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How the Brain Got Language – Towards a New Road Map
Edited by Michael A. Arbib
[Benjamins Current Topics 112] 2020
► pp. 54–69

Plasticity, innateness, and the path to language in the primate brain

Comparing macaque, chimpanzee and human circuitry for visuomotor integration

| Georgia State University

Many researchers consider language to be definitionally unique to humans. However, increasing evidence suggests that language emerged via a series of adaptations to neural systems supporting earlier capacities for visuomotor integration and manual action. This paper reviews comparative neuroscience evidence for the evolutionary progression of these adaptations. An outstanding question is how to mechanistically explain the emergence of new capacities from pre-existing circuitry. One possibility is that human brains may have undergone selection for greater plasticity, reducing the extent to which brain organization is hard-wired and increasing the extent to which it is shaped by socially transmitted, learned behaviors. Mutations that made these new abilities easier or faster to learn would have undergone positive selection, and over time, the neural changes once associated with individual neural plasticity would tend to become heritable, innate, and fixed. Clearly, though, language is not entirely “innate;” it does not emerge without the requisite environmental input and experience. Thus, a mechanistic explanation for the evolution of language must address the inherent trade-off between the evolutionary pressure for underlying neural systems to be flexible and sensitive to environmental input vs. the tendency over time for continually adaptive behaviors to become reliably expressed in an early-emerging, canalized, less flexible manner.

Keywords: action perception, tool use, white matter, diffusion tensor imaging, superior longitudinal fasciculus, dorsal stream, evolution, chimpanzees, macaques
Article outline
  • Introduction: Comparative neuroscience, exaptation, and language
    • LCA-m: Early primate adaptations for the visual control of action
    • LCA-c: Hominid dorsal stream adaptations for social transmission of learned skills
    • Human-specific adaptations: Integrating cognitive control and action sequencing with high-fidelity representations of action details
  • The chicken or the egg: Continuity, divergence, and the environmental context for change in brain-behavior evolution
    • Flexibility and environmental sensitivity
    • Specificity and innateness
  • Toward a new road map
  • References
Published online: 11 August 2020
DOI logo
https://doi.org/10.1075/bct.112.05hec
References
Anwander, A., Tittgemeyer, M., von Cramon, D. Y., Friederici, A. D., & Knosche, T. R.
(2007) Connectivity-Based Parcellation of Broca’s Area. Cereb Cortex, 17(4), 816–825. DOI logoGoogle Scholar
Arbib, M.
(2012) How the Brain Got Language: Oxford University Press. DOI logoGoogle Scholar
Baldwin, J. Mark
(1896) A New Factor in Evolution. The American Naturalist, 30(354), 441–451.DOI logoGoogle Scholar
Bateson, P.
(2004) The active role of behaviour in evolution. Biol Phi/as, 19(2), 283–298. DOI logoGoogle Scholar
Bogin, B.
(1997) Evolutionary Hypotheses for Human Childhood. Yearbook of Physical Anthropology, 40, 63–89 DOI logoGoogle Scholar
Buckner, R. L., & Krienen, F. M.
(2013) The evolution of distributed association networks in the human brain. Trends Cogn Sci, 17(12), 648–665. DOI logoGoogle Scholar
Byrne, R. W., Hobaiter, C., & Klailova, M.
(2011) Local traditions in gorilla manual skill: evidence for observational learning of behavioral organization. Anim Cogn, 14(5), 683–693. DOI logoGoogle Scholar
Caspers, S., Zilles, K., Laird, A. R., & Eickhoff, S. B.
(2010) ALE meta-analysis of action observation and imitation in the human brain. Neuroimage, 50(3), 1148–1167. DOI logoGoogle Scholar
Chartrand, T. L., & Bargh, J. A.
(1999) The chameleon effect: the perception-behavior link and social interaction. J Pers Soc Psycho/, 76(6), 893–910. DOI logoGoogle Scholar
Denys, K., Vanduffel, W., Fize, O., Nelissen, K., Sawamura, H., Georgieva, S., … Orban, G. A.
(2004) Visual activation in prefrontal cortex is stronger in monkeys than in humans. J Cogn Neurosci, 16(9), 1505–1516. DOI logoGoogle Scholar
Finlay, B. L., Hinz, F., & Darlington, R. B.
(2011) Mapping behavioural evolution onto brain evolution: the strategic roles of conserved organization in individuals and species. Phi/as Trans R Soc Land B Biol Sci, 366(1574), 2111–2123. DOI logoGoogle Scholar
Fitch, W. T., Huber, L., & Bugnyar, T.
(2010) Social cognition and the evolution of language: constructing cognitive phylogenies. Neuron, 65(6), 795–814. DOI logoGoogle Scholar
Flechsig, P. E.
(1920) Anatomie des menschlichen Gehirns und Ruckenmarks auf myelogenetischer Grundlage. G. Thieme (in German).Google Scholar
Frey, S. H., Vinton, D., Norlund, R., & Grafton, S. T.
(2005) Cortical topography of human anterior intraparietal cortex active during visually guided grasping. Brain Res Cogn Brain Res, 23(2–3), 397–405. DOI logoGoogle Scholar
Galaburda, A. M., Rosen, G. D., & Sherman, G. F.
(1990) Individual variability in cortical organization: its relationship to brain laterality and implications to function. Neuropsycho/ogia, 28(6), 529–546. DOI logoGoogle Scholar
Gomez-Robles, A., Hopkins, W. D., Schapiro, S. J., & Sherwood, C. C.
(2015) Relaxed genetic control of cortical organization in human brains compared with chimpanzees. Proc Natl Acad Sci U S A, 112(48), 14799–14804. DOI logoGoogle Scholar
Gomez-Robles, A., Hopkins, W. D., & Sherwood, C. C.
(2013) Increased morphological asymmetry, evolvability and plasticity in human brain evolution. Proc Biol Sci, 280(1761), 20130575. DOI logoGoogle Scholar
(2014) Modular structure facilitates mosaic evolution of the brain in chimpanzees and humans. Nat Commun, 5, 4469. DOI logoGoogle Scholar
Goodman, M., Porter, C. A., Czelusniak, J., Page, S. L., Schneider, H., Shoshani, J., … Groves, C. P.
(1998) Toward a phylogenetic classification of Primates based on DNA evidence complemented by fossil evidence. Mol Phylogenet Evol, 9(3), 585–598. DOI logoGoogle Scholar
Greenfield, P. M.
(1991) Language, tools, and brain: the development and evolution of hierarchically organized sequential behavior. Behav. Brain Sci., 14, 531–595. DOI logoGoogle Scholar
Gruber, T., Singleton, I., & van Schaik, C.
(2012) Sumatran orangutans differ in their cultural knowledge but not in their cognitive abilities. Curr Biol, 22(23), 2231–2235. DOI logoGoogle Scholar
Hayes, K. J., & Hayes, C.
(1952) Imitation in a home-raised chimpanzee. J Comp Physio/ Psycho/, 45(5), 450–459. DOI logoGoogle Scholar
Hecht, E.
(2016) Adaptations to vision-for-action in primate brain evolution: Comment on “Towards a Computational Comparative Neuroprimatology: Framing the language-ready brain” by Michael A. Arbib. Phys Life Rev, 16, 74–76. DOI logoGoogle Scholar
Hecht, E., Gutman, D. A., Bradley, B. A., Preuss, T. M., & Stout, D.
(2015) Virtual dissection and comparative connectivity of the superior longitudinal fasciculus in chimpanzees and humans. Neuroimage, 108, 124–137.DOI logoGoogle Scholar
Hecht, E. E., Gutman, D. A., Bradley, B. A., Preuss, T. M., & Stout, D.
(2015) Virtual dissection and comparative connectivity of the superior longitudinal fasciculus in chimpanzees and humans. Neuroimage, 108, 124–137. DOI logoGoogle Scholar
Hecht, E. E., Gutman, D. A., Khreisheh, N., Taylor, S. V., Kilner, J., Faisal, A. A., … Stout, D.
(2015) Acquisition of Paleolithic toolmaking abilities involves structural remodeling to inferior frontoparietal regions. Brain Struct Funct, 220(4), 2315–2331. DOI logoGoogle Scholar
Hecht, E. E., Gutman, D. A., Preuss, T. M., Sanchez, M. M., Parr, L. A., & Rilling, J. K.
(2013) Process versus product in social learning: comparative diffusion tensor imaging of neural systems for action execution-observation matching in macaques, chimpanzees, and humans. Cereb Cortex, 23(5), 1014–1024. DOI logoGoogle Scholar
Hecht, E. E., Murphy, L. E., Gutman, D. A., Votaw, J. R., Schuster, D. M., Preuss, T. M., … Parr, L. A.
(2013) Differences in neural activation for object-directed grasping in chimpanzees and humans. J Neurosci, 33(35), 14117–14134.DOI logoGoogle Scholar
Hill, J., lnder, T., Neil, J., Dierker, D., Harwell, J., & Van Essen, D.
(2010) Similar patterns of cortical expansion during human development and evolution. Proc Natl Acad Sci US A, 107(29), 13135–13140. DOI logoGoogle Scholar
Hopkins, W. D., Russell, J. L., & Cantalupo, C.
(2007) Neuroanatomical correlates of handedness for tool use in chimpanzees (Pan troglodytes): implication for theories on the evolution of language. Psycho/ Sci, 18(11), 971–977. DOI logoGoogle Scholar
Horner, V., & Whiten, A.
(2005) Causal knowledge and imitation/emulation switching in chimpanzees (Pan troglodytes) and children (Homo sapiens). Anim Cogn, 8(3), 164–181. DOI logoGoogle Scholar
Inoue-Nakamura, N., & Matsuzawa, T.
(1997) Development of stone tool use by wild chimpanzees (Pan troglodytes). J Comp Psycho/, 111(2), 159–173. DOI logoGoogle Scholar
Kaas, J. H.
(2012) The evolution of neocortex in primates. Prag Brain Res, 195, 91–102. DOI logoGoogle Scholar
Kanai, R., Dong, M. Y., Bahrami, B., & Rees, G.
(2011) Distractibility in daily life is reflected in the structure and function of human parietal cortex. J Neurosci, 31(18), 6620–6626.DOI logoGoogle Scholar
Kaneko, T., & Tomonaga, M.
(2012) Relative contributions of goal representation and kinematic information to self-monitoring by chimpanzees and humans. Cognition, 125(2), 168–178. DOI logoGoogle Scholar
Human-specific transcriptional networks in the brain
Neuron, 75(4), 601–617. DOI logo
Kraskov, A., Dancause, N., Quallo, M. M., Shepherd, S., & Lemon, R. N.
(2009) Corticospinal neurons in macaque ventral premotor cortex with mirror properties: a potential mechanism for action suppression? Neuron, 64(6), 922–930. DOI logoGoogle Scholar
Marshall-Pescini, S., & Whiten, A.
(2008) Chimpanzees (Pan troglodytes) and the question of cumulative culture: an experimental approach. Anim Cogn, 11(3), 449–456. DOI logoGoogle Scholar
Miller, D. J., Duka, T., Stimpson, C. D., Schapiro, S. J., Baze, W. B., McArthur, M. J., … Sherwood, C. C.
(2012) Prolonged myelination in human neocortical evolution. Proc Natl Acad Sci US A, 109(41), 16480–16485. DOI logoGoogle Scholar
Molenberghs, P., Cunnington, R., & Mattingley, J. B.
(2009) Is the mirror neuron system involved in imitation? A short review and meta-analysis. Neurosci Biobehav Rev, 33(7), 975–980. DOI logoGoogle Scholar
Ojemann, G. A.
(1991) Cortical organization of language. J Neurosci, 11(8), 2281–2287. DOI logoGoogle Scholar
Osborn, H. F.
(1896) A mode of evolution requiring neither natural selection nor the inheritance of acquired characters. Transactions of the New York Academy of Sciences, 15, 141–148.Google Scholar
Paukner, A., Suomi, S. J., Visalberghi, E., & Ferrari, P. F.
(2009) Capuchin monkeys display affiliation toward humans who imitate them. Science, 325(5942), 880–883. DOI logoGoogle Scholar
Peeters, R., Simone, L., Nelissen, K., Fabbri-Destro, M., Vanduffel, W., Rizzolatti, G., & Orban, G. A.
(2009) The representation of tool use in humans and monkeys: common and uniquely human features. J Neurosci, 29(37), 11523–11539.DOI logoGoogle Scholar
Petrides, M.
(2005) Lateral prefrontal cortex: architectonic and functional organization. Philos Trans R Soc Land B Biol Sci, 360(1456), 781–795. DOI logoGoogle Scholar
Petrides, M., & Pandya, D. N.
(2002) Comparative cytoarchitectonic analysis of the human and the macaque ventrolateral prefrontal cortex and corticocortical connection patterns in the monkey. Eur J Neurosci, 16(2), 291–310. DOI logoGoogle Scholar
(2009) Distinct parietal and temporal pathways to the homologues of Broca’s area in the monkey. PLoS Biol, 7(8), e1000170. DOI logoGoogle Scholar
Preuss, T. M., Caceres, M., Oldham, M. C., & Geschwind, D. H.
(2004) Human brain evolution: insights from microarrays. Nat Rev Genet, 5(11), 850–860. DOI logoGoogle Scholar
Pulvermuller, F., & Fadiga, L.
(2010) Active perception: sensorimotor circuits as a cortical basis for language. Nat Rev Neurosci, 11(5), 351–360. DOI logoGoogle Scholar
Raos, V., Evangeliou, M. N., & Savaki, H. E.
(2004) Observation of action: grasping with the mind’s hand. Neuroimage, 23(1), 193–201. DOI logoGoogle Scholar
(2007) Mental simulation of action in the service of action perception. J Neurosci, 27(46), 12675–12683.DOI logoGoogle Scholar
Rizzolatti, G., Fadiga, L., Gallese, V., & Fogassi, L.
(1996) Premotor cortex and the recognition of motor actions. Brain Res Cogn Brain Res, 3(2), 131–141. DOI logoGoogle Scholar
Roffman, I., Savage-Rumbaugh, S., Rubert-Pugh, E., Stadler, A., Ronen, A., & Nevo, E.
(2015) Preparation and use of varied natural tools for extractive foraging by bonobos (Pan Paniscus). Am J Phys Anthropol, 158(1), 78–91. DOI logoGoogle Scholar
Rozzi, S., Calzavara, R., Belmalih, A., Borra, E., Gregoriou, G. G., Matelli, M., & Luppino, G.
(2006) Cortical connections of the inferior parietal cortical convexity of the macaque monkey. Cereb Cortex, 16(10), 1389–1417. DOI logoGoogle Scholar
Ryan, S., Bonilha, L., & Jackson, S. R.
(2006) Individual variation in the location of the parietal eye fields: a TMS study. Exp Brain Res, 173(3), 389–394. DOI logoGoogle Scholar
Schenker, N. M., Buxhoeveden, D. P., Blackmon, W. L., Amunts, K., Zilles, K., & Semendeferi, K.
(2008) A comparative quantitative analysis of cytoarchitecture and minicolumnar organization in Broca’s area in humans and great apes. J Comp Neural, 510(1), 117–128. DOI logoGoogle Scholar
Sclafani, V., Paukner, A., Suomi, S. J., & Ferrari, P. F.
(2015) Imitation promotes affiliation in infant macaques at risk for impaired social behaviors. Dev Sci, 18(4), 614–621. DOI logoGoogle Scholar
Stout, D., & Chaminade, T.
(2012) Stone tools, language and the brain in human evolution. Philos Trans R Soc Land B Biol Sci, 367(1585), 75–87. DOI logoGoogle Scholar
Stout, D., Passingham, R., Frith, C., Apel, J., & Chaminade, T.
(2011) Technology, expertise and social cognition in human evolution. Eur J Neurosci, 33(7), 1328–1338. DOI logoGoogle Scholar
Stout, D., Toth, N., Schick, K., & Chaminade, T.
(2008) Neural correlates of Early Stone Age toolmaking: technology, language and cognition in human evolution. Philos Trans R Soc Land B Biol Sci, 363(1499), 1939–1949. DOI logoGoogle Scholar
Sussman, R. W., Tab Rasmussen, D., & Raven, P. H.
(2013) Rethinking primate origins again. Am J Primato/, 75(2), 95–106. DOI logoGoogle Scholar
Umiltà, M. A., Kohler, E., Gallese, V., Fogassi, L., Fadiga, L., Keysers, C., & Rizzolatti, G.
(2001) I know what you are doing. A neurophysiological study. Neuron, 31(1), 155–165. DOI logo [pii]Google Scholar
van Schaik, C. P., Deaner, R. O., & Merrill, M. Y.
(1999) The conditions for tool use in primates: implications for the evolution of material culture. J Hum Evol, 36(6), 719–741. DOI logoGoogle Scholar
Vanduffel, W., Fize, D., Peuskens, H., Denys, K., Sunaert, S., Todd, J. T., & Orban, G. A.
(2002) Extracting 3D from motion: differences in human and monkey intraparietal cortex. Science, 298(5592), 413–415. DOI logoGoogle Scholar
Visalberghi, E., & Fragaszy, D. M.
(2002) “Do Monkeys Ape?” Ten Years After. In C. N. K. Dautenhahn (Ed.), Imitation in animals and artefacts (pp. 471–499). Cambridge, MA: MIT Press.Google Scholar
Weber, Bruce H., & Depew, David J.
(Eds.) (2003) Evolution and learning: the Baldwin effect reconsidered. Cambridge, Mass.: MIT Press.Google Scholar
Whiten, A., McGuigan, N., Marshall-Pescini, S., & Hopper, L. M.
(2009) Emulation, imitation, overimitation and the scope of culture for child and chimpanzee. Philos Trans R Soc Lond B Biol Sci, 364(1528), 2417–2428. DOI logoGoogle Scholar
Yakovlev, P. I., & Lecours, A. R.
(1966) The myelinogenic cycles of regional maturation of the brain. In A. Minkovski (Ed.), Regional Development of the Brain in Early Life (pp. 3–70). Oxford, UK: Blackwell.Google Scholar
Zhong, Y. M., & Rockland, K. S.
(2003) Inferior parietal lobule projections to anterior inferotemporal cortex (area TE) in macaque monkey. Cereb Cortex, 13(5), 527–540. DOI logoGoogle Scholar