Skip to main content
Log in

Hemispheric asymmetry in the fusiform gyrus distinguishes Homo sapiens from chimpanzees

  • Original Article
  • Published:
Brain Structure and Function Aims and scope Submit manuscript

Abstract

While the neural basis for linguistic communication has been linked to brain structural asymmetries found only in humans (wider connective spacing is found between the minicolumns of neurons in the left hemisphere language areas), it is unknown if the opposite microanatomical asymmetry exists in the fusiform gyrus which typically supports a right hemisphere bias for face processing. Unlike language, face processing is an ability shared with chimpanzees and, as Darwin observed, the widespread use of facial expressions in animal communication suggests a biological basis. We tested the principle that minicolumn asymmetry follows typical functional dominance in humans, and tested its evolutionary continuity, by measuring minicolumn width, neuronal size and density in the mid-fusiform cortex in 14 humans and 14 chimpanzees. We found that microanatomical asymmetry distinguishes humans from chimpanzees although the direction of asymmetry is the same as in language areas—the right hemisphere contained narrower minicolumns and smaller pyramidal neurons, as in auditory language areas. Uniformly narrow minicolumns in chimpanzees and in the human right hemisphere are consistent with mechanistic predictions supporting the apparent bias towards holistic face processing. Wider minicolumns and larger neurons in the human left hemisphere may be consistent with a language function such as word-form processing. Microanatomical asymmetry in the neocortex therefore provides a correlate of hemispheric specialisation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Amunts K, Schleicher A, Bürgel U, Mohlberg H, Uylings HBMl, Zilles K (1999) Broca’s region revisited: cytoarchitecture and intersubject variability. J Comp Neurol 412:319–341

    Article  PubMed  CAS  Google Scholar 

  • Anderson B, Southern BD, Powers RE (1999) Anatomic asymmetries of the posterior superior temporal lobes: a postmortem study. Neuropsychiatry Neuropsychol Behav Neurol 12:247–254

    PubMed  CAS  Google Scholar 

  • Annett M (1985) Left, right, hand and brain: the right shift theory. Lawrence Erlbaum Associates Ltd., Hove

    Google Scholar 

  • Bailey P, von Bonin G, McCulloch WS (1950) The isocortex of the chimpanzee. University of Illinois Press, Urbana

    Google Scholar 

  • Broad KD, Mimmack ML, Kendrick KM (2000) Is right hemisphere specialization for face discrimination specific to humans? Eur J Neurosci 12(2):731–741

    Article  PubMed  CAS  Google Scholar 

  • Buldyrev S, Cruz L, Gomez-Isla T, Gomez-Tortosa E, Havlin S, Le R, Stanley HE, Urbanc B, Hyman BT (2000) Description of microcolumnar ensembles in association cortex and their disruption in Alzheimer and Lewy body dementias. Proc Natl Acad Sci USA 97:5039–5043

    Article  PubMed  CAS  Google Scholar 

  • Buxhoeveden DP, Switala AE, Roy E, Casanova MF (2000) Quantitative analysis of cell columns in the cerebral cortex. J Neuroscie Methods 97:7–17

    Article  CAS  Google Scholar 

  • Buxhoeveden DP, Switala AE, Litaker M, Roy E, Casanova MF (2001) Lateralization of minicolumns in human planum temporale is absent in nonhuman primate cortex. Brain Behav Evol 57:349–358

    Article  PubMed  CAS  Google Scholar 

  • Cantalupo C, Hopkins WD (2001) Asymmetric Broca’s area in great apes. Nature 414:505

    Article  PubMed  CAS  Google Scholar 

  • Casanova MF, Switala AE. (2005) Minicolumnar morphometry: computerized image analysis in Neocortical modularity and the cell minicolumn. In: Casanova MF (ed), Nova Biomedical, New York, pp 161–180

  • Casanova MF, van Kooten IA, Switala AE, van Engeland H, Heinsen H, Steinbusch HW, Hof PR, Trippe J, Stone J, Schmitz C (2006) Minicolumnar abnormalities in autism. Acta Neuropathol 112(3):287–303

    Article  PubMed  Google Scholar 

  • Chance SA, Crow TJ (2007) Distinctively human: cerebral lateralisation and language in Homo sapiens. J Anthropol Sci 85:153–164

    Google Scholar 

  • Chance SA, Tzotzoli PM, Vitelli A, Esiri MM, Crow TJ (2004) The cytoarchitecture of sulcal folding in Heschl’s sulcus and the temporal cortex in the normal brain and schizophrenia: lamina thickness and cell density. Neurosci Lett 367:384–388

    Article  PubMed  CAS  Google Scholar 

  • Chance SA, Casanova MF, Switala AE, Crow TJ (2006) Minicolumnar structure in Heschl’s gyrus and planum temporale: Asymmetries in relation to sex and callosal fiber number. Neuroscience 143:1041–1050

    Article  PubMed  CAS  Google Scholar 

  • Chance SA, Casanova MF, Switala AE, Crow TJ (2008) Auditory cortex asymmetry, altered minicolumn spacing and absence of aging effects in schizophrenia. Brain. 131(12):3178–3192

    Article  PubMed  Google Scholar 

  • Chance SA, Clover L, Cousijn H, Currah L, Pettingill R, Esiri MM (2011) Micro-anatomical correlates of cognitive ability and decline: normal ageing, MCI and Alzheimers disease. Cereb Cortex 21(8):1870–1878

    Article  PubMed  Google Scholar 

  • Corballis MC (1992) The lopsided ape: evolution of the generative mind. Oxford University Press, New York

    Google Scholar 

  • Crow TJ (2000) Schizophrenia as the price that Homo sapiens pays for language: a resolution of the central paradox in the origin of species. Brain Res Rev 31:118–131

    Article  PubMed  CAS  Google Scholar 

  • Cruz L, Roe DL, Urbanc B, Inglis A, Stanley HE, Rosene DL (2009) Age-related reduction in microcolumnar structure correlates with cognitive decline in ventral but not dorsal area 46 of the rhesus monkey. Neuroscience 158(4):1509–1520

    Article  PubMed  CAS  Google Scholar 

  • Dehaene S, Pegado F, Braga LW, Ventura P, Filho GN, Jobert A, Dehaene-Lambertz G, Kolinsky R, Morais J, Cohen L (2010) How learning to read changes the cortical networks for vision and language. Science 330:1359–1364

    Article  PubMed  CAS  Google Scholar 

  • Di Rosa E, Crow TJ, Walker MA, Black G, Chance SA (2009) Reduced neuron density, enlarged minicolumn spacing and altered ageing effects in fusiform cortex in schizophrenia. Psychiatry Res 166(2–3):102–115

    Article  PubMed  Google Scholar 

  • Dorph-Petersen KA, Pierri JN, Wu Q, Sampson AR, Lewis DA (2007) Primary visual cortex volume and total neuron number are reduced in schizophrenia. J Comp Neurol 501(2):290–301

    Article  PubMed  Google Scholar 

  • Gabbott PL (2003) Radial organization of neurons and dendrites in human cortical areas 25, 32, and 32’. Brain Res 992(2):298–304

    Article  PubMed  CAS  Google Scholar 

  • Gannon PJ, Holloway RL, Broadfield DC, Braun AR (1998) Asymmetry of chimpanzee planum temporale: humanlike pattern of Wernicke’s brain language area homolog. Science 279(5348):220–222

    Article  PubMed  CAS  Google Scholar 

  • Gathers AD, Bhatt R, Corbly CR, Farley AB, Joseph JE (2004) Developmental shifts in cortical loci for face and object recognition. NeuroReport 15(10):1549–1553

    Article  PubMed  CAS  Google Scholar 

  • Geschwind N, Levitsky W (1968) Human brain: left–right asymmetries in temporal speech region. Science 161:186–187

    Article  PubMed  CAS  Google Scholar 

  • Goh JO, Suzuki A, Park DC (2010) Reduced neural selectivity increases fMRI adaptation with age during face discrimination. Neuroimage 51(1):336–344

    Article  PubMed  Google Scholar 

  • Greenblatt SH (1990) Alexia without agraphia, right homonymous hemianopsia, and color anomia. Report of four cases with location of the lesion by computerized axial tomography of the brain. Brain Lang 38(4):576–595

    Article  PubMed  CAS  Google Scholar 

  • Harasty J, Seldon HL, Chan P, Halliday G, Harding A (2003) The left human speech-processing cortex is thinner but longer than the right. Laterality 8(3):247–260

    Article  PubMed  CAS  Google Scholar 

  • Hof PR, Cox K, Morrison JH (1990) Quantitative analysis of a vulnerable subset of pyramidal neurons in Alzheimer’s disease: I. Superior frontal and inferior temporal cortex. J Comp Neurol 301:44–54

    Article  PubMed  CAS  Google Scholar 

  • Hof PR, Morrison JH (1995) Neurofilament protein defines regional patterns of cortical organization in the macaque monkey visual system: a quantitative immunohistochemical analysis. J Comp Neurol 352:161–186

    Google Scholar 

  • Holloway RL, De LaCoste-Lareymondie MC (1982) Brain endocast asymmetry in pongids and hominids: some preliminary findings on the paleontology of cerebral dominance. Am J Phys Anthropol 58:101–110

    Article  PubMed  CAS  Google Scholar 

  • Horton JC, Adams DL (2005) The cortical column: a structure without a function. Philos Trans R Soc Lond B Biol Sci 360:837–862

    Article  PubMed  Google Scholar 

  • Hutsler JJ (2003) The specialized structure of human language cortex: pyramidal cell size asymmetries within auditory and language-associated regions of the temporal lobes. Brain Lang 86(2):226–242

    Article  PubMed  Google Scholar 

  • Hutsler J, Galuske RA (2003) Hemispheric asymmetries in cerebral cortical networks. Trends Neurosci 26(8):429–435

    Article  PubMed  CAS  Google Scholar 

  • Jung-Beeman M (2005) Bilateral brain processes for comprehending natural language. Trends Cogn Sci 9:512–518

    Article  PubMed  Google Scholar 

  • Kanwisher N, McDermott J, Chun MM (1997) The fusiform face area: a module in human extrastriate cortex specialized for face perception. J Neurosci 17(11):4302–4311

    PubMed  CAS  Google Scholar 

  • Law AJ, Harrison PJ (2003) The distribution and morphology of prefrontal cortex pyramidal neurons identified using anti-neurofilament antibodies SMI32, N200 and FNP7. Normative data and a comparison in subjects with schizophrenia, bipolar disorder or major depression. J Psychiatr Res 37(6):487–499

    Article  PubMed  Google Scholar 

  • Matsuzawa T (2007) Comparative cognitive development. Dev Sci 10(1):97–103

    Article  PubMed  Google Scholar 

  • McManus IC (1985) Handedness, language dominance and aphasia: a genetic model. Psychological Medicine, Monograph Supplement No.8. Cambridge University Press, Cambridge

  • Mercure E, Dick F, Halit H, Kaufman J, Johnson MH (2008) Differential lateralization for words and faces: category or psychophysics? J Cogn Neurosci 20(11):2070–2087

    Article  PubMed  Google Scholar 

  • Moore CJ, Price CJ (1999) Three distinct ventral occipitotemporal regions for reading and object naming. NeuroImage 10(2):181–192

    Article  PubMed  CAS  Google Scholar 

  • Morrison JH, Lewis DA, Campbell MJ, Huntley GW, Benson DL, Bouras C (1987) A monoclonal antibody to non-phosphorylated neurofilament protein marks the vulnerable cortical neurons in Alzheimer’s disease. Brain Res 416:331–336

    Article  PubMed  CAS  Google Scholar 

  • Mountcastle VB (1997) The columnar organization of the neocortex. Brain 120(4):701–722

    Article  PubMed  Google Scholar 

  • Ono K, Nakamura A, Yoshiyama K, Kinkori T, Bundo M, Kato T, Ito K (2011) The effect of musical experience on hemispheric lateralization in musical feature processing. Neurosci Lett 496(2):141–145

    Article  PubMed  CAS  Google Scholar 

  • Parr LA, Hecht E, Barks SK, Preuss TM, Votaw JR (2009) Face processing in the chimpanzee brain. Curr Biol 19:50–53

    Article  PubMed  CAS  Google Scholar 

  • Peters A (2010) The morphology of minicolumns. In: Blatt GJ (ed) The neurochemical basis of autism: from molecules to minicolumns. Springer, New York, pp 45–68

    Chapter  Google Scholar 

  • Pierce K, Haist F, Sedaghat F, Courchesne E (2004) The brain response to personally familiar faces in autism: findings of fusiform activity and beyond. Brain 127(12):2703–2716

    Article  PubMed  Google Scholar 

  • Peirce JW, Kendrick KM (2002) Functional asymmetry in sheep temporal cortex. Neuroreport 13:2395–2399

    Google Scholar 

  • Pinsk MA, DeSimone K, Moore T, Gross CG, Kastner S (2005) Representations of faces and body parts in macaque temporal cortex: a functional MRI study. Proc Natl Acad Sci USA 102:6996–7001

    Article  PubMed  CAS  Google Scholar 

  • Quester R, Schroder R (1997) The shrinkage of the human brain stem during formalin fixation and embedding in paraffin. J Neurosci Methods 75:81–89

    Article  PubMed  CAS  Google Scholar 

  • Radenahmad N, Neal JW, Wilcock GW, Pearson RCA (2003) A neurofilament antibody recognises a subset of pyramidal cells in the human neocortex that are preserved in Alzheimer’s disease. Neuropathol Appl Neurobiol 29:316–320

    Article  PubMed  CAS  Google Scholar 

  • Rakic P (1995) A small step for the cell, a giant leap for mankind: a hypothesis of neocortical expansion during evolution. Trends Neurosci 18(9):383–388

    Article  PubMed  CAS  Google Scholar 

  • Rossion B, Dricot L, Devolder A, Bodart J-M, Crommelinck M, de Gelder B, Zoontjes R (2000) Hemispheric asymmetries for whole-based and part-based face processing in the human fusiform gyrus. J Cogn Neurosci 12(5):793–802

    Article  PubMed  CAS  Google Scholar 

  • Schenker NM, Hopkins WD, Spocter MA, Garrison AR, Stimpson CD, Erwin JM, Hof PR, Sherwood CC (2010) Broca’s area homologue in chimpanzees (Pan troglodytes): probabilistic mapping, asymmetry, and comparison to humans. Cereb Cortex 20(3):730–742

    Article  PubMed  Google Scholar 

  • Seldon HL (1981a) Structure of human auditory cortex: I. Cytoarchitectonics and dendritic distributions. Brain Res 229:277–294

    Article  PubMed  CAS  Google Scholar 

  • Seldon HL (1981b) Structure of human auditory cortex: II. Axon distributions and morphological correlates of speech perception. Brain Res 229:295–310

    Article  PubMed  CAS  Google Scholar 

  • Sherwood CC, Stimpson CD, Raghanti MA, Wildman DE, Uddin M, Grossman LI, Goodman M, Redmond JC, Bonar CJ, Erwin JM, Hof PR (2006) Evolution of increased glia-neuron ratios in the human frontal cortex. Proc Natl Acad Sci USA 103:13606–13611

    Article  PubMed  CAS  Google Scholar 

  • Sherwood CC, Wahl E, Erwin JM, Hof PR, Hopkins WD (2007) Histological asymmetries of primary motor cortex predict handedness in chimpanzees (Pan troglodytes). J Comp Neurol 503:525–537

    Article  PubMed  Google Scholar 

  • Skoglund TS, Pascher R, Berthold CH (2004) Aspects of the organization of neurons and dendritic bundles in primary somatosensory cortex of the rat. Neurosci Res 50:189–198

    Article  PubMed  CAS  Google Scholar 

  • Spocter MA, Hopkins WD, Garrison AR, Bauernfeind AL, Stimpson CD, Hof PR, Sherwood CC (2010) Wernicke’s area homologue in chimpanzees (Pan troglodytes) and its relation to the appearance of modern human language. Proc Biol Sci 277(1691):2165–2174

    Article  PubMed  Google Scholar 

  • Taubert J, Parr LA (2010) Geometric distortions affect face recognition in chimpanzees (Pan troglodytes) and monkeys (Macaca mulatta). Anim Cogn 14:35–43

    Article  PubMed  Google Scholar 

  • Teunisse JP, de Gelder B (2001) Impaired categorical perception of facial expressions in high-functioning adolescents with autism. Child neuropsychol 7(1):1–14

    Article  PubMed  CAS  Google Scholar 

  • Tsao DY, Moeller S, Freiwald WA (2008) Comparing face patch systems in macaques and humans. Proc Natl Acad Sci USA 105(49):19514–19519

    Article  PubMed  CAS  Google Scholar 

  • Van Kooten IA, Palmen SJ, von Cappeln P, Steinbusch HW, Korr H, Heinsen H, Hof PR, van Engeland H, Schmitz C (2008) Neurons in the fusiform gyrus are fewer and smaller in autism. Brain 131:987–999

    Article  PubMed  Google Scholar 

  • Von Economo C, Koskinas GN (1925) Die Cytoarchitektonik der Hirnrinde des Erwachsenen Menschen. Springer, Berlin (Germany) (Translated by Dr Lee Seldon)

  • Wilson HR, Diaconescu A (2006) Learning alters local face space geometry. Vision Res 46:4143–4151

    Article  PubMed  Google Scholar 

  • Young MP, Yamane S (1992) Sparse population coding of faces in the inferotemporal cortex. Science 256:1327–1331

    Article  PubMed  CAS  Google Scholar 

  • Zatorre RJ, Belin P (2001) Spectral and temporal processing in human auditory cortex. Cereb Cortex 11:946–953

    Article  PubMed  CAS  Google Scholar 

  • Zhu Q, Song Y, Hu S, Li X, Tian M, Zhen Z, Dong Q, Kanwisher N, Liu J (2010) Heritability of the specific cognitive ability of face perception. Curr Biol 20(2):137–142

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Dr. Chet Sherwood for his contribution to discussion of the project and Dr. Joseph Erwin who both helped P.R.H. with the original collection of chimpanzee brain materials at Mount Sinai School of Medicine. The work was supported by a grant from the European Union framework 6 programme: “What makes us human”. S.A.C. was the recipient of a fellowship from Alzheimer Scotland, UK, and a project grant from Autism Speaks, USA. Additional support was provided by the James S. McDonnell Foundation (grant 22002078) to P.R.H.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Steven A. Chance.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chance, S.A., Sawyer, E.K., Clover, L.M. et al. Hemispheric asymmetry in the fusiform gyrus distinguishes Homo sapiens from chimpanzees. Brain Struct Funct 218, 1391–1405 (2013). https://doi.org/10.1007/s00429-012-0464-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-012-0464-8

Keywords

Navigation