In:How the Brain Got Language – Towards a New Road Map:
Edited by Michael A. Arbib
[Benjamins Current Topics 112] 2020
► pp. 102–120
Why do we want to talk?
Evolution of neural substrates of emotion and social cognition
Published online: 11 August 2020
https://doi.org/10.1075/bct.112.08sem
https://doi.org/10.1075/bct.112.08sem
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)
Adolphs, R. (2001). The neurobiology of social cognition. Current Opinion in Neurobiology, 11(2), 231–239.
(2017). How should neuroscience study emotions? By distinguishing emotion states, concepts, and experiences Social Cognitive and Affective Neuroscience, 24–31.
Allman, J., Hakeem, A., Watson, K. (2002). Two phylogenetic specializations in the human brain. Neuroscientist 8 (4), 335–346.
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.
Anderson, D. J., & Adolphs, R. (2014). A Framework for Studying Emotions across Species. Cell, 157(1), 187–200.
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 15, 1179–1188.
Arbib, M. A. (2012). How the Brain Got Language: The Mirror System Hypothesis. New York & Oxford: Oxford University Press.
Arbib, M. A., & Bota, M. (2003). Language Evolution: Neural Homologies and Neuroinformatics. Neural Networks, 16, 1237–1260.
Arbib, M. A., & Fellous, J. M. (2004). Emotions: from brain to robot. Trends Cogn Sci, 8(12), 554–561.
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.
(1990). The limbic system and culture: an allometric analysis of the neocortex and limbic nuclei. Hum. Nat. 2, 117–136.
Barbas, H. (2015). General Cortical and Special Prefrontal Connections: Principles from Structure to Function. (Edited by: Hyman, S. E.) Annual Review of Neuroscience 38, 269–289
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.
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.
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. 8, 1–17.
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
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, 5, 197–208.
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 22, 197–207.
Belyk, Michel; Brown, Steven; Lim, Jessica; et al. (2017). Convergence of semantics and emotional expression within the IFG pars orbitalis Neuroimage. 156, 240–248.
Benga, O. (2005). Intentional communication and the anterior cingulate cortex. Interaction Studies, 6, 201–221.
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
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.
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 536, 338–343.
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. 15, 343–347.
Coudé, G., & Ferrari, P. F. (2018). Reflections on the organization of the cortical motor system and its role in the evolution of communication in primates Interaction Studies.
Craig, A. D. (2009). How do you feel now? the anterior insula and human awareness. Nat. Rev. Neurosci. 10, 59–70.
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.
DeFelipe, J., Alonso-Nanclares, L., Arellano, J. I. (2002): Microstructure of the neocortex: comparative aspects. J Neurocytol 31, 299–316.
Etkin, A., Egner, T., Kalisch, R. (2011). Emotional processing in anterior cingulate and medial prefrontal cortex. Trends Cogn. Sci. 15 (2), 85–93.
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
Falk, D. (2016). Evolution of brain and culture: the neurological and cognitive journey from Australopithecus to Albert Einstein J Anthropological Sciences. 94, 99–111.
Ferrari, P. F., Gerbella, M., Coudé, G., & Rozzi, S. (2017). Two different mirror neuron networks: The sensorimotor (hand) and limbic (face) pathways. Neuroscience 358, 300–315.
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; 84, 135–155.
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.
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.
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.
Horton Lew, C., C. Brown, U. Bellugi, and K. Semendeferi. (2017). Neuron density is decreased in the prefrontal cortex in Williams syndrome. Autism Research 10, 99–112.
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. 11, 419.
Hutsler, J. J., Zhang, H. (2010): Increased dendritic spine densities on cortical projection neurons in autism spectrum disorders. Brain Res 1309, 83–94.
Iacoboni, M., Dapretto, M. (2006). The mirror neuron system and the consequences of its dysfunction. Nat. Rev. Neurosci. 7 (12), 942–951.
Jarvinen, A., Korenberg, J., Bellugi, U. (2013). The social phenotype of Williams syndrome. Current Opinion in Neurobiology 23, 1–9.
Krubitzer, L., Kahn, D. M. (2003). Nature versus nurture revisited: an old idea with a new twist. Progress in Neurobiology 70, 33–52.
Lew, C. H., Semendeferi, K. (2017). Evolutionary Specializations of the Human Limbic System. In: Kaas, J. (ed.), Evolution of Nervous Systems 2e. vol. 4, pp. 277–291. Oxford: Elsevier.
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.
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
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. 119, 52–72
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.
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, 9, 58.
Pessoa, L. (2013). The Cognitive-Emotional Brain: From Interactions to Integration. Cambridge, MA: MIT Press.
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 18, 915–929.
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 108, 13281–13286.
Schumann, C. M., Amaral, D. G. (2006). Stereological analysis of amygdala neuron number in autism. J. Neurosci. 26 (29), 7674–7679.
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.
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.
(2001). Prefrontal cortex in humans and apes: A comparative study of Area 10. Am. J. Phys. Anthropol. 114, 224–241.
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).
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. 421, 52–79.