1887
Volume 19, Issue 1-2
  • ISSN 1572-0373
  • E-ISSN: 1572-0381
USD
Buy:$35.00 + Taxes

Abstract

Abstract

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.

Loading

Article metrics loading...

/content/journals/10.1075/is.17039.hec
2018-09-17
2024-09-09
Loading full text...

Full text loading...

References

  1. 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), 816–825.10.1093/cercor/bhk034
    https://doi.org/10.1093/cercor/bhk034 [Google Scholar]
  2. Arbib, M.
    (2012) How the Brain Got Language:Oxford University Press.10.1093/acprof:osobl/9780199896684.001.0001
    https://doi.org/10.1093/acprof:osobl/9780199896684.001.0001 [Google Scholar]
  3. Baldwin, J. Mark
    (1896) A New Factor in Evolution. The American Naturalist, 30(354), 441–451.10.2307/2453130
    https://doi.org/10.2307/2453130 [Google Scholar]
  4. Bateson, P.
    (2004) The active role of behaviour in evolution. Biol Phi/as, 19(2), 283–298.10.1023/B:BIPH.0000024468.12161.83
    https://doi.org/10.1023/B:BIPH.0000024468.12161.83 [Google Scholar]
  5. Bogin, B.
    (1997) Evolutionary Hypotheses for Human Childhood. Yearbook of Physical Anthropology, 40, 63–8910.1002/(SICI)1096‑8644(1997)25+<63::AID‑AJPA3>3.0.CO;2‑8
    https://doi.org/10.1002/(SICI)1096-8644(1997)25+<63::AID-AJPA3>3.0.CO;2-8 [Google Scholar]
  6. Buckner, R. L., & Krienen, F. M.
    (2013) The evolution of distributed association networks in the human brain. Trends Cogn Sci, 17(12), 648–665.10.1016/j.tics.2013.09.017
    https://doi.org/10.1016/j.tics.2013.09.017 [Google Scholar]
  7. 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), 683–693.10.1007/s10071‑011‑0403‑8
    https://doi.org/10.1007/s10071-011-0403-8 [Google Scholar]
  8. 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), 1148–1167.10.1016/j.neuroimage.2009.12.112
    https://doi.org/10.1016/j.neuroimage.2009.12.112 [Google Scholar]
  9. Chartrand, T. L., & Bargh, J. A.
    (1999) The chameleon effect: the perception-behavior link and social interaction. J Pers Soc Psycho/, 76(6), 893–910.10.1037/0022‑3514.76.6.893
    https://doi.org/10.1037/0022-3514.76.6.893 [Google Scholar]
  10. 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), 1505–1516.10.1162/0898929042568505
    https://doi.org/10.1162/0898929042568505 [Google Scholar]
  11. 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), 2111–2123.10.1098/rstb.2010.0344
    https://doi.org/10.1098/rstb.2010.0344 [Google Scholar]
  12. Fitch, W. T., Huber, L., & Bugnyar, T.
    (2010) Social cognition and the evolution of language: constructing cognitive phylogenies. Neuron, 65(6), 795–814.10.1016/j.neuron.2010.03.011
    https://doi.org/10.1016/j.neuron.2010.03.011 [Google Scholar]
  13. Flechsig, P. E.
    (1920) Anatomie des menschlichen Gehirns und Ruckenmarks auf myelogenetischer Grundlage. G. Thieme (in German).
    [Google Scholar]
  14. 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), 397–405.10.1016/j.cogbrainres.2004.11.010
    https://doi.org/10.1016/j.cogbrainres.2004.11.010 [Google Scholar]
  15. 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), 529–546.10.1016/0028‑3932(90)90032‑J
    https://doi.org/10.1016/0028-3932(90)90032-J [Google Scholar]
  16. 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), 14799–14804.10.1073/pnas.1512646112
    https://doi.org/10.1073/pnas.1512646112 [Google Scholar]
  17. 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), 20130575.10.1098/rspb.2013.0575
    https://doi.org/10.1098/rspb.2013.0575 [Google Scholar]
  18. (2014) Modular structure facilitates mosaic evolution of the brain in chimpanzees and humans. Nat Commun, 5, 4469.10.1038/ncomms5469
    https://doi.org/10.1038/ncomms5469 [Google Scholar]
  19. 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), 585–598.10.1006/mpev.1998.0495
    https://doi.org/10.1006/mpev.1998.0495 [Google Scholar]
  20. Greenfield, P. M.
    (1991) Language, tools, and brain: the development and evolution of hierarchically organized sequential behavior. Behav. Brain Sci., 14, 531–595.10.1017/S0140525X00071235
    https://doi.org/10.1017/S0140525X00071235 [Google Scholar]
  21. 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), 2231–2235.10.1016/j.cub.2012.09.041
    https://doi.org/10.1016/j.cub.2012.09.041 [Google Scholar]
  22. Hayes, K. J., & Hayes, C.
    (1952) Imitation in a home-raised chimpanzee. J Comp Physio/ Psycho/, 45(5), 450–459.10.1037/h0053609
    https://doi.org/10.1037/h0053609 [Google Scholar]
  23. 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, 74–76.10.1016/j.plrev.2016.01.010
    https://doi.org/10.1016/j.plrev.2016.01.010 [Google Scholar]
  24. 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, 124–137.10.1016/j.neuroimage.2014.12.039
    https://doi.org/10.1016/j.neuroimage.2014.12.039 [Google Scholar]
  25. 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, 124–137.10.1016/j.neuroimage.2014.12.039
    https://doi.org/10.1016/j.neuroimage.2014.12.039 [Google Scholar]
  26. 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), 2315–2331.10.1007/s00429‑014‑0789‑6
    https://doi.org/10.1007/s00429-014-0789-6 [Google Scholar]
  27. 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), 1014–1024.10.1093/cercor/bhs097
    https://doi.org/10.1093/cercor/bhs097 [Google Scholar]
  28. 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), 14117–14134.10.1523/JNEUROSCl.2172‑13.2013
    https://doi.org/10.1523/JNEUROSCl.2172-13.2013 [Google Scholar]
  29. 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), 13135–13140.10.1073/pnas.1001229107
    https://doi.org/10.1073/pnas.1001229107 [Google Scholar]
  30. 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), 971–977.10.1111/j.1467‑9280.2007.02011.x
    https://doi.org/10.1111/j.1467-9280.2007.02011.x [Google Scholar]
  31. Horner, V., & Whiten, A.
    (2005) Causal knowledge and imitation/emulation switching in chimpanzees (Pan troglodytes) and children (Homo sapiens). Anim Cogn, 8(3), 164–181.10.1007/s10071‑004‑0239‑6
    https://doi.org/10.1007/s10071-004-0239-6 [Google Scholar]
  32. Inoue-Nakamura, N., & Matsuzawa, T.
    (1997) Development of stone tool use by wild chimpanzees (Pan troglodytes). J Comp Psycho/, 111(2), 159–173.10.1037/0735‑7036.111.2.159
    https://doi.org/10.1037/0735-7036.111.2.159 [Google Scholar]
  33. Kaas, J. H.
    (2012) The evolution of neocortex in primates. Prag Brain Res, 195, 91–102.10.1016/B978‑0‑444‑53860‑4.00005‑2
    https://doi.org/10.1016/B978-0-444-53860-4.00005-2 [Google Scholar]
  34. 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), 6620–6626.10.1523/JNEUROSCl.5864‑10.2011
    https://doi.org/10.1523/JNEUROSCl.5864-10.2011 [Google Scholar]
  35. Kaneko, T., & Tomonaga, M.
    (2012) Relative contributions of goal representation and kinematic information to self-monitoring by chimpanzees and humans. Cognition, 125(2), 168–178.10.1016/j.cognition.2012.07.006
    https://doi.org/10.1016/j.cognition.2012.07.006 [Google Scholar]
  36. Human-specific transcriptional networks in the brain
    Human-specific transcriptional networks in the brain. Neuron, 75(4), 601–617.10.1016/j.neuron.2012.05.034
    https://doi.org/10.1016/j.neuron.2012.05.034 [Google Scholar]
  37. 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), 922–930.10.1016/j.neuron.2009.12.010
    https://doi.org/10.1016/j.neuron.2009.12.010 [Google Scholar]
  38. Marshall-Pescini, S., & Whiten, A.
    (2008) Chimpanzees (Pan troglodytes) and the question of cumulative culture: an experimental approach. Anim Cogn, 11(3), 449–456.10.1007/s10071‑007‑0135‑y
    https://doi.org/10.1007/s10071-007-0135-y [Google Scholar]
  39. 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), 16480–16485.10.1073/pnas.1117943109
    https://doi.org/10.1073/pnas.1117943109 [Google Scholar]
  40. 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), 975–980.10.1016/j.neubiorev.2009.03.010
    https://doi.org/10.1016/j.neubiorev.2009.03.010 [Google Scholar]
  41. Ojemann, G. A.
    (1991) Cortical organization of language. J Neurosci, 11(8), 2281–2287.10.1523/JNEUROSCI.11‑08‑02281.1991
    https://doi.org/10.1523/JNEUROSCI.11-08-02281.1991 [Google Scholar]
  42. 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]
  43. Paukner, A., Suomi, S. J., Visalberghi, E., & Ferrari, P. F.
    (2009) Capuchin monkeys display affiliation toward humans who imitate them. Science, 325(5942), 880–883.10.1126/science.1176269
    https://doi.org/10.1126/science.1176269 [Google Scholar]
  44. 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), 11523–11539.10.1523/JNEUROSCl.2040‑09.2009
    https://doi.org/10.1523/JNEUROSCl.2040-09.2009 [Google Scholar]
  45. Petrides, M.
    (2005) Lateral prefrontal cortex: architectonic and functional organization. Philos Trans R Soc Land B Biol Sci, 360(1456), 781–795.10.1098/rstb.2005.1631
    https://doi.org/10.1098/rstb.2005.1631 [Google Scholar]
  46. 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), 291–310.10.1046/j.1460‑9568.2001.02090.x
    https://doi.org/10.1046/j.1460-9568.2001.02090.x [Google Scholar]
  47. (2009) Distinct parietal and temporal pathways to the homologues of Broca’s area in the monkey. PLoS Biol, 7(8), e1000170.10.1371/journal.pbio.1000170
    https://doi.org/10.1371/journal.pbio.1000170 [Google Scholar]
  48. Preuss, T. M., Caceres, M., Oldham, M. C., & Geschwind, D. H.
    (2004) Human brain evolution: insights from microarrays. Nat Rev Genet, 5(11), 850–860.10.1038/nrg1469
    https://doi.org/10.1038/nrg1469 [Google Scholar]
  49. Pulvermuller, F., & Fadiga, L.
    (2010) Active perception: sensorimotor circuits as a cortical basis for language. Nat Rev Neurosci, 11(5), 351–360.10.1038/nrn2811
    https://doi.org/10.1038/nrn2811 [Google Scholar]
  50. Raos, V., Evangeliou, M. N., & Savaki, H. E.
    (2004) Observation of action: grasping with the mind’s hand. Neuroimage, 23(1), 193–201.10.1016/j.neuroimage.2004.04.024
    https://doi.org/10.1016/j.neuroimage.2004.04.024 [Google Scholar]
  51. (2007) Mental simulation of action in the service of action perception. J Neurosci, 27(46), 12675–12683.10.1523/JNEUROSCl.2988‑07.2007
    https://doi.org/10.1523/JNEUROSCl.2988-07.2007 [Google Scholar]
  52. Rizzolatti, G., Fadiga, L., Gallese, V., & Fogassi, L.
    (1996) Premotor cortex and the recognition of motor actions. Brain Res Cogn Brain Res, 3(2), 131–141.10.1016/0926‑6410(95)00038‑0
    https://doi.org/10.1016/0926-6410(95)00038-0 [Google Scholar]
  53. 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), 78–91.10.1002/ajpa.22778
    https://doi.org/10.1002/ajpa.22778 [Google Scholar]
  54. 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), 1389–1417.10.1093/cercor/bhj076
    https://doi.org/10.1093/cercor/bhj076 [Google Scholar]
  55. 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), 389–394.10.1007/s00221‑006‑0379‑9
    https://doi.org/10.1007/s00221-006-0379-9 [Google Scholar]
  56. 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), 117–128.10.1002/cne.21792
    https://doi.org/10.1002/cne.21792 [Google Scholar]
  57. 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), 614–621.10.1111/desc.12237
    https://doi.org/10.1111/desc.12237 [Google Scholar]
  58. Stout, D., & Chaminade, T.
    (2012) Stone tools, language and the brain in human evolution. Philos Trans R Soc Land B Biol Sci, 367(1585), 75–87.10.1098/rstb.2011.0099
    https://doi.org/10.1098/rstb.2011.0099 [Google Scholar]
  59. Stout, D., Passingham, R., Frith, C., Apel, J., & Chaminade, T.
    (2011) Technology, expertise and social cognition in human evolution. Eur J Neurosci, 33(7), 1328–1338.10.1111/j.1460‑9568.2011.07619.x
    https://doi.org/10.1111/j.1460-9568.2011.07619.x [Google Scholar]
  60. 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), 1939–1949.10.1098/rstb.2008.0001
    https://doi.org/10.1098/rstb.2008.0001 [Google Scholar]
  61. Sussman, R. W., Tab Rasmussen, D., & Raven, P. H.
    (2013) Rethinking primate origins again. Am J Primato/, 75(2), 95–106.10.1002/ajp.22096
    https://doi.org/10.1002/ajp.22096 [Google Scholar]
  62. 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), 155–165.10.1016/S0896‑6273(01)00337‑3 [pii]
    https://doi.org/10.1016/S0896-6273(01)00337-3 [Google Scholar]
  63. 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), 719–741.10.1006/jhev.1999.0304
    https://doi.org/10.1006/jhev.1999.0304 [Google Scholar]
  64. 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), 413–415.10.1126/science.1073574
    https://doi.org/10.1126/science.1073574 [Google Scholar]
  65. Visalberghi, E., & Fragaszy, D. M.
    (2002) “Do Monkeys Ape?” Ten Years After. InC. N. K. Dautenhahn (Ed.), Imitation in animals and artefacts (pp.471–499). Cambridge, MA: MIT Press.
    [Google Scholar]
  66. Weber, Bruce H., & Depew, David J.
    (Eds.) (2003) Evolution and learning: the Baldwin effect reconsidered. Cambridge, Mass.: MIT Press.
    [Google Scholar]
  67. 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), 2417–2428.10.1098/rstb.2009.0069
    https://doi.org/10.1098/rstb.2009.0069 [Google Scholar]
  68. Yakovlev, P. I., & Lecours, A. R.
    (1966) The myelinogenic cycles of regional maturation of the brain. InA. Minkovski (Ed.), Regional Development of the Brain in Early Life (pp.3–70). Oxford, UK: Blackwell.
    [Google Scholar]
  69. Zhong, Y. M., & Rockland, K. S.
    (2003) Inferior parietal lobule projections to anterior inferotemporal cortex (area TE) in macaque monkey. Cereb Cortex, 13(5), 527–540.10.1093/cercor/13.5.527
    https://doi.org/10.1093/cercor/13.5.527 [Google Scholar]
/content/journals/10.1075/is.17039.hec
Loading
/content/journals/10.1075/is.17039.hec
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was successful
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error