Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

On the relationship between maps and domains in inferotemporal cortex

Abstract

How does the brain encode information about the environment? Decades of research have led to the pervasive notion that the object-processing pathway in primate cortex consists of multiple areas that are each specialized to process different object categories (such as faces, bodies, hands, non-face objects and scenes). The anatomical consistency and modularity of these regions have been interpreted as evidence that these regions are innately specialized. Here, we propose that ventral-stream modules do not represent clusters of circuits that each evolved to process some specific object category particularly important for survival, but instead reflect the effects of experience on a domain-general architecture that evolved to be able to adapt, within a lifetime, to its particular environment. Furthermore, we propose that the mechanisms underlying the development of domains are both evolutionarily old and universal across cortex. Topographic maps are fundamental, governing the development of specializations across systems, providing a framework for brain organization.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: Development of face selectivity in macaque and human infants.
Fig. 2: Intrinsic and experience-dependent organization in macaque visual cortex.
Fig. 3: Topographic receptive-field tuning.
Fig. 4: Congruence between sensory maps.

References

  1. 1.

    Underleider, L. G. & Mishkin, M. in Analysis of Visual Behavior (eds Ingle, M. A., Goodale, M. I. & Masfield, R. J. W.) 549–586 (MIT Press, 1982).

  2. 2.

    Goodale, M. A. & Milner, A. D. Separate visual pathways for perception and action. Trends Neurosci. 15, 20–25 (1992).

    CAS  PubMed  Article  Google Scholar 

  3. 3.

    Farah, M. J. Visual Agnosia (MIT Press, 2004).

  4. 4.

    Konorski, J. Integrative activity of the brain; an interdisciplinary approach (University of Chicago Press, 1967).

  5. 5.

    Bell, A. H., Hadj-Bouziane, F., Frihauf, J. B., Tootell, R. B. & Ungerleider, L. G. Object representations in the temporal cortex of monkeys and humans as revealed by functional magnetic resonance imaging. J. Neurophysiol. 101, 688–700 (2009).

    PubMed  Article  Google Scholar 

  6. 6.

    Pinsk, M. A., Desimone, K., Moore, T., Gross, C. G. & Kastner, S. Representations of faces and body parts in macaque temporal cortex: a functional MRI study. Proc. Natl Acad. Sci. USA 102, 6996–7001 (2005).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  7. 7.

    Tsao, D. Y., Moeller, S. & Freiwald, W. A. Comparing face patch systems in macaques and humans. Proc. Natl Acad. Sci. USA 105, 19514–19519 (2008).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  8. 8.

    Parvizi, J. & Kastner, S. Promises and limitations of human intracranial electroencephalography. Nat. Neurosci. 21, 474–483 (2018).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  9. 9.

    Tsao, D. Y. & Livingstone, M. S. Mechanisms of face perception. Annu. Rev. Neurosci. 31, 411–437 (2008).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  10. 10.

    Kanwisher, N. Domain specificity in face perception. Nat. Neurosci. 3, 759–763 (2000).

    CAS  PubMed  Article  Google Scholar 

  11. 11.

    Weiner, K. S. & Zilles, K. The anatomical and functional specialization of the fusiform gyrus. Neuropsychologia 83, 48–62 (2016).

    PubMed  Article  Google Scholar 

  12. 12.

    Arcaro, M. J., Schade, P. F. & Livingstone, M. S. Universal mechanisms and the development of the face network: what you see is what you get. Annu. Rev. Vis. Sci. 5, 341–372 (2019).

    PubMed  PubMed Central  Article  Google Scholar 

  13. 13.

    Chomsky, N. Knowledge of Language: Its Nature, Origin, and Use (Praeger, 1986).

  14. 14.

    McKone, E., Crookes, K., Jeffery, L. & Dilks, D. D. A critical review of the development of face recognition: experience is less important than previously believed. Cogn. Neuropsychol. 29, 174–212 (2012).

    PubMed  Article  Google Scholar 

  15. 15.

    Dehaene, S. & Cohen, L. Cultural recycling of cortical maps. Neuron 56, 384–398 (2007).

    CAS  PubMed  Article  Google Scholar 

  16. 16.

    Desimone, R. & Gross, C. G. Visual areas in the temporal cortex of the macaque. Brain Res. 178, 363–380 (1979).

    CAS  PubMed  Article  Google Scholar 

  17. 17.

    Grill-Spector, K. & Malach, R. The human visual cortex. Annu. Rev. Neurosci. 27, 649–677 (2004).

    CAS  PubMed  Article  Google Scholar 

  18. 18.

    Arcaro, M. J., Schade, P. F., Vincent, J. L., Ponce, C. R. & Livingstone, M. S. Seeing faces is necessary for face-domain formation. Nat. Neurosci. 20, 1404–1412 (2017).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  19. 19.

    Deen, B. et al. Organization of high-level visual cortex in human infants. Nat. Commun. 8, 13995 (2017).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  20. 20.

    Brem, S. et al. Brain sensitivity to print emerges when children learn letter-speech sound correspondences. Proc. Natl Acad. Sci. USA 107, 7939–7944 (2010).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  21. 21.

    Ben-Shachar, M., Dougherty, R. F., Deutsch, G. K. & Wandell, B. A. The development of cortical sensitivity to visual word forms. J. Cogn. Neurosci. 23, 2387–2399 (2011).

    PubMed  PubMed Central  Article  Google Scholar 

  22. 22.

    Bouhali, F. et al. Anatomical connections of the visual word form area. J. Neurosci. 34, 15402–15414 (2014).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  23. 23.

    Mahon, B. Z. & Caramazza, A. What drives the organization of object knowledge in the brain? Trends Cogn. Sci. 15, 97–103 (2011).

    PubMed  PubMed Central  Article  Google Scholar 

  24. 24.

    Srihasam, K., Mandeville, J. B., Morocz, I. A., Sullivan, K. J. & Livingstone, M. S. Behavioral and anatomical consequences of early versus late symbol training in macaques. Neuron 73, 608–619 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  25. 25.

    Srihasam, K., Vincent, J. L. & Livingstone, M. S. Novel domain formation reveals proto-architecture in inferotemporal cortex. Nat. Neurosci. 17, 1776–1783 (2014).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  26. 26.

    Livingstone, M. S., Srihasam, K. & Morocz, I. A. The benefit of symbols: monkeys show linear, human-like, accuracy when using symbols to represent scalar value. Anim. Cogn. 13, 711–719 (2010).

    PubMed  PubMed Central  Article  Google Scholar 

  27. 27.

    Arcaro, M. J. & Livingstone, M. S. A hierarchical, retinotopic proto-organization of the primate visual system at birth. eLife 6, e26196 (2017).

    PubMed  PubMed Central  Article  Google Scholar 

  28. 28.

    Arcaro, M. J., Schade, P. F. & Livingstone, M. S. Body map proto-organization in newborn macaques. Proc. Natl Acad. Sci. USA 116, 24861–24871 (2019).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  29. 29.

    Arsenault, J. T., Janssens, T., Polimeni, J. R., Wald, L. L. & Vanduffel, W. Ultra high-resolution fMRI with an implanted 8-channel array coil reveals detailed retinotopic maps. Soc. Neurosci. Abstr. 573, 63261337 (2012).

    Google Scholar 

  30. 30.

    Kolster, H., Janssens, T., Orban, G. A. & Vanduffel, W. The retinotopic organization of macaque occipitotemporal cortex anterior to V4 and caudoventral to the middle temporal (MT) cluster. J. Neurosci. 34, 10168–10191 (2014).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  31. 31.

    Arcaro, M. J. & Livingstone, M. S. Retinotopic organization of scene areas in macaque inferior temporal cortex. J. Neurosci. 37, 7373–7389 (2017).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  32. 32.

    Kolster, H. et al. Visual field map clusters in macaque extrastriate visual cortex. J. Neurosci. 29, 7031–7039 (2009).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  33. 33.

    Tootell, R. B. & Hadjikhani, N. Where is ‘dorsal V4’ in human visual cortex? Retinotopic, topographic and functional evidence. Cereb. Cortex 11, 298–311 (2001).

    CAS  PubMed  Article  Google Scholar 

  34. 34.

    Norman-Haignere, S. V., Kanwisher, N., McDermott, J. H. & Conway, B. R. Divergence in the functional organization of human and macaque auditory cortex revealed by fMRI responses to harmonic tones. Nat. Neurosci. 22, 1057–1060 (2019).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  35. 35.

    Petkov, C. I., Kayser, C., Augath, M. & Logothetis, N. K. Functional imaging reveals numerous fields in the monkey auditory cortex. PLoS Biol. 4, e215 (2006).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  36. 36.

    Levy, I., Hasson, U., Avidan, G., Hendler, T. & Malach, R. Center-periphery organization of human object areas. Nat. Neurosci. 4, 533–539 (2001).

    CAS  PubMed  Article  Google Scholar 

  37. 37.

    Lafer-Sousa, R. & Conway, B. R. Parallel, multi-stage processing of colors, faces and shapes in macaque inferior temporal cortex. Nat. Neurosci. 16, 1870–1878 (2013).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  38. 38.

    Hasson, U., Levy, I., Behrmann, M., Hendler, T. & Malach, R. Eccentricity bias as an organizing principle for human high-order object areas. Neuron 34, 479–490 (2002).

    CAS  PubMed  Article  Google Scholar 

  39. 39.

    Konkle, T. & Oliva, A. A real-world size organization of object responses in occipitotemporal cortex. Neuron 74, 1114–1124 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  40. 40.

    Hasson, U., Harel, M., Levy, I. & Malach, R. Large-scale mirror-symmetry organization of human occipito-temporal object areas. Neuron 37, 1027–1041 (2003).

    CAS  PubMed  Article  Google Scholar 

  41. 41.

    Kamps, F. S., Hendrix, C. L., Brennan, P. A. & Dilks, D. D. Connectivity at the origins of domain specificity in the cortical face and place networks. Proc. Natl Acad. Sci. USA 117, 6163–6169 (2020).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  42. 42.

    Hubel, D. H. & Wiesel, T. N. Uniformity of monkey striate cortex: a parallel relationship between field size, scatter, and magnification factor. J. Comp. Neurol. 158, 295–305 (1974).

    CAS  PubMed  Article  Google Scholar 

  43. 43.

    Hubel, D. H. & Wiesel, T. N. Receptive fields and functional architecture in two nonstriate visual areas (18 and 19) of the cat. J. Neurophysiol. 28, 229–289 (1965).

    CAS  PubMed  Article  Google Scholar 

  44. 44.

    Hubel, D. H. & Wiesel, T. N. Receptive fields and functional architecture of monkey striate cortex. J. Physiol. 195, 215–243 (1968).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  45. 45.

    Hubel, D. H. & Livingstone, M. S. Segregation of form, color, and stereopsis in primate area 18. J. Neurosci. 7, 3378–3415 (1987).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  46. 46.

    Yue, X., Pourladian, I. S., Tootell, R. B. & Ungerleider, L. G. Curvature-processing network in macaque visual cortex. Proc. Natl Acad. Sci. USA 111, E3467–E3475 (2014).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  47. 47.

    Yue, X., Robert, S. & Ungerleider, L. G. Curvature processing in human visual cortical areas. Neuroimage 222, 117295 (2020).

    PubMed  Article  Google Scholar 

  48. 48.

    Bao, P., She, L., McGill, M. & Tsao, D. Y. A map of object space in primate inferotemporal cortex. Nature 583, 103–108 (2020).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  49. 49.

    Bell, A. H. et al. Relationship between functional magnetic resonance imaging-identified regions and neuronal category selectivity. J. Neurosci. 31, 12229–12240 (2011).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  50. 50.

    Aparicio, P. L., Issa, E. B. & DiCarlo, J. J. Neurophysiological organization of the middle face patch in macaque inferior temporal cortex. J. Neurosci. 36, 12729–12745 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  51. 51.

    Durbin, R. & Mitchison, G. A dimension reduction framework for understanding cortical maps. Nature 343, 644–647 (1990).

    CAS  PubMed  Article  Google Scholar 

  52. 52.

    Swindale, N. V., Shoham, D., Grinvald, A., Bonhoeffer, T. & Hubener, M. Visual cortex maps are optimized for uniform coverage. Nat. Neurosci. 3, 822–826 (2000).

    CAS  PubMed  Article  Google Scholar 

  53. 53.

    Hubel, D. H. & Wiesel, T. N. Sequence regularity and geometry of orientation columns in the monkey striate cortex. J. Comp. Neurol. 158, 267–293 (1974).

    CAS  PubMed  Article  Google Scholar 

  54. 54.

    Grimaldi, P., Saleem, K. S. & Tsao, D. Anatomical connections of the functionally defined “face patches” in the macaque monkey. Neuron 90, 1325–1342 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  55. 55.

    Lyon, D. C. & Connolly, J. D. The case for primate V3. Proc. Biol. Sci. 279, 625–633 (2012).

    PubMed  Google Scholar 

  56. 56.

    Livingstone, M. S. & Hubel, D. H. Anatomy and physiology of a color system in the primate visual cortex. J. Neurosci. 4, 309–356 (1984).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  57. 57.

    Malach, R., Levy, I. & Hasson, U. The topography of high-order human object areas. Trends Cogn. Sci. 6, 176–184 (2002).

    PubMed  Article  Google Scholar 

  58. 58.

    Konkle, T. & Caramazza, A. Tripartite organization of the ventral stream by animacy and object size. J. Neurosci. 33, 10235–10242 (2013).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  59. 59.

    Long, B., Yu, C.-P. & Konkle, T. Mid-level visual features underlie the high-level categorical organization of the ventral stream. Proc. Natl Acad. Sci. USA 115, E9015–E9024 (2018).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  60. 60.

    Coggan, D. D., Liu, W., Baker, D. H. & Andrews, T. J. Category-selective patterns of neural response in the ventral visual pathway in the absence of categorical information. Neuroimage 135, 107–114 (2016).

    PubMed  Article  Google Scholar 

  61. 61.

    Peelen, M. V. & Downing, P. E. Category selectivity in human visual cortex: Beyond visual object recognition. Neuropsychologia 105, 177–183 (2017).

    PubMed  Article  Google Scholar 

  62. 62.

    Bracci, S., Ritchie, J. B. & de Beeck, H. O. On the partnership between neural representations of object categories and visual features in the ventral visual pathway. Neuropsychologia 105, 153–164 (2017).

    PubMed  PubMed Central  Article  Google Scholar 

  63. 63.

    Kriegeskorte, N. et al. Matching categorical object representations in inferior temporal cortex of man and monkey. Neuron 60, 1126–1141 (2008).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  64. 64.

    Bracci, S. & Op de Beeck, H. Dissociations and associations between shape and category representations in the two visual pathways. J. Neurosci. 36, 432–444 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  65. 65.

    Carlson, T. A., Simmons, R. A., Kriegeskorte, N. & Slevc, L. R. The emergence of semantic meaning in the ventral temporal pathway. J. Cogn. Neurosci. 26, 120–131 (2014).

    PubMed  Article  Google Scholar 

  66. 66.

    Bryan, P. B., Julian, J. B. & Epstein, R. A. Rectilinear edge selectivity is insufficient to explain the category selectivity of the parahippocampal place area. Front. Hum. Neurosci. 10, 137 (2016).

    PubMed  PubMed Central  Article  Google Scholar 

  67. 67.

    Bi, H. et al. Neuronal responses in visual area V2 (V2) of macaque monkeys with strabismic amblyopia. Cereb. Cortex 21, 2033–2045 (2011).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  68. 68.

    Kiorpes, L., Walton, P. J., O’Keefe, L. P., Movshon, J. A. & Lisberger, S. G. Effects of early-onset artificial strabismus on pursuit eye movements and on neuronal responses in area MT of macaque monkeys. J. Neurosci. 16, 6537–6553 (1996).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  69. 69.

    Tsao, D. Y., Freiwald, W. A., Tootell, R. B. & Livingstone, M. S. A cortical region consisting entirely of face-selective cells. Science 311, 670–674 (2006).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  70. 70.

    Golarai, G. et al. Differential development of high-level visual cortex correlates with category-specific recognition memory. Nat. Neurosci. 10, 512–522 (2007).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  71. 71.

    Scherf, K. S., Behrmann, M., Humphreys, K. & Luna, B. Visual category-selectivity for faces, places and objects emerges along different developmental trajectories. Dev. Sci. 10, F15–F30 (2007).

    PubMed  Article  Google Scholar 

  72. 72.

    Hubel, D. H., Wiesel, T. N. & LeVay, S. Functional architecture of area 17 in normal and monocularly deprived macaque monkeys. Cold Spring Harb. Symp. Quant. Biol. 40, 581–589 (1976).

    CAS  PubMed  Article  Google Scholar 

  73. 73.

    Wiesel, T. N. & Hubel, D. H. Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens. J. Neurophysiol. 28, 1029–1040 (1965).

    CAS  PubMed  Article  Google Scholar 

  74. 74.

    Blakemore, C. & Cooper, G. F. Development of the brain depends on the visual environment. Nature 228, 477–478 (1970).

    CAS  PubMed  Article  Google Scholar 

  75. 75.

    Sengpiel, F., Stawinski, P. & Bonhoeffer, T. Influence of experience on orientation maps in cat visual cortex. Nat. Neurosci. 2, 727–732 (1999).

    CAS  PubMed  Article  Google Scholar 

  76. 76.

    Stryker, M. P. & Sherk, H. Modification of cortical orientation selectivity in the cat by restricted visual experience: a reexamination. Science 190, 904–906 (1975).

    CAS  PubMed  Article  Google Scholar 

  77. 77.

    Tanaka, S., Ribot, J., Imamura, K. & Tani, T. Orientation-restricted continuous visual exposure induces marked reorganization of orientation maps in early life. Neuroimage 30, 462–477 (2006).

    PubMed  Article  Google Scholar 

  78. 78.

    Aboitiz, F., Scheibel, A. B., Fisher, R. S. & Zaidel, E. Individual differences in brain asymmetries and fiber composition in the human corpus callosum. Brain Res. 598, 154–161 (1992).

    CAS  PubMed  Article  Google Scholar 

  79. 79.

    Zhang, L. I., Bao, S. & Merzenich, M. M. Persistent and specific influences of early acoustic environments on primary auditory cortex. Nat. Neurosci. 4, 1123–1130 (2001).

    CAS  Article  Google Scholar 

  80. 80.

    Van der Loos, H. & Woolsey, T. A. Somatosensory cortex: structural alterations following early injury to sense organs. Science 179, 395–398 (1973).

    PubMed  Article  Google Scholar 

  81. 81.

    Jayaraman, S., Fausey, C. M. & Smith, L. B. The faces in infant-perspective scenes change over the first year of life. PLoS ONE 10, e0123780 (2015).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  82. 82.

    Goren, C. C., Sarty, M. & Wu, P. Y. Visual following and pattern discrimination of face-like stimuli by newborn infants. Pediatrics 56, 544–549 (1975).

    CAS  PubMed  Google Scholar 

  83. 83.

    Johnson, M. H., Dziurawiec, S., Ellis, H. & Morton, J. Newborns’ preferential tracking of face-like stimuli and its subsequent decline. Cognition 40, 1–19 (1991).

    CAS  PubMed  Article  Google Scholar 

  84. 84.

    Kenney, M. D., Mason, W. A. & Hill, S. D. Effects of age, objects, and visual experience on affective responses of rhesus monkeys to strangers. Dev. Psychol. 15, 176–184 (1979).

    Article  Google Scholar 

  85. 85.

    Maurer, D. & Young, R. Newborns’ following of natural and distorted arrangements of facial features. Infant. Behav. Dev. 6, 127–131 (1983).

    Article  Google Scholar 

  86. 86.

    Valenza, E., Simion, F., Cassia, V. M. & Umilta, C. Face preference at birth. J. Exp. Psychol. Hum. Percept. Perform. 22, 892–903 (1996).

    CAS  PubMed  Article  Google Scholar 

  87. 87.

    Banks, M. S. & Salapatek, P. Contrast sensitivity function of the infant visual system. Vis. Res. 16, 867–869 (1976).

    CAS  PubMed  Article  Google Scholar 

  88. 88.

    Kleiner, K. Amplitude and phase spectra as indices of infants’ pattern preferences. Infant. Behav. Dev. 10, 49–59 (1987).

    Article  Google Scholar 

  89. 89.

    Simion, F., Valenza, E., Cassia, V. M., Turati, C. & Umilta, C. Newborns’ preference for up-down asymmetrical configurations. Dev. Sci. 5, 427–434 (2002).

    Article  Google Scholar 

  90. 90.

    Bushnell, I. W. R. Mother’s face recognition in newborn infants: learning and memory. Infant. Child. Dev. 10, 67–74 (2001).

    Article  Google Scholar 

  91. 91.

    Wurtz, R. H. & Albano, J. E. Visual-motor function of the primate superior colliculus. Annu. Rev. Neurosci. 3, 189–226 (1980).

    CAS  PubMed  Article  Google Scholar 

  92. 92.

    Hafed, Z. M. & Chen, C. Y. Sharper, stronger, faster upper visual field representation in primate superior colliculus. Curr. Biol. 26, 1647–1658 (2016).

    CAS  PubMed  Article  Google Scholar 

  93. 93.

    Wallace, M. T., McHaffie, J. G. & Stein, B. E. Visual response properties and visuotopic representation in the newborn monkey superior colliculus. J. Neurophysiol. 78, 2732–2741 (1997).

    CAS  PubMed  Article  Google Scholar 

  94. 94.

    Sugita, Y. Face perception in monkeys reared with no exposure to faces. Proc. Natl Acad. Sci. USA 105, 394–398 (2008).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  95. 95.

    Davies-Thompson, J. & Andrews, T. J. Intra- and interhemispheric connectivity between face-selective regions in the human brain. J. Neurophysiol. 108, 3087–3095 (2012).

    PubMed  PubMed Central  Article  Google Scholar 

  96. 96.

    Gschwind, M., Pourtois, G., Schwartz, S., Van De Ville, D. & Vuilleumier, P. White-matter connectivity between face-responsive regions in the human brain. Cereb. Cortex 22, 1564–1576 (2012).

    PubMed  Article  Google Scholar 

  97. 97.

    Moeller, S., Freiwald, W. A. & Tsao, D. Y. Patches with links: a unified system for processing faces in the macaque temporal lobe. Science 320, 1355–1359 (2008).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  98. 98.

    Saygin, Z. M. et al. Anatomical connectivity patterns predict face selectivity in the fusiform gyrus. Nat. Neurosci. 15, 321–327 (2011).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  99. 99.

    Saygin, Z. M. et al. Connectivity precedes function in the development of the visual word form area. Nat. Neurosci. 19, 1250–1255 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  100. 100.

    Arcaro, M., Mautz, T. & Livingstone, M. S. Anatomical correlates of face patches in macaque inferotemporal cortex. Proc. Natl Acad. Sci. USA 117, 32667–32678 (2020).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  101. 101.

    Brodmann, K. Localisation in the Cerebral Cortex (Imperial Press, 1909).

  102. 102.

    Janssens, T., Zhu, Q., Popivanov, I. D. & Vanduffel, W. Probabilistic and single-subject retinotopic maps reveal the topographic organization of face patches in the macaque cortex. J. Neurosci. 34, 10156–10167 (2014).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  103. 103.

    DeFelipe, J., Alonso-Nanclares, L. & Arellano, J. I. Microstructure of the neocortex: comparative aspects. J. Neurocytol. 31, 299–316 (2002).

    PubMed  Article  Google Scholar 

  104. 104.

    Miller, K. D. Canonical computations of cerebral cortex. Curr. Opin. Neurobiol. 37, 75–84 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  105. 105.

    Hebb, D. O. The Organization of Behavior; a Neuropsychological Theory (Wiley, 1949).

  106. 106.

    Constantine-Paton, M. & Law, M. I. Eye-specific termination bands in tecta of three-eyed frogs. Science 202, 639–641 (1978).

    CAS  PubMed  Article  Google Scholar 

  107. 107.

    Leibo, J. Z., Liao, Q., Anselmi, F. & Poggio, T. The invariance hypothesis implies domain-specific regions in visual cortex. PLoS Comput. Biol. 11, e1004390 (2015).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  108. 108.

    Nasr, S., Polimeni, J. R. & Tootell, R. B. Interdigitated color- and disparity-selective columns within human visual cortical areas V2 and V3. J. Neurosci. 36, 1841–1857 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  109. 109.

    Murty, N. A. et al. Visual experience is not necessary for the development of face-selectivity in the lateral fusiform gyrus. Proc. Natl Acad. Sci. USA 117, 23011–23020 (2020).

    Article  CAS  Google Scholar 

  110. 110.

    van den Hurk, J., Van Baelen, M. & Op de Beeck, H. P. Development of visual category selectivity in ventral visual cortex does not require visual experience. Proc. Natl Acad. Sci. USA 114, E4501–E4510 (2017).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  111. 111.

    Reich, L., Szwed, M., Cohen, L. & Amedi, A. A ventral visual stream reading center independent of visual experience. Curr. Biol. 21, 363–368 (2011).

    CAS  PubMed  Article  Google Scholar 

  112. 112.

    Striem-Amit, E., Cohen, L., Dehaene, S. & Amedi, A. Reading with sounds: sensory substitution selectively activates the visual word form area in the blind. Neuron 76, 640–652 (2012).

    CAS  PubMed  Article  Google Scholar 

  113. 113.

    Mahon, B. Z., Anzellotti, S., Schwarzbach, J., Zampini, M. & Caramazza, A. Category-specific organization in the human brain does not require visual experience. Neuron 63, 397–405 (2009).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  114. 114.

    Mahon, B. Z., Schwarzbach, J. & Caramazza, A. The representation of tools in left parietal cortex is independent of visual experience. Psychol. Sci. 21, 764–771 (2010).

    PubMed  Article  Google Scholar 

  115. 115.

    He, C. et al. Selectivity for large nonmanipulable objects in scene-selective visual cortex does not require visual experience. Neuroimage 79, 1–9 (2013).

    PubMed  Article  Google Scholar 

  116. 116.

    Bourne, J. A. & Rosa, M. G. Hierarchical development of the primate visual cortex, as revealed by neurofilament immunoreactivity: early maturation of the middle temporal area (MT). Cereb. Cortex 16, 405–414 (2006).

    PubMed  Article  Google Scholar 

  117. 117.

    Flechsig, P. E. Anatomie des Menschlichen Gehirn und Ruckenmarks, auf Myelogenetischer Grundlage (Thieme, 1920).

  118. 118.

    Guillery, R. W. Is postnatal neocortical maturation hierarchical? Trends Neurosci. 28, 512–517 (2005).

    CAS  PubMed  Article  Google Scholar 

  119. 119.

    Burkhalter, A. Development of forward and feedback connections between areas V1 and V2 of human visual cortex. Cereb. Cortex 3, 476–487 (1993).

    CAS  PubMed  Article  Google Scholar 

  120. 120.

    Dong, H., Wang, Q., Valkova, K., Gonchar, Y. & Burkhalter, A. Experience-dependent development of feedforward and feedback circuits between lower and higher areas of mouse visual cortex. Vis. Res. 44, 3389–3400 (2004).

    PubMed  Article  Google Scholar 

  121. 121.

    Markov, N. T. et al. A weighted and directed interareal connectivity matrix for macaque cerebral cortex. Cereb. Cortex 24, 17–36 (2014).

    CAS  PubMed  Article  Google Scholar 

  122. 122.

    Bavelier, D. & Neville, H. J. Cross-modal plasticity: where and how? Nat. Rev. Neurosci. 3, 443–452 (2002).

    CAS  PubMed  Article  Google Scholar 

  123. 123.

    Bedny, M., Pascual-Leone, A., Dodell-Feder, D., Fedorenko, E. & Saxe, R. Language processing in the occipital cortex of congenitally blind adults. Proc. Natl Acad. Sci. USA 108, 4429–4434 (2011).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  124. 124.

    Fuster, J. M., Bodner, M. & Kroger, J. K. Cross-modal and cross-temporal association in neurons of frontal cortex. Nature 405, 347–351 (2000).

    CAS  PubMed  Article  Google Scholar 

  125. 125.

    Flanagan, J. G. Neural map specification by gradients. Curr. Opin. Neurobiol. 16, 59–66 (2006).

    CAS  PubMed  Article  Google Scholar 

  126. 126.

    Duhamel, J. R., Colby, C. L. & Goldberg, M. E. Ventral intraparietal area of the macaque: congruent visual and somatic response properties. J. Neurophysiol. 79, 126–136 (1998).

    CAS  PubMed  Article  Google Scholar 

  127. 127.

    Andersen, R. A. Multimodal integration for the representation of space in the posterior parietal cortex. Philos. Trans. R. Soc. Lond. B Biol. Sci. 352, 1421–1428 (1997).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  128. 128.

    Mullette-Gillman, O. A., Cohen, Y. E. & Groh, J. M. Motor-related signals in the intraparietal cortex encode locations in a hybrid, rather than eye-centered reference frame. Cereb. Cortex 19, 1761–1775 (2009).

    PubMed  Article  Google Scholar 

  129. 129.

    Wallace, M. T. & Stein, B. E. Sensory and multisensory responses in the newborn monkey superior colliculus. J. Neurosci. 21, 8886–8894 (2001).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  130. 130.

    Triplett, J. W., Phan, A., Yamada, J. & Feldheim, D. A. Alignment of multimodal sensory input in the superior colliculus through a gradient-matching mechanism. J. Neurosci. 32, 5264–5271 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  131. 131.

    Kravitz, D. J., Saleem, K. S., Baker, C. I., Ungerleider, L. G. & Mishkin, M. The ventral visual pathway: an expanded neural framework for the processing of object quality. Trends Cogn. Sci. 17, 26–49 (2013).

    PubMed  Article  Google Scholar 

  132. 132.

    Butt, O. H., Benson, N. C., Datta, R. & Aguirre, G. K. The fine-scale functional correlation of striate cortex in sighted and blind people. J. Neurosci. 33, 16209–16219 (2013).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  133. 133.

    Striem-Amit, E. et al. Functional connectivity of visual cortex in the blind follows retinotopic organization principles. Brain 138, 1679–1695 (2015).

    PubMed  PubMed Central  Article  Google Scholar 

  134. 134.

    Ungerleider, L. G., Galkin, T. W., Desimone, R. & Gattass, R. Cortical connections of area V4 in the macaque. Cereb. Cortex 18, 477–499 (2008).

    PubMed  Article  Google Scholar 

  135. 135.

    Moerel, M., De Martino, F. & Formisano, E. Processing of natural sounds in human auditory cortex: tonotopy, spectral tuning, and relation to voice sensitivity. J. Neurosci. 32, 14205–14216 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  136. 136.

    O’Rawe, J. F. & Leung, H. C. Topographic mapping as a basic principle of functional organization for visual and prefrontal functional connectivity. eNeuro https://doi.org/10.1523/ENEURO.0532-19.2019 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  137. 137.

    Yeo, B. T. et al. The organization of the human cerebral cortex estimated by intrinsic functional connectivity. J. Neurophysiol. 106, 1125–1165 (2011).

    PubMed  Article  Google Scholar 

  138. 138.

    Haile, T. M., Bohon, K. S., Romero, M. C. & Conway, B. R. Visual stimulus-driven functional organization of macaque prefrontal cortex. Neuroimage 188, 427–444 (2019).

    PubMed  Article  Google Scholar 

  139. 139.

    Tamber-Rosenau, B. J., Dux, P. E., Tombu, M. N., Asplund, C. L. & Marois, R. Amodal processing in human prefrontal cortex. J. Neurosci. 33, 11573–11587 (2013).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  140. 140.

    Janata, P. et al. The cortical topography of tonal structures underlying Western music. Science 298, 2167–2170 (2002).

    CAS  PubMed  Article  Google Scholar 

  141. 141.

    Fausey, C. M., Jayaraman, S. & Smith, L. B. From faces to hands: changing visual input in the first two years. Cognition 152, 101–107 (2016).

    PubMed  PubMed Central  Article  Google Scholar 

  142. 142.

    Eagleman, D. M., Kagan, A. D., Nelson, S. S., Sagaram, D. & Sarma, A. K. A standardized test battery for the study of synesthesia. J. Neurosci. Methods 159, 139–145 (2007).

    PubMed  Article  Google Scholar 

  143. 143.

    Fox, M. W. A phylogenetic analysis of behavioral neuro-ontogeny in precocial and nonprecocial mammals. Can. J. Comp. Med. Vet. Sci. 28, 197–202 (1964).

    CAS  PubMed  PubMed Central  Google Scholar 

  144. 144.

    Jones, T. A., Leake, P. A., Snyder, R. L., Stakhovskaya, O. & Bonham, B. Spontaneous discharge patterns in cochlear spiral ganglion cells before the onset of hearing in cats. J. Neurophysiol. 98, 1898–1908 (2007).

    PubMed  Article  Google Scholar 

  145. 145.

    Khazipov, R. et al. Early motor activity drives spindle bursts in the developing somatosensory cortex. Nature 432, 758–761 (2004).

    CAS  PubMed  Article  Google Scholar 

  146. 146.

    Meister, M., Wong, R. O., Baylor, D. A. & Shatz, C. J. Synchronous bursts of action potentials in ganglion cells of the developing mammalian retina. Science 252, 939–943 (1991).

    CAS  PubMed  Article  Google Scholar 

  147. 147.

    Marr, D. Vision: a Computational Investigation into the Human Representation and Processing of Visual Information (Freeman, 1982).

  148. 148.

    Livingstone, M. S. et al. Development of the macaque face-patch system. Nat. Commun. 8, 14897 (2017).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  149. 149.

    Rosenke, M., van Hoof, R., van den Hurk, J., Grill-Spector, K. & Goebel, R. A probabilistic functional atlas of human occipito-temporal visual cortex. Cereb. Cortex 31, 603–619 (2020).

    PubMed Central  Article  PubMed  Google Scholar 

  150. 150.

    Benson, N. C. & Winawer, J. Individual differences in human retinotopic maps revealed by Bayesian analysis of retinotopic organization. Preprint at bioRxiv https://doi.org/10.1101/325597 (2018).

    Article  Google Scholar 

  151. 151.

    Hubel, D. H. & Wiesel, T. N. Ferrier lecture. Functional architecture of macaque monkey visual cortex. Proc. R. Soc. Lond. B Biol. Sci. 198, 1–59 (1977).

    CAS  PubMed  Article  Google Scholar 

  152. 152.

    Mountcastle, V. B. Perceptual Neuroscience: the Cerebral Cortex (Harvard University Press, 1998).

  153. 153.

    Hofman, M. A. On the evolution and geometry of the brain in mammals. Prog. Neurobiol. 32, 137–158 (1989).

    CAS  PubMed  Article  Google Scholar 

  154. 154.

    Metin, C. & Frost, D. O. Visual responses of neurons in somatosensory cortex of hamsters with experimentally induced retinal projections to somatosensory thalamus. Proc. Natl Acad. Sci. USA 86, 357–361 (1989).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  155. 155.

    Roe, A. W., Pallas, S. L., Hahm, J. O. & Sur, M. A map of visual space induced in primary auditory cortex. Science 250, 818–820 (1990).

    CAS  PubMed  Article  Google Scholar 

  156. 156.

    Sur, M., Pallas, S. L. & Roe, A. W. Cross-modal plasticity in cortical development: differentiation and specification of sensory neocortex. Trends Neurosci. 13, 227–233 (1990).

    CAS  PubMed  Article  Google Scholar 

  157. 157.

    Gao, W. J. & Pallas, S. L. Cross-modal reorganization of horizontal connectivity in auditory cortex without altering thalamocortical projections. J. Neurosci. 19, 7940–7950 (1999).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  158. 158.

    Pallas, S. L., Littman, T. & Moore, D. R. Cross-modal reorganization of callosal connectivity without altering thalamocortical projections. Proc. Natl Acad. Sci. USA 96, 8751–8756 (1999).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  159. 159.

    von Melchner, L., Pallas, S. L. & Sur, M. Visual behaviour mediated by retinal projections directed to the auditory pathway. Nature 404, 871–876 (2000).

    Article  CAS  Google Scholar 

  160. 160.

    O’Leary, D. D. & Stanfield, B. B. Selective elimination of axons extended by developing cortical neurons is dependent on regional locale: experiments utilizing fetal cortical transplants. J. Neurosci. 9, 2230–2246 (1989).

    PubMed  PubMed Central  Article  Google Scholar 

  161. 161.

    Schlaggar, B. L. & O’Leary, D. D. Potential of visual cortex to develop an array of functional units unique to somatosensory cortex. Science 252, 1556–1560 (1991).

    CAS  PubMed  Article  Google Scholar 

  162. 162.

    Chou, S. J. et al. Geniculocortical input drives genetic distinctions between primary and higher-order visual areas. Science 340, 1239–1242 (2013).

    CAS  PubMed  Article  Google Scholar 

Download references

Author information

Affiliations

Authors

Contributions

The authors contributed equally to all aspects of the article.

Corresponding author

Correspondence to Margaret S. Livingstone.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information

Nature Reviews Neuroscience thanks H.-C. Leung, H. Op de Beeck and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Arcaro, M.J., Livingstone, M.S. On the relationship between maps and domains in inferotemporal cortex. Nat Rev Neurosci 22, 573–583 (2021). https://doi.org/10.1038/s41583-021-00490-4

Download citation

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing