Skip to content
Frontiers
Search

Neuroscience

Frontiers in Evolutionary Neuroscience ·

Volume 3 - 2012 | https://doi.org/10.3389/fnevo.2011.00011

Continuity, Divergence, and the Evolution of Brain Language Pathways

  • James K. Rilling1,2,3,4*corresponding author
  • Matthew F. Glasser5
  • Saad Jbabdi6
  • Jesper Andersson6
  • Todd M. Preuss3,7,8
  1. 11 Department of Anthropology, Emory University Atlanta, GA, USA
  2. 22 Department of Psychiatry and Behavioral Sciences, Emory University Atlanta, GA, USA
  3. 33 Center for Translational Social Neuroscience, Emory University Atlanta, GA, USA
  4. 44 Yerkes National Primate Research Center, Emory University Atlanta, GA, USA
  5. 55 Department of Anatomy and Neurobiology, Washington University St. Louis, MO, USA
  6. 66 Centre for Functional Magnetic Resonance Imaging of the Brain, University of Oxford Oxford, UK
  7. 77 Division of Neuropharmacology and Neurologic Diseases, Yerkes National Primate Research Center, Emory University Atlanta, GA, USA
  8. 88 Department of Pathology and Laboratory Medicine, Emory University School of Medicine Atlanta, GA, USA
Article metrics0 viewsView details
PDFCiteMetrics

Abstract

Recently, the assumption of evolutionary continuity between humans and non-human primates has been used to bolster the hypothesis that human language is mediated especially by the ventral extreme capsule pathway that mediates auditory object recognition in macaques. Here, we argue for the importance of evolutionary divergence in understanding brain language evolution. We present new comparative data reinforcing our previous conclusion that the dorsal arcuate fasciculus pathway was more significantly modified than the ventral extreme capsule pathway in human evolution. Twenty-six adult human and twenty-six adult chimpanzees were imaged with diffusion-weighted MRI and probabilistic tractography was used to track and compare the dorsal and ventral language pathways. Based on these and other data, we argue that the arcuate fasciculus is likely to be the pathway most essential for higher-order aspects of human language such as syntax and lexical–semantics.

Keywords

References

  1. Aitken P. G. (1981). Cortical control of conditioned and spontaneous vocal behavior in rhesus monkeys. Brain Lang. 13, 171 – 184. doi:10.1016/0093-934X(81)90137-1
  2. Amunts K., Schleicher A., Bürgel U., Mohlberg H., Uylings H., Zilles K. (1999). Broca’s region revisited: cytoarchitecture and intersubject variability. J. Comp. Neurol. 412, 319 – 341. doi:10.1002/(SICI)1096-9861(19990920)412:2<319::AID-CNE10>3.0.CO;2-7
  3. Andersson J. L. R., Skare S., Ashburner J. (2003). How to correct susceptibility distortions in spin-echo echo-planar images: application to diffusion tensor imaging. Neuroimage 20, 870 – 888. doi:10.1016/S1053-8119(03)00336-7
  4. Arbib M. A. (2007). “Premotor cortex and the mirror neuron hypothesis for the evolution of language,” in Evolution of Nervous Systems, Vol. 4, Primates, eds Kaas J. H., Preuss T. M. (Oxford: Elsevier), 417 – 422.
  5. Behrens T., Berg H. J., Jbabdi S., Rushworth M., Woolrich M. (2007). Probabilistic diffusion tractography with multiple fibre orientations: what can we gain? Neuroimage 34, 144 – 155. doi:10.1016/j.neuroimage.2006.09.018
  6. Binder J. R., Desai R. H., Graves W. W., Conant L. L. (2009). Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies. Cereb. Cortex 19, 2767 – 2796. doi:10.1093/cercor/bhp055
  7. Bonin G. V. (1944). “The architecture,” in The Precentral Motor Cortex, ed. Bucy P. C. (Urbana, IL: University of Illinois Press), 7 – 82.
  8. Brodmann K. (1909). Vergleichende Lokalisationslehre der Grosshirnrhinde. Leipzig: Barth (reprinted as Brodmann’s “Localisation in the Cerebral Cortex,” translated and edited by Garey L. J. London: Smith-Gordon, 1994).
  9. Cantalupo C., Oliver J., Smith J., Nir T., Taglialatela J. P., Hopkins W. D. (2009). The chimpanzee brain shows human-like perisylvian asymmetries in white matter. Eur. J. Neurosci. 30, 431 – 438. doi:10.1111/j.1460-9568.2009.06830.x
  10. Crick F., Jones E. (1993). Backwardness of human neuroanatomy. Nature 361, 109 – 110. doi:10.1038/361109a0
  11. Damasio H., Grabowski T. J., Tranel D., Hichwa R. D., Damasio A. R. (1996). A neural basis for lexical retrieval. Nature 380, 499 – 505. doi:10.1038/380499a0
  12. Deacon T. (1997). The Symbolic Species. New York: W. W. Norton.
  13. Deacon T. W. (1992). Cortical connections of the inferior arcuate sulcus cortex in the macaque brain. Brain Res. 573, 8 – 26. doi:10.1016/0006-8993(92)90109-M
  14. Dronkers N. F., Wilkins D. P., Van Valin R. D. Jr., Redfern B. B., Jaeger J. J. (2004). Lesion analysis of the brain areas involved in language comprehension. Cognition 92, 145 – 177. doi:10.1016/j.cognition.2003.11.002
  15. Duffau H. (2008). The anatomo-functional connectivity of language revisited. New insights provided by electrostimulation and tractography. Neuropsychologia 46, 927 – 934. doi:10.1016/j.neuropsychologia.2008.07.017
  16. Fischl B., Rajendran N., Busa E., Augustinack J., Hinds O., Yeo B., Mohlberg H., Amunts K., Zilles K. (2008). Cortical folding patterns and predicting cytoarchitecture. Cereb. Cortex 18, 1973. doi:10.1093/cercor/bhm225
  17. Frey S., Campbell J. S., Pike G. B., Petrides M. (2008). Dissociating the human language pathways with high angular resolution diffusion fiber tractography. J. Neurosci. 28, 11435 – 11444. doi:10.1523/JNEUROSCI.2388-08.2008
  18. Galaburda A. M., Pandya P. N. (1982). “Role of architectonics and connections in the study of primate brain evolution,” in Primate Brain Evolution: Methods and Concepts, eds Armstrong E., Falk D. (New York: Plenum), 203 – 226.
  19. Gannon P. J., Holloway R. L., Broadfield D. C., Braun A. R. (1998). Asymmetry of chimpanzee planum temporale: humanlike pattern of Wernicke’s brain language area homolog. Science 279, 220 – 222. doi:10.1126/science.279.5348.220
  20. Glasser M., Preuss T., Snyder L., Nair G., Rilling J., Zhang X., Li L., Van Essen D. (2011). Comparative Mapping of Cortical Myelin Content in Humans, Chimpanzees, and Macaques Using T1-weighted and T2-weighted MRI. Washington, DC: Society for Neuroscience.
  21. Glasser M. F., Rilling J. K. (2008). DTI tractography of the human brain’s language pathways. Cereb. Cortex 18, 2471 – 2482. doi:10.1093/cercor/bhn011
  22. Glasser M. F., Van Essen D. C. (2011). Mapping human cortical areas in ivo based on myelin content as revealed by T1- and T2-weighted MRI. J. Neurosci. 31, 11597 – 11616. doi:10.1523/JNEUROSCI.2180-11.2011
  23. Grodzinsky Y., Friederici A. D. (2006). Neuroimaging of syntax and syntactic processing. Curr Opin Neurobiol 16, 240 – 246. doi:10.1016/j.conb.2006.03.007
  24. Heffner H. E., Heffner R. S. (1986). Effect of unilateral and bilateral auditory cortex lesions on the discrimination of vocalizations by Japanese macaques. J. Neurophysiol. 56, 683 – 701.
  25. Holloway R. L., Sherwood C. C., Rilling J. K., Hof P. R. (2008). “Evolution, of the brain: in humans – paleoneurology,” in Encyclopedia of Neuroscience, eds Binder M. D., Hirokawa N., Windhorst U., Hirsch M. C. (Springer-Verlag), 1326 – 1334.
  26. Hopkins W. D., Marino L., Rilling J. K., Macgregor L. A. (1998). Planum temporale asymmetries in great apes as revealed by magnetic resonance imaging (MRI). Neuroreport 9, 2913 – 2918. doi:10.1097/00001756-199808240-00043
  27. Hopkins W. D., Taglialatela J. P., Meguerditchian A., Nir T., Schenker N. M., Sherwood C. C. (2008). Gray matter asymmetries in chimpanzees as revealed by voxel-based morphometry. Neuroimage 42, 491 – 497. doi:10.1016/j.neuroimage.2008.05.014
  28. Li L., Preuss T. M., Rilling J. K., Hopkins W. D., Glasser M. F., Kumar B., Nana R., Zhang X., Hu X. (2010). Chimpanzee (Pan troglodytes) precentral corticospinal system asymmetry and handedness: a diffusion magnetic resonance imaging study. PloS ONE 5, e12886. doi:10.1371/journal.pone.0012886
  29. Makris N., Pandya D. N. (2009). The extreme capsule in humans and rethinking of the language circuitry. Brain Struct. Funct. 213, 343 – 358. doi:10.1007/s00429-008-0199-8
  30. Martino J., Brogna C., Robles S. G., Vergani F., Duffau H. (2010). Anatomic dissection of the inferior fronto-occipital fasciculus revisited in the lights of brain stimulation data. Cortex 46, 691 – 699. doi:10.1016/j.cortex.2009.07.015
  31. Morosan P., Schleicher A., Amunts K., Zilles K. (2005). Multimodal architectonic mapping of human superior temporal gyrus. Anat. Embryol. (Berl). 210, 401 – 406. doi:10.1007/s00429-005-0029-1
  32. Nucifora P. G., Verma R., Melhem E. R., Gur R. E., Gur R. C. (2005). Leftward asymmetry in relative fiber density of the arcuate fasciculus. Neuroreport 16, 791 – 794. doi:10.1097/00001756-200505310-00002
  33. Öngür D., Ferry A., Price J. (2003). Architectonic subdivision of the human orbital and medial prefrontal cortex. J. Comp. Neurol. 460, 425 – 449. doi:10.1002/cne.10609
  34. Parker G. J., Luzzi S., Alexander D. C., Wheeler-Kingshott C. A., Ciccarelli O., Lambon Ralph M. A. (2005). Lateralization of ventral and dorsal auditory-language pathways in the human brain. Neuroimage 24, 656 – 666. doi:10.1016/j.neuroimage.2004.08.047
  35. Petrides M., Cadoret G., Mackey S. (2005). Orofacial somatomotor responses in the macaque monkey homologue of Broca’s area. Nature 435, 1235 – 1238. doi:10.1038/nature03628
  36. Petrides M., Pandya D. N. (2002). “Association pathways of the prefrontal cortex and functional observations,” in Principles of Frontal Lobe Function, eds Stuss D. T., Knight R. T. (New York: Oxford University Press), 31 – 50.
  37. Petrides M., Pandya D. N. (2009). Distinct parietal and temporal pathways to the homologues of Broca’s area in the monkey. PLoS Biol. 7, e1000170. doi:10.1371/journal.pbio.1000170
  38. Premack D. (2007). Human and animal cognition: continuity and discontinuity. Proc. Natl. Acad. Sci. U.S.A. 104, 13861 – 13867. doi:10.1073/pnas.0706147104
  39. Preuss T. M. (2000). “What’s human about the human brain?” in The New Cognitive Neurosciences, 2nd Edn., ed. Michael S. Gazzaniga (Cambridge, MA: MIT Press), 1219 – 1234.
  40. Preuss T. M. (2011). The human brain: rewired and running hot. Ann. N. Y. Acad. Sci. 1225 (Suppl. 1), E182 – E191. doi:10.1111/j.1749-6632.2011.06001.x
  41. Price C. J. (2010). The anatomy of language: a review of 100 fMRI studies published in 2009. Ann. N. Y. Acad. Sci. 1191, 62 – 88. doi:10.1111/j.1749-6632.2010.05444.x
  42. Rilling J. K., Glasser M. F., Preuss T. M., Ma X., Zhao T., Hu X., Behrens T. E. (2008). The evolution of the arcuate fasciculus revealed with comparative DTI. Nat. Neurosci. 11, 426 – 428. doi:10.1038/nn2072
  43. Rivas E. (2005). Recent use of signs by chimpanzees (Pan troglodytes) in interactions with humans. J. Comp. Psychol. 119, 404 – 417. doi:10.1037/0735-7036.119.4.404
  44. Rizzolatti G., Arbib M. A. (1998). Language within our grasp. Trends Neurosci. 21, 188 – 194. doi:10.1016/S0166-2236(98)01260-0
  45. Rizzolatti G., Fogassi L. (2007). “Mirror neurons and social cognition,” in The Oxford Handbook of Evolutionary Psychology, eds Dunbar R. I. M., Barrett L. (Oxford: Oxford University Press), 179 – 196.
  46. Romanski L. M., Tian B., Fritz J., Mishkin M., Goldman-Rakic P. S., Rauschecker J. P. (1999). Dual streams of auditory afferents target multiple domains in the primate prefrontal cortex. Nat. Neurosci. 2, 1131 – 1136. doi:10.1038/16056
  47. Saur D., Schelter B., Schnell S., Kratochvil D., Kupper H., Kellmeyer P., Kummerer D., Kloppel S., Glauche V., Lange R., Mader W., Feess D., Timmer J., Weiller C. (2010). Combining functional and anatomical connectivity reveals brain networks for auditory language comprehension. Neuroimage 49, 3187 – 3197. doi:10.1016/j.neuroimage.2009.11.009
  48. Schenker N. M., Hopkins W. D., Spocter M. A., Garrison A. R., Stimpson C. D., Erwin J. M., Hof P. R., Sherwood C. C. (2010). Broca’s area homologue in chimpanzees (Pan troglodytes): probabilistic mapping, asymmetry, and comparison to humans. Cereb. Cortex 20, 730. doi:10.1093/cercor/bhp138
  49. Schmahmann J. D., Pandya D. N., Wang R., Dai G., D’Arceuil H. E., De Crespigny A. J., Wedeen V. J. (2007). Association fibre pathways of the brain: parallel observations from diffusion spectrum imaging and autoradiography. Brain 130, 630 – 653. doi:10.1093/brain/awl359
  50. Sherwood C. C., Subiaul F., Zawidzki T. W. (2008). A natural history of the human mind: tracing evolutionary changes in brain and cognition. J. Anat. 212, 426 – 454. doi:10.1111/j.1469-7580.2008.00868.x
  51. Spocter M. A., Hopkins W. D., Garrison A. R., Bauernfeind A. L., Stimpson C. D., Hof P. R., Sherwood C. C. (2010). Wernicke’s area homologue in chimpanzees (Pan troglodytes) and its relation to the appearance of modern human language. Proc. R. Soc. Lond. B Biol. Sci. 277, 2165. doi:10.1098/rspb.2010.0011
  52. Turken A. U., Dronkers N. F. (2011). The neural architecture of the language comprehension network: converging evidence from lesion and connectivity analyses. Front. Syst. Neurosci. 5: 1. doi:10.3389/fnsys.2011.00001
  53. Ungerleider L. G., Courtney S. M., Haxby J. V. (1998). A neural system for human visual working memory. Proc. Natl. Acad. Sci. U.S.A. 95, 883 – 890. doi:10.1073/pnas.95.3.883
  54. Van Essen D. C., Glasser M. F., Dierker D. L., Harwell J., Coalson T. (2011). Parcellations and hemispheric asymmetries of human cerebral cortex analyzed on surface-based atlases. Cereb. Cortex. doi:10.1093/cercor/bhr291
  55. Van Essen D. C., Dierker D. L. (2007). Surface-based and probabilistic atlases of primate cerebral cortex. Neuron 56, 209 – 225. doi:10.1016/j.neuron.2007.10.015
  56. Vigneau M., Beaucousin V., Herve P. Y., Duffau H., Crivello F., Houde O., Mazoyer B., Tzourio-Mazoyer N. (2006). Meta-analyzing left hemisphere language areas: phonology, semantics, and sentence processing. Neuroimage 30, 1414 – 1432. doi:10.1016/j.neuroimage.2005.11.002
  57. Wallman J. (1992). Aping Language. Cambridge: Cambridge University Press.

Citation

Rilling, J. K., et al. (2012). Continuity, Divergence, and the Evolution of Brain Language Pathways. Frontiers in Evolutionary Neuroscience, Volume 3. https://doi.org/
Received
Accepted
Published
Volume
3 - 2012

Copyright

Copyright © 2012 Rilling, Glasser, Jbabdi, Andersson and Preuss.

License: http://www.frontiersin.org/licenseagreement

*Correspondence: James K. Rilling

Article metrics

Views
0
Downloads
0
Citations
0
Shares
0

Related articles

NeuroscienceNeurobiology of human language and its evolution: primate and non-primate perspectivesConstance Scharff, Angela D. Friederici, Michael PetridesNeuroscienceBirdsong: Is It Music to Their Ears?Sarah E. Earp, Donna L. ManeyNeuroscienceLife History Theory and Social PsychologyDonald F. Sacco, Karol Osipowicz