1887
Volume 19, Issue 1-2
  • ISSN 1572-0373
  • E-ISSN: 1572-0381
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Abstract

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.

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2018-09-17
2024-10-12
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References

  1. Adolphs, R.
    (2001) The neurobiology of social cognition. Current Opinion in Neurobiology, 11(2), 231–239.10.1016/S0959‑4388(00)00202‑6
    https://doi.org/10.1016/S0959-4388(00)00202-6 [Google Scholar]
  2. (2009) The Social Brain: Neural Basis of Social Knowledge. Annu Rev Psychol, 60, 693–716.10.1146/annurev.psych.60.110707.163514
    https://doi.org/10.1146/annurev.psych.60.110707.163514 [Google Scholar]
  3. (2017) How should neuroscience study emotions? By distinguishing emotion states, concepts, and experiences Social Cognitive and Affective Neuroscience, 24–31.
    [Google Scholar]
  4. Allman, J., Hakeem, A., Watson, K.
    (2002) Two phylogenetic specializations in the human brain. Neuroscientist8 (4), 335–346.10.1177/107385840200800409
    https://doi.org/10.1177/107385840200800409 [Google Scholar]
  5. 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), 495–517.10.1007/s00429‑010‑0254‑0
    https://doi.org/10.1007/s00429-010-0254-0 [Google Scholar]
  6. Anderson, D. J., & Adolphs, R.
    (2014) A Framework for Studying Emotions across Species. Cell, 157(1), 187–200.10.1016/j.cell.2014.03.003
    https://doi.org/10.1016/j.cell.2014.03.003 [Google Scholar]
  7. 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 Res15, 1179–1188.10.1101/gr.3944605
    https://doi.org/10.1101/gr.3944605 [Google Scholar]
  8. Arbib, M. A.
    (2012) How the Brain Got Language: The Mirror System Hypothesis. New York & Oxford: Oxford University Press.10.1093/acprof:osobl/9780199896684.001.0001
    https://doi.org/10.1093/acprof:osobl/9780199896684.001.0001
  9. Arbib, M. A., & Bota, M.
    (2003) Language Evolution: Neural Homologies and Neuroinformatics. Neural Networks, 16, 1237–1260.10.1016/j.neunet.2003.08.002
    https://doi.org/10.1016/j.neunet.2003.08.002 [Google Scholar]
  10. Arbib, M. A., & Fellous, J. M.
    (2004) Emotions: from brain to robot. Trends Cogn Sci, 8(12), 554–561.10.1016/j.tics.2004.10.004
    https://doi.org/10.1016/j.tics.2004.10.004 [Google Scholar]
  11. 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]
  12. (1990) The limbic system and culture: an allometric analysis of the neocortex and limbic nuclei. Hum. Nat. 2, 117–136.10.1007/BF02692184
    https://doi.org/10.1007/BF02692184 [Google Scholar]
  13. Barbas, H.
    (2015) General Cortical and Special Prefrontal Connections: Principles from Structure to Function. (Edited by: Hyman, S. E.) Annual Review of Neuroscience38, 269–28910.1146/annurev‑neuro‑071714‑033936
    https://doi.org/10.1146/annurev-neuro-071714-033936 [Google Scholar]
  14. 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), 392–403.10.1002/ajpa.20684
    https://doi.org/10.1002/ajpa.20684 [Google Scholar]
  15. 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), 3035–3054.10.1002/cne.23118
    https://doi.org/10.1002/cne.23118 [Google Scholar]
  16. 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, 1–17.10.3389/fnhum.2014.00277
    https://doi.org/10.3389/fnhum.2014.00277 [Google Scholar]
  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), 263–27910.1016/j.jhevol.2012.12.003
    https://doi.org/10.1016/j.jhevol.2012.12.003 [Google Scholar]
  18. 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.
    [Google Scholar]
  19. Bellugi, U., Lichtenberger, L., Mills, D., Galaburda, A., Korenberg, J. R.
    (1999): Bridging cognition, the brain and molecular genetics: evidence from Williams syndrome. Trends Neurosci22, 197–207.10.1016/S0166‑2236(99)01397‑1
    https://doi.org/10.1016/S0166-2236(99)01397-1 [Google Scholar]
  20. Belyk, Michel; Brown, Steven; Lim, Jessica; et al.
    (2017) Convergence of semantics and emotional expression within the IFG pars orbitalis Neuroimage. 156, 240–248.10.1016/j.neuroimage.2017.04.020
    https://doi.org/10.1016/j.neuroimage.2017.04.020 [Google Scholar]
  21. Benga, O.
    (2005) Intentional communication and the anterior cingulate cortex. Interaction Studies, 6, 201–221.10.1075/is.6.2.04ben
    https://doi.org/10.1075/is.6.2.04ben [Google Scholar]
  22. 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 Cortex23(10):2429–243610.1093/cercor/bhs239
    https://doi.org/10.1093/cercor/bhs239 [Google Scholar]
  23. 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), 163–164.10.1038/nn.2724
    https://doi.org/10.1038/nn.2724 [Google Scholar]
  24. 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. Nature536, 338–343.
  25. 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.
    [Google Scholar]
  26. 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.10.1075/is.17037.cou
    https://doi.org/10.1075/is.17037.cou [Google Scholar]
  27. Craig, A. D.
    (2009) How do you feel now? the anterior insula and human awareness. Nat. Rev. Neurosci. 10, 59–70.10.1038/nrn2555
    https://doi.org/10.1038/nrn2555 [Google Scholar]
  28. Damasio, A. R.
    (1994) Descartes’ Error Grosset/Putnam, New York.
  29. 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), 115–24.10.1159/000102973
    https://doi.org/10.1159/000102973 [Google Scholar]
  30. DeFelipe, J., Alonso-Nanclares, L., Arellano, J. I.
    (2002): Microstructure of the neocortex: comparative aspects. J Neurocytol31, 299–316.10.1023/A:1024130211265
    https://doi.org/10.1023/A:1024130211265 [Google Scholar]
  31. Etkin, A., Egner, T., Kalisch, R.
    (2011) Emotional processing in anterior cingulate and medial prefrontal cortex. Trends Cogn. Sci.15 (2), 85–93.10.1016/j.tics.2010.11.004
    https://doi.org/10.1016/j.tics.2010.11.004 [Google Scholar]
  32. Evrard, H. C., Forro, T., Logothetis, N. K.
    (2012) Von Economo neurons in the anterior insula of the macaque monkey. Neuron74 (3), 482–48910.1016/j.neuron.2012.03.003
    https://doi.org/10.1016/j.neuron.2012.03.003 [Google Scholar]
  33. Falk, D.
    (2016) Evolution of brain and culture: the neurological and cognitive journey from Australopithecus to Albert Einstein J Anthropological Sciences. 94, 99–111.
    [Google Scholar]
  34. Ferrari, P. F., Gerbella, M., Coudé, G., & Rozzi, S.
    (2017) Two different mirror neuron networks: The sensorimotor (hand) and limbic (face) pathways. Neuroscience358, 300–315.10.1016/j.neuroscience.2017.06.052
    https://doi.org/10.1016/j.neuroscience.2017.06.052 [Google Scholar]
  35. 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.
    [Google Scholar]
  36. 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]
  37. Heimer, L. and Van Hoesen G. W.
    (2006) The limbic lobe and its output channels: implications for emotional functions and adaptive behavior. Neuroscience & Biobehavioral Reviews30(2):126–147.10.1016/j.neubiorev.2005.06.006
    https://doi.org/10.1016/j.neubiorev.2005.06.006 [Google Scholar]
  38. 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), 139–142.10.1016/S0304‑3940(01)01964‑4
    https://doi.org/10.1016/S0304-3940(01)01964-4 [Google Scholar]
  39. Horton Lew, C., C. Brown, U. Bellugi, and K. Semendeferi
    (2017) Neuron density is decreased in the prefrontal cortex in Williams syndrome. Autism Research10, 99–112.10.1002/aur.1677
    https://doi.org/10.1002/aur.1677 [Google Scholar]
  40. 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.
    [Google Scholar]
  41. Hutsler, J. J., Zhang, H.
    (2010): Increased dendritic spine densities on cortical projection neurons in autism spectrum disorders. Brain Res1309, 83–94.10.1016/j.brainres.2009.09.120
    https://doi.org/10.1016/j.brainres.2009.09.120 [Google Scholar]
  42. Iacoboni, M., Dapretto, M.
    (2006) The mirror neuron system and the consequences of its dysfunction. Nat. Rev. Neurosci.7 (12), 942–951.10.1038/nrn2024
    https://doi.org/10.1038/nrn2024 [Google Scholar]
  43. Jarvinen, A., Korenberg, J., Bellugi, U.
    (2013) The social phenotype of Williams syndrome. Current Opinion in Neurobiology23, 1–9.10.1016/j.conb.2012.12.006
    https://doi.org/10.1016/j.conb.2012.12.006 [Google Scholar]
  44. Krubitzer, L., Kahn, D. M.
    (2003) Nature versus nurture revisited: an old idea with a new twist. Progress in Neurobiology70, 33–52.10.1016/S0301‑0082(03)00088‑1
    https://doi.org/10.1016/S0301-0082(03)00088-1 [Google Scholar]
  45. LeDoux, J.
    (1996) The Emotional Brain, Simon & Schuster.
    [Google Scholar]
  46. Lew, C. H., Semendeferi, K.
    (2017) Evolutionary Specializations of the Human Limbic System. In: Kaas, J. (ed.), Evolution of Nervous Systems2e.vol.4, pp.277–291. Oxford: Elsevier.10.1016/B978‑0‑12‑804042‑3.00115‑9
    https://doi.org/10.1016/B978-0-12-804042-3.00115-9
  47. 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.10.1007/s00429‑017‑1592‑y
    https://doi.org/10.1007/s00429-017-1592-y [Google Scholar]
  48. 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), 38–5210.1002/cne.902120104
    https://doi.org/10.1002/cne.902120104 [Google Scholar]
  49. 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, 52–7210.1016/j.brainresbull.2015.10.004
    https://doi.org/10.1016/j.brainresbull.2015.10.004 [Google Scholar]
  50. 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), 5268–5273.10.1073/pnas.96.9.5268
    https://doi.org/10.1073/pnas.96.9.5268 [Google Scholar]
  51. 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, 58.10.3389/fnhum.2015.00058
    https://doi.org/10.3389/fnhum.2015.00058 [Google Scholar]
  52. Pessoa, L.
    (2013) The Cognitive-Emotional Brain: From Interactions to Integration. Cambridge, MA: MIT Press.10.7551/mitpress/9780262019569.001.0001
    https://doi.org/10.7551/mitpress/9780262019569.001.0001
  53. 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 Cortex18, 915–929.10.1093/cercor/bhm124
    https://doi.org/10.1093/cercor/bhm124 [Google Scholar]
  54. 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 USA108, 13281–13286.10.1073/pnas.1105108108
    https://doi.org/10.1073/pnas.1105108108 [Google Scholar]
  55. Schumann, C. M., Amaral, D. G.
    (2006) Stereological analysis of amygdala neuron number in autism. J. Neurosci.26 (29), 7674–7679.10.1523/JNEUROSCI.1285‑06.2006
    https://doi.org/10.1523/JNEUROSCI.1285-06.2006 [Google Scholar]
  56. 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), 660–667.10.1002/ana.21055
    https://doi.org/10.1002/ana.21055 [Google Scholar]
  57. 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), 129–155.10.1002/(SICI)1096‑8644(199806)106:2<129::AID‑AJPA3>3.0.CO;2‑L
    https://doi.org/10.1002/(SICI)1096-8644(199806)106:2<129::AID-AJPA3>3.0.CO;2-L [Google Scholar]
  58. (2001) Prefrontal cortex in humans and apes: A comparative study of Area 10. Am. J. Phys. Anthropol. 114, 224–241.10.1002/1096‑8644(200103)114:3<224::AID‑AJPA1022>3.0.CO;2‑I
    https://doi.org/10.1002/1096-8644(200103)114:3<224::AID-AJPA1022>3.0.CO;2-I [Google Scholar]
  59. 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]
  60. 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, 52–79.10.1002/(SICI)1096‑9861(20000522)421:1<52::AID‑CNE4>3.0.CO;2‑O
    https://doi.org/10.1002/(SICI)1096-9861(20000522)421:1<52::AID-CNE4>3.0.CO;2-O [Google Scholar]
  61. Striedter, G. F.
    (2004) Principles of Brain Evolution Sinauer Associates.
    [Google Scholar]
  62. Von Economo, C.
    (1929) The Cytoarchitectonics of the Human Cerebral Cortex. Oxford University Press, Oxford, UK.
  63. 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), 655–664.10.1016/S0896‑6273(03)00679‑2
    https://doi.org/10.1016/S0896-6273(03)00679-2 [Google Scholar]
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