoj Džaja, Ana Hladnik, Mladen Roko Rašin & Nataša Jovanov-Milosevic
2019. The Protracted Maturation of Associative Layer IIIC Pyramidal Neurons in the Human Prefrontal Cortex During Childhood: A Major Role in Cognitive Development and Selective Alteration in Autism. Frontiers in Psychiatry 10 DOI logo
Arbib, Michael A., Francisco Aboitiz, Judith M. Burkart, Michael Corballis, Gino Coudé, Erin Hecht, Katja Liebal, Masako Myowa-Yamakoshi, James Pustejovsky, Shelby Putt, Federico Rossano, Anne E. Russon, P. Thomas Schoenemann, Uwe Seifert, Katerina Semendeferi, Chris Sinha, Dietrich Stout, Virginia Volterra, Sławomir Wacewicz & Benjamin Wilson
2018. The comparative neuroprimatology 2018 (CNP-2018) road map for research on How the Brain Got Language . Interaction Studies. Social Behaviour and Communication in Biological and Artificial Systems 19:1-2 ► pp. 370 ff. DOI logo
Arbib, Michael A., Francisco Aboitiz, Judith M. Burkart, Michael Corballis, Gino Coudé, Erin Hecht, Katja Liebal, Masako Myowa-Yamakoshi, James Pustejovsky, Shelby Putt, Federico Rossano, Anne E. Russon, P. Thomas Schoenemann, Uwe Seifert, Katerina Semendeferi, Chris Sinha, Dietrich Stout, Virginia Volterra, Sławomir Wacewicz & Benjamin Wilson
2020. The comparative neuroprimatology 2018 (CNP-2018) road map for research on How the Brain Got Language . In How the Brain Got Language – Towards a New Road Map [Benjamins Current Topics, 112], ► pp. 370 ff. DOI logo

This list is based on CrossRef data as of 17 march 2026. 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.

Mobile Menu Logo with link to supplementary files background Layer 1 prag Twitter_Logo_Blue