Abstract
Objects constitute the fundamental currency of our consciousness: they are the things that we perceive, remember and think about. One of the most important objects for a primate is a face. Research on the macaque face patch system in recent years has given us a remarkable window into the detailed processes underlying object recognition. Here, we review the macaque face patch system, including its anatomical organization, coding principles, role in behaviour and interactions with other brain regions. We highlight not only how it constitutes an archetypal object recognition system but also how it may provide a key to understanding mechanisms for higher cognitive function.
This is a preview of subscription content, access via your institution
Access options
Access Nature and 54 other Nature Portfolio journals
Get Nature+, our best-value online-access subscription
$29.99 / 30 days
cancel any time
Subscribe to this journal
Receive 12 print issues and online access
$189.00 per year
only $15.75 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Sherrington, C. S. Man on his nature. Nature 147, 127–129 (1940).
Tanaka, K. Inferotemporal cortex and object vision. Ann. Rev. Neurosci. 19, 109–139 (1996).
Todorov, A., Mandisodza, A. N., Goren, A. & Hall, C. C. Inferences of competence from faces predict election outcomes. Science 308, 1623–1626 (2005).
Medawar, P. B. Advice to a Young Scientist (Basic Books, 2008).
Bao, P., She, L., Mcgill, M. & Tsao, D. Y. A map of object space in primate inferotemporal cortex. Nature 583, 103–108 (2020). This paper clarifies the general organizational principle of the IT cortex, showing that the face patch network constitutes part of a map of object space within IT.
Gross, C. G. in History of Neuroscience in Autobiography (eds Albright, T. & Squire, L. R.) (Oxford University Press, 2006).
Konorski, J. Integrative Activity of the Brain (University of Chicago Press, 1967).
Bruce, C., Desimone, R. & Gross, C. G. Visual properties of neurons in a polysensory area in superior temporal sulcus of the macaque. J. Neurophysiol. 46, 369–384 (1981).
Desimone, R., Albright, T. D., Gross, C. G. & Bruce, C. Stimulus-selective properties of inferior temporal neurons in the macaque. J. Neurosci. 4, 2051–2062 (1984). This is one of the earliest attempts to systematically analyse the selectivity of IT cells, including face cells, reporting a concentrated cluster of face cells in the fundus of the STS, likely corresponding to face patch MF.
Gross, C. G., Rocha-Miranda, C. D. & Bender, D. B. Visual properties of neurons in inferotemporal cortex of the Macaque. J. Neurophysiol. 35, 96–111 (1972).
Marr, D. Vision: A Computational Investigation into the Human Representation and Processing of Visual Information (Henry Holt and Co. Inc., 1982).
Baylis, G., Rolls, E. T. & Leonard, C. Selectivity between faces in the responses of a population of neurons in the cortex in the superior temporal sulcus of the monkey. Brain Res. 342, 91–102 (1985).
Baylis, G. C., Rolls, E. T. & Leonard, C. Functional subdivisions of the temporal lobe neocortex. J. Neurosci. 7, 330–342 (1987).
Kanwisher, N., McDermott, J. & Chun, M. M. The fusiform face area: a module in human extrastriate cortex specialized for face perception. J. Neurosci. 17, 4302–4311 (1997). This landmark paper identified several regions in the human brain that respond selectively to faces, including one in the right fusiform gyrus and demonstrated this region is specialized for processing faces through a stringent set of tests.
Clark, V. et al. Functional magnetic resonance imaging of human visual cortex during face matching: a comparison with positron emission tomography. Neuroimage 4, 1–15 (1996).
Courtney, S. M., Ungerleider, L. G., Keil, K. & Haxby, J. V. Transient and sustained activity in a distributed neural system for human working memory. Nature 386, 608–611 (1997).
Haxby, J. V. et al. The effect of face inversion on activity in human neural systems for face and object perception. Neuron 22, 189–199 (1999).
Malach, R. et al. Object-related activity revealed by functional magnetic resonance imaging in human occipital cortex. Proc. Natl Acad. Sci. USA 92, 8135–8139 (1995).
Puce, A., Allison, T., Asgari, M., Gore, J. C. & McCarthy, G. Differential sensitivity of human visual cortex to faces, letterstrings, and textures: a functional magnetic resonance imaging study. J. Neurosci. 16, 5205–5215 (1996).
Puce, A., Allison, T., Gore, J. C. & McCarthy, G. Face-sensitive regions in human extrastriate cortex studied by functional MRI. J. Neurophysiol. 74, 1192–1199 (1995).
Sergent, J., Ohta, S. & Macdonald, B. Functional neuroanatomy of face and object processing: a positron emission tomography study. Brain 115, 15–36 (1992).
DiCarlo, J. J. & Cox, D. D. Untangling invariant object recognition. Trends Cogn. Sci. 11, 333–341 (2007).
Sapountzis, P., Schluppeck, D., Bowtell, R. & Peirce, J. W. A comparison of fMRI adaptation and multivariate pattern classification analysis in visual cortex. Neuroimage 49, 1632–1640 (2010).
Gauthier, I., Tarr, M. J., Anderson, A. W., Skudlarski, P. & Gore, J. C. Activation of the middle fusiform face area increases with expertise in recognizing novel objects. Nat. Neurosci. 2, 568–573 (1999).
de Beeck, H. P. O., Baker, C. I., DiCarlo, J. J. & Kanwisher, N. G. Discrimination training alters object representations in human extrastriate cortex. J. Neurosci. 26, 13025–13036 (2006).
Tsao, D. Y., Freiwald, W. A., Knutsen, T. A., Mandeville, J. B. & Tootell, R. B. Faces and objects in macaque cerebral cortex. Nat. Neurosci. 6, 989–995 (2003). This was the first paper to identify face patches in macaques with fMRI.
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).
Afraz, A., Boyden, E. S. & DiCarlo, J. J. Optogenetic and pharmacological suppression of spatial clusters of face neurons reveal their causal role in face gender discrimination. Proc. Natl Acad. Sci. USA 112, 6730–6735 (2015).
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).
Arcaro, M. J., Schade, P. F., Vincent, J. L., Ponce, C. R. & Livingstone, M. S. Seeing faces is necessary for face-domain formation. J. Neurosci. 20, 1404–1412 (2017). In this study, monkeys were deprived of face experience from birth and it was found that these monkeys did not develop face patches but retained a retinotopic organization and modules selective for other categories.
Issa, E. B. & DiCarlo, J. J. Precedence of the eye region in neural processing of faces. J. Neurosci. 32, 16666–16682 (2012).
Livingstone, M. S. et al. Development of the macaque face-patch system. Nat. Commun. 8, 14897 (2017).
McMahon, D. B., Jones, A. P., Bondar, I. V. & Leopold, D. A. Face-selective neurons maintain consistent visual responses across months. Proc. Natl Acad. Sci. USA 111, 8251–8256 (2014).
McMahon, D. B., Russ, B. E., Elnaiem, H. D., Kurnikova, A. I. & Leopold, D. A. Single-unit activity during natural vision: diversity, consistency, and spatial sensitivity among AF face patch neurons. J. Neurosci. 35, 5537–5548 (2015).
Pinsk, M. A. et al. Neural representations of faces and body parts in macaque and human cortex: a comparative FMRI study. J. Neurophysiol. 101, 2581–2600 (2009).
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).
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).
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). This paper was the first to target an fMRI-identified region of the IT cortex for single-unit recording and found that face patches contain an extremely high concentration of face-selective cells, opening the possibility to systematically dissect the organization and coding properties of these cells.
Freiwald, W. A. & Tsao, D. Y. Functional compartmentalization and viewpoint generalization within the macaque face-processing system. Science 330, 845–851 (2010). This paper found that face patches form a functional hierarchy, with a view-specific representation in face patch ML, a mirror-symmetric representation in face patch AL and a view-invariant representation in face patch AM.
Fisher, C. & Freiwald, W. A. Contrasting specializations for facial motion within the macaque face-processing system. Curr. Biol. 25, 261–266 (2015).
Landi, S. M. & Freiwald, W. A. Two areas for familiar face recognition in the primate brain. Science 357, 591–595 (2017).
Ku, S.-P., Tolias, A. S., Logothetis, N. K. & Goense, J. fMRI of the face-processing network in the ventral temporal lobe of awake and anesthetized macaques. Neuron 70, 352–362 (2011).
Tsao, D. Y., Schweers, N., Moeller, S. & Freiwald, W. A. Patches of face-selective cortex in the macaque frontal lobe. Nat. Neurosci. 11, 877–879 (2008).
Saleem, K. S., Tanaka, K. & Rockland, K. S. Specific and columnar projection from area TEO to TE in the macaque inferotemporal cortex. Cereb. Cortex 3, 454–464 (1993).
Borra, E., Ichinohe, N., Sato, T., Tanifuji, M. & Rockland, K. S. Cortical connections to area TE in monkey: hybrid modular and distributed organization. Cereb. Cortex 20, 257–270 (2010).
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). This paper combined electrical microstimulation with simultaneous fMRI and found that face patches are strongly and specifically connected to each other.
Premereur, E., Taubert, J., Janssen, P., Vogels, R. & Vanduffel, W. Effective connectivity reveals largely independent parallel networks of face and body patches. Curr. Biol. 26, 3269–3279 (2016).
Grimaldi, P., Saleem, K. S. & Tsao, D. Anatomical connections of the functionally defined “face patches” in the macaque monkey. Neuron 90, 1325–1342 (2016).
Felleman, D. J. & Van Essen, D. C. Distributed hierarchical processing in the primate cerebral cortex. Cereb. Cortex 1, 1–47 (1991).
Saleem, K. S., Miller, B. & Price, J. L. Subdivisions and connectional networks of the lateral prefrontal cortex in the macaque monkey. J. Comp. Neurol. 522, 1641–1690 (2014).
Sato, T. et al. Object representation in inferior temporal cortex is organized hierarchically in a mosaic-like structure. J. Neurosci. 33, 16642–16656 (2013).
Rajimehr, R., Bilenko, N. Y., Vanduffel, W. & Tootell, R. B. Retinotopy versus face selectivity in macaque visual cortex. J. Cogn. Neurosci. 26, 2691–2700 (2014).
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).
Dubois, J., de Berker, A. O. & Tsao, D. Y. Single-unit recordings in the macaque face patch system reveal limitations of fMRI MVPA. J. Neurosci. 35, 2791–2802 (2015).
Tang, S. et al. Complex pattern selectivity in macaque primary visual cortex revealed by large-scale two-photon imaging. Curr. Biol. 28, 38–48.e3 (2018).
Bruce, V. & Young, A. Understanding face recognition. Br. J. Psychol. 77, 305–327 (1986).
Young, M. P. & Yamane, S. Sparse population coding of faces in the inferotemporal cortex. Science 256, 1327–1331 (1992).
Freiwald, W. A., Tsao, D. Y. & Livingstone, M. S. A face feature space in the macaque temporal lobe. Nat. Neurosci. 12, 1187–1196 (2009). This paper measured responses of face cells to a large, parametric set of cartoon faces and found that they detect the presence of subsets of parts such as eyes and measure subsets of features such as inter-eye distance, showing a characteristic ramp-shaped tuning.
Leopold, D. A., Bondar, I. V. & Giese, M. A. Norm-based face encoding by single neurons in the monkey inferotemporal cortex. Nature 442, 572–575 (2006).
Tanaka, J. W. & Farah, M. J. Parts and wholes in face recognition. Q. J. Exp. Psychol. 46, 225–245 (1993).
Sinha, P. Recognizing complex patterns. Nat. Neurosci. 5, 1093–1097 (2002).
Sinha, P. in International Workshop on Biologically Motivated Computer Vision. 249–262 (Springer).
Viola, P. & Jones, M. Computer vision and pattern recognition, 2001. in Proceedings of the 2001 IEEE Computer Society Conference on. I-I (IEEE, 2001).
Ohayon, S., Freiwald, W. A. & Tsao, D. Y. What makes a cell face selective? The importance of contrast. Neuron 74, 567–581 (2012).
Leibo, J. Z., Liao, Q., Anselmi, F., Freiwald, W. A. & Poggio, T. View-tolerant face recognition and Hebbian learning imply mirror-symmetric neural tuning to head orientation. Curr. Biol. 27, 62–67 (2017).
Yildirim, I., Belledonne, M., Freiwald, W. & Tenenbaum, J. Efficient inverse graphics in biological face processing. Sci. Adv. 6, eaax5979 (2020).
Chang, L. & Tsao, D. Y. The code for facial identity in the primate brain. Cell 169, 1013–1028.e14 (2017). This paper revealed that face cells use a shape-based and appearance-based axis code to represent facial identity, and that this simple code could be used to reconstruct faces seen by monkeys with remarkable accuracy.
Cootes, T. F., Edwards, G. J. & Taylor, C. J. in European Conference on Computer Vision. 484-498 (Springer, 1998).
Phillips, P. J. et al. Face recognition accuracy of forensic examiners, superrecognizers, and face recognition algorithms. Proc. Natl Acad. Sci. USA 115, 6171–6176 (2018).
Krizhevsky, A., Sutskever, I. & Hinton, G. ImageNet classification with deep convolutional neural networks. Adv. Neur. Inf. Process. Syst. https://doi.org/10.1145/3065386 (2012).
Yamins, D. L. et al. Performance-optimized hierarchical models predict neural responses in higher visual cortex. Proc. Natl Acad. Sci. USA 111, 8619–8624 (2014). This paper showed that units in a deep neural network trained to classify objects are predictive of neural responses in IT cortex and formalized the hypothesis that neural representations are equivalent if they are related by a linear transform.
Lillicrap, T. P., Santoro, A., Marris, L., Akerman, C. J. & Hinton, G. Backpropagation and the brain. Nat. Rev. Neurosci. 21, 335–346 (2020).
Kietzmann, T., McClure, P. & Kriegeskorte, N. Deep neural networks in computational neuroscience. bioRxiv https://doi.org/10.1101/133504 (2018).
Chang, L., Egger, B., Vetter, T. & Tsao, D. Y. What computational model provides the best explanation of face representations in the primate brain? bioRxiv https://doi.org/10.1101/2020.06.07.111930 (2020).
Higgins, I. et al. Unsupervised deep learning identifies semantic disentanglement in single inferotemporal neurons. arxiv https://arxiv.org/abs/2006.14304 (2020).
Bashivan, P., Kar, K. & DiCarlo, J. J. Neural population control via deep image synthesis. Science https://doi.org/10.1126/science.aav9436 (2019).
Ponce, C. R. et al. Evolving images for visual neurons using a deep generative network reveals coding principles and neuronal preferences. Cell 177, 999–1009.e10 (2019). This paper used a generative deep network and a genetic algorithm to iteratively evolve optimal images for IT cells, including face cells.
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).
Barat, E., Wirth, S. & Duhamel, J.-R. Face cells in orbitofrontal cortex represent social categories. Proc. Natl Acad. Sci. USA 115, E11158–E11167 (2018).
Hadj-Bouziane, F., Bell, A. H., Knusten, T. A., Ungerleider, L. G. & Tootell, R. B. Perception of emotional expressions is independent of face selectivity in monkey inferior temporal cortex. Proc. Natl Acad. Sci. USA 105, 5591–5596 (2008).
Furl, N., Hadj-Bouziane, F., Liu, N., Averbeck, B. B. & Ungerleider, L. G. Dynamic and static facial expressions decoded from motion-sensitive areas in the macaque monkey. J. Neurosci. 32, 15952–15962 (2012).
Marciniak, K., Atabaki, A., Dicke, P. W. & Thier, P. Disparate substrates for head gaze following and face perception in the monkey superior temporal sulcus. eLife https://doi.org/10.7554/eLife.03222 (2014).
She, L. & Tsao, D.Y. Recordings from macaque face and body patches in the upper bank of the superior temporal sulcus reveal strong species selectivity (abstract 192.04) (Society for Neuroscience, 2017).
Roy, A., Shepherd, S. V. & Platt, M. L. Reversible inactivation of pSTS suppresses social gaze following in the macaque (Macaca mulatta). Soc. Cogn. Affect. Neurosci. 9, 209–217 (2014).
She, L. & Tsao, D.Y. Face coding in the macaque perirhinal face patch (abstract 307.12) (Society for Neuroscience, 2018).
Park, S. H. et al. Functional subpopulations of neurons in a macaque face patch revealed by single-unit fMRI mapping. Neuron 95, 971–981.e5 (2017).
Arcaro, M. J., Ponce, C. & Livingstone, M. The neurons that mistook a hat for a face. eLife https://doi.org/10.7554/eLife.53798 (2020). This paper challenged the notion that face cells respond only to face-like stimuli, reporting that they also respond to bodies if the body indicates a face should be located in the cell’s receptive field.
Inagaki, M. & Fujita, I. Reference frames for spatial frequency in face representation differ in the temporal visual cortex and amygdala. J. Neurosci. 31, 10371–10379 (2011).
Taubert, J., Goffaux, V., Van Belle, G., Vanduffel, W. & Vogels, R. The impact of orientation filtering on face-selective neurons in monkey inferior temporal cortex. Sci. Rep. 6, 21189 (2016).
Bao, P. & Tsao, D. Y. Representation of multiple objects in macaque category-selective areas. Nat. Commun. 9, 1774 (2018).
Sugita, Y. Face perception in monkeys reared with no exposure to faces. Proc. Natl Acad. Sci. USA 105, 394–398 (2008).
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).
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).
Valenza, E., Simion, F., Cassia, V. M. & Umiltà, C. Face preference at birth. J. Exp. Psychol. Hum. Percept. Perform. 22, 892 (1996).
Bahrick, H. P., Bahrick, P. O. & Wittlinger, R. P. Fifty years of memory for names and faces: a cross-sectional approach. J. Exp. Psychol. Gen. 104, 54 (1975).
Yin, R. K. Looking at upside-down faces. J. Exp. Psychol. 81, 141 (1969).
Rosenfeld, S. A. & Van Hoesen, G. W. Face recognition in the rhesus monkey. Neuropsychologia 17, 503–509 (1979).
Bruce, C. Face recognition by monkeys: absence of an inversion effect. Neuropsychologia 20, 515–521 (1982).
Overman, W. H. Jr. & Doty, R. W. Hemispheric specialization displayed by man but not macaques for analysis of faces. Neuropsychologia 20, 113–128 (1982).
Wright, A. A. & Roberts, W. A. Monkey and human face perception: inversion effects for human faces but not for monkey faces or scenes. J. Cogn. Neurosci. 8, 278–290 (1996).
Moeller, S., Crapse, T., Chang, L. & Tsao, D. Y. The effect of face patch microstimulation on perception of faces and objects. Nat. Neurosci. 20, 743–752 (2017).
Gothard, K. M., Brooks, K. N. & Peterson, M. A. Multiple perceptual strategies used by macaque monkeys for face recognition. Anim. Cogn. 12, 155–167 (2009).
Pascalis, O. & Bachevalier, J. Face recognition in primates: a cross-species study. Behav. Processes 43, 87–96 (1998).
Rossion, B. & Taubert, J. What can we learn about human individual face recognition from experimental studies in monkeys? Vision Res. 157, 142–158 (2019).
Parr, L. A., Heintz, M. & Pradhan, G. Rhesus monkeys (Macaca mulatta) lack expertise in face processing. J. Comp. Psychol. 122, 390–402 (2008).
Heywood, C. & Cowey, A. The role of the ‘face-cell’ area in the discrimination and recognition of faces by monkeys. Phil. Trans. R. Soc. Lond. B Biol. Sci. 335, 31–37 (1992).
Afraz, S.-R., Kiani, R. & Esteky, H. Microstimulation of inferotemporal cortex influences face categorization. Nature 442, 692–695 (2006). This study reported that microstimulation of face-selective sites in the inferotemporal cortex biases monkeys to judge an image as a face.
Parvizi, J. et al. Electrical stimulation of human fusiform face-selective regions distorts face perception. J. Neurosci. 32, 14915–14920 (2012). This study reported that, when the fusiform face area was stimulated, a human patient reported perceived distortions in the faces of people in the room.
Schalk, G. et al. Facephenes and rainbows: causal evidence for functional and anatomical specificity of face and color processing in the human brain. Proc. Natl Acad. Sci. USA 114, 12285–12290 (2017).
Taubert, J., Wardle, S. G., Flessert, M., Leopold, D. A. & Ungerleider, L. G. Face pareidolia in the rhesus monkey. Curr. Biol. 27, 2505–2509.e2 (2017).
Haxby, J. V. et al. Distributed and overlapping representations of faces and objects in ventral temporal cortex. Science 293, 2425–2430 (2001). This paper challenged the notion that face patches are specialized to process faces. It showed that different visual categories elicit widely distributed and overlapping responses across cortex and activity in face areas reliably distinguishes between different non-face categories.
Sadagopan, S., Zarco, W. & Freiwald, W. A. A causal relationship between face-patch activity and face-detection behavior. eLife 6, e18558 (2017).
Shadlen, M. N. & Kiani, R. in Research and Perspectives in Neurosciences Vol. 18 27–46 (Springer, 2011).
Shadlen, M. N. & Kiani, R. Decision making as a window on cognition. Neuron 80, 791–806 (2013).
Kar, K., Kubilius, J., Schmidt, K., Issa, E. B. & DiCarlo, J. J. Evidence that recurrent circuits are critical to the ventral stream’s execution of core object recognition behavior. Nat. Neurosci. 22, 974 (2019).
Tang, H. et al. Recurrent computations for visual pattern completion. Proc. Natl Acad. Sci. USA 115, 8835–8840 (2018).
Schwiedrzik, C. M. & Freiwald, W. A. High-level prediction signals in a low-level area of the macaque face-processing hierarchy. Neuron 96, 89–97.e4 (2017).
Friston, K. The free-energy principle: a rough guide to the brain? Trends Cogn. Sci. 13, 293–301 (2009).
Huang, Y. & Rao, R. P. Predictive coding. Wiley Interdiscip. Rev. Cogn. Sci. 2, 580–593 (2011).
Rao, R. P. & Ballard, D. H. Predictive coding in the visual cortex: a functional interpretation of some extra-classical receptive-field effects. Nat. Neurosci. 2, 79–87 (1999). This landmark paper proposed a general model of the visual system as a predictive coding engine, with feedback pathways predicting visual input based on past experience and feedforward pathways conveying prediction errors. The scheme provides one model for the purpose of feedback within the face patch system.
Fernández-Miranda, J. C., Rhoton, A. L. Jr. Kakizawa, Y., Choi, C. & Álvarez-Linera, J. The claustrum and its projection system in the human brain: a microsurgical and tractographic anatomical study. J. Neurosurg. 108, 764–774 (2008).
Pearson, R., Brodal, P., Gatter, K. & Powell, T. The organization of the connections between the cortex and the claustrum in the monkey. Brain Res. 234, 435–441 (1982).
Tanné-Gariépy, J., Boussaoud, D. & Rouiller, E. M. Projections of the claustrum to the primary motor, premotor, and prefrontal cortices in the macaque monkey. J. Comp. Neurol. 454, 140–157 (2002).
Edelstein, L. & Denaro, F. The claustrum: a historical review of its anatomy, physiology, cytochemistry and functional significance. Pathology 104, 675–702 (2004).
Ettlinger, G. & Wilson, W. Cross-modal performance: behavioural processes, phylogenetic considerations and neural mechanisms. Behav. Brain Res. 40, 169–192 (1990).
Sherk, H. in Sensory-Motor Areas and Aspects of Cortical Connectivity 467-499 (Springer, 1986).
Crick, F. C. & Koch, C. What is the function of the claustrum? Philos. Trans. R. Soc. B Biol. Sci. 360, 1271–1279 (2005).
Tong, F., Nakayama, K., Vaughan, J. T. & Kanwisher, N. Binocular rivalry and visual awareness in human extrastriate cortex. Neuron 21, 753–759 (1998).
Frässle, S., Sommer, J., Jansen, A., Naber, M. & Einhäuser, W. Binocular rivalry: frontal activity relates to introspection and action but not to perception. J. Neurosci. 34, 1738–1747 (2014).
Overgaard, M. & Fazekas, P. Can no-report paradigms extract true correlates of consciousness. Trends Cogn Sci 20, 241–242 (2016).
Tsuchiya, N., Wilke, M., Frässle, S. & Lamme, V. A. No-report paradigms: extracting the true neural correlates of consciousness. Trends Cogn. Sci. 19, 757–770 (2015).
Hesse, J. K. & Tsao, D. Y. Representation of conscious percept without report in the macaque face patch network. bioRxiv https://doi.org/10.1101/2020.04.22.047522 (2020).
Desimone, R., Wessinger, M., Thomas, L. & Schneider, W. Attentional control of visual perception: cortical and subcortical mechanisms. Cold Spring Harb. Symp. Quant. Biol. 55, 963–971 (1990).
Olshausen, B. A., Anderson, C. H. & Van Essen, D. C. A neurobiological model of visual attention and invariant pattern recognition based on dynamic routing of information. J. Neurosci. 13, 4700–4719 (1993).
Robinson, D. L. & Petersen, S. E. The pulvinar and visual salience. Trends Neurosci. 15, 127–132 (1992).
Saalmann, Y. B. & Kastner, S. Cognitive and perceptual functions of the visual thalamus. Neuron 71, 209–223 (2011).
Shipp, S. The brain circuitry of attention. Trends Cogn. Sci. 8, 223–230 (2004).
Petersen, S. E., Robinson, D. L. & Morris, J. D. Contributions of the pulvinar to visual spatial attention. Neuropsychologia 25, 97–105 (1987).
Wilke, M., Kagan, I. & Andersen, R. A. Effects of pulvinar inactivation on spatial decision-making between equal and asymmetric reward options. J. Cogn. Neurosci. 25, 1270–1283 (2013).
Wilke, M., Turchi, J., Smith, K., Mishkin, M. & Leopold, D. A. Pulvinar inactivation disrupts selection of movement plans. J. Neurosc. 30, 8650–8659 (2010).
Saalmann, Y. B., Pinsk, M. A., Wang, L., Li, X. & Kastner, S. The pulvinar regulates information transmission between cortical areas based on attention demands. Science 337, 753–756 (2012).
Arrington, C. M., Carr, T. H., Mayer, A. R. & Rao, S. M. Neural mechanisms of visual attention: object-based selection of a region in space. J. Cogn. Neurosci. 12, 106–117 (2000).
Cerf, M., Frady, E. P. & Koch, C. Faces and text attract gaze independent of the task: experimental data and computer model. J. Vision https://doi.org/10.1167/9.12.10 (2009).
Maunsell, J. H. & Treue, S. Feature-based attention in visual cortex. Trends Neurosci. 29, 317–322 (2006).
Calder, A. J. & Nummenmaa, L. Face cells: separate processing of expression and gaze in the amygdala. Curr. Biol. 17, R371–R372 (2007).
Fried, I., MacDonald, K. A. & Wilson, C. L. Single neuron activity in human hippocampus and amygdala during recognition of faces and objects. Neuron 18, 753–765 (1997).
Kuraoka, K. & Nakamura, K. Responses of single neurons in monkey amygdala to facial and vocal emotions. J. Neurophysiol. 97, 1379–1387 (2007).
Nakamura, K., Mikami, A. & Kubota, K. Activity of single neurons in the monkey amygdala during performance of a visual discrimination task. J. Neurophysiol. 67, 1447–1463 (1992).
Rutishauser, U. et al. Single-unit responses selective for whole faces in the human amygdala. Curr. Biol. 21, 1654–1660 (2011).
Sanghera, M., Rolls, E. & Roper-Hall, A. Visual responses of neurons in the dorsolateral amygdala of the alert monkey. Exp. Neurol. 63, 610–626 (1979).
Wang, S. et al. Neurons in the human amygdala selective for perceived emotion. Proc. Natl Acad. Sci. USA 111, E3110–E3119 (2014).
Adolphs, R., Tranel, D., Damasio, H. & Damasio, A. Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala. Nature 372, 669–672 (1994).
Minxha, J. et al. Fixations gate species-specific responses to free viewing of faces in the human and macaque amygdala. Cell Rep. 18, 878–891 (2017).
Sigala, R., Logothetis, N. K. & Rainer, G. Own-species bias in the representations of monkey and human face categories in the primate temporal lobe. J. Neurophysiol. 105, 2740–2752 (2011).
Mosher, C. P., Zimmerman, P. E. & Gothard, K. M. Neurons in the monkey amygdala detect eye contact during naturalistic social interactions. Curr. Biol. 24, 2459–2464 (2014).
Taubert, J. et al. Amygdala lesions eliminate viewing preferences for faces in rhesus monkeys. Proc. Natl Acad. Sci. USA 115, 8043–8048 (2018).
Fahy, F. L., Riches, I. P. & Brown, M. W. Neuronal activity related to visual recognition memory: long-term memory and the encoding of recency and familiarity information in the primate anterior and medial inferior temporal and rhinal cortex. Exp. Brain Res. 96, 457–472 (1993).
Kornblith, S. & Tsao, D. Y. How thoughts arise from sights: inferotemporal and prefrontal contributions to vision. Curr. Opin. Neurobiol. 46, 208–218 (2017).
O’Craven, K. M. & Kanwisher, N. Mental imagery of faces and places activates corresponding stimulus-specific brain regions. J. Cogn. Neurosci. 12, 1013–1023 (2000).
Wallis, J. D. Orbitofrontal cortex and its contribution to decision-making. Annu. Rev. Neurosci. 30, 31–56 (2007).
Romanski, L. M. & Diehl, M. M. Neurons responsive to face-view in the primate ventrolateral prefrontal cortex. Neuroscience 189, 223–235 (2011).
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). This paper showed that colour-selective regions are adjacent to face patches and further reported multiple coarse eccentricity maps in IT.
Chang, L., Bao, P. & Tsao, D. Y. The representation of colored objects in macaque color patches. Nat. Commun. 8, 2064 (2017).
Kornblith, S., Cheng, X., Ohayon, S. & Tsao, D. Y. A network for scene processing in the macaque temporal lobe. Neuron 79, 766–781 (2013).
Kumar, S., Popivanov, I. D. & Vogels, R. Transformation of visual representations across ventral stream body-selective patches. Cereb. Cortex 29, 215–229 (2019). This study showed that neural responses to bodies in body-selective patches become more view-invariant as one moves more anterior in the cortical hierarchy.
Popivanov, I. D., Jastorff, J., Vanduffel, W. & Vogels, R. Stimulus representations in body-selective regions of the macaque cortex assessed with event-related fMRI. Neuroimage 63, 723–741 (2012).
Young, A. W., Hellawell, D. & Hay, D. C. Configurational information in face perception. Perception 42, 1166–1178 (2013).
Valentine, T. Upside-down faces: a review of the effect of inversion upon face recognition. Br. J. Psychol. 79, 471–491 (1988).
Parr, L., Winslow, J. & Hopkins, W. Is the inversion effect in rhesus monkeys face-specific? Anim. Cogn. 2, 123–129 (1999).
Taubert, J., Van Belle, G., Vanduffel, W., Rossion, B. & Vogels, R. The effect of face inversion for neurons inside and outside fMRI-defined face-selective cortical regions. J. Neurophysiol. 113, 1644–1655 (2014).
Thompson, P. Margaret Thatcher: a new illusion. Perception 9, 483–484 (1980).
Adachi, I., Chou, D. P. & Hampton, R. R. Thatcher effect in monkeys demonstrates conservation of face perception across primates. Curr. Biol. 19, 1270–1273 (2009).
Taubert, J., Van Belle, G., Vanduffel, W., Rossion, B. & Vogels, R. Neural correlate of the thatcher face illusion in a monkey face-selective patch. J. Neurosci. 35, 9872–9878 (2015).
Sugase-Miyamoto, Y., Matsumoto, N., Ohyama, K. & Kawano, K. Face inversion decreased information about facial identity and expression in face-responsive neurons in macaque area TE. J. Neurosci. 34, 12457–12469 (2014).
Tan, C. & Poggio, T. Neural tuning size in a model of primate visual processing accounts for three key markers of holistic face processing. PloS ONE 11, e0150980 (2016).
Riesenhuber, M. & Poggio, T. Hierarchical models of object recognition in cortex. Nat. Neurosci. 2, 1019 (1999).
Leibo, J. Z., Mutch, J. & Poggio, T. Why the brain separates face recognition from object recognition. Adv. Neural. Inf. Process. Syst. https://doi.org/10.5555/2986459.2986539 (2011).
Hung, C.-C. et al. Functional mapping of face-selective regions in the extrastriate visual cortex of the marmoset. J. Neurosci. 35, 1160–1172 (2015). This paper demonstrated that marmosets also have at least six face-selective patches.
Cuaya, L. V., Hernández-Pérez, R. & Concha, L. Our faces in the dog’s brain: Functional imaging reveals temporal cortex activation during perception of human faces. PLoS ONE 11, e0149431 (2016).
Khuvis, S. et al. Face-selective units in human ventral temporal cortex reactivate during free recall. bioRxiv https://doi.org/10.1101/487686 (2018).
Kendrick, K. & Baldwin, B. Cells in temporal cortex of conscious sheep can respond preferentially to the sight of faces. Science 236, 448–450 (1987).
Coulon, M., Deputte, B. L., Heyman, Y. & Baudoin, C. Individual recognition in domestic cattle (Bos taurus): evidence from 2D-images of heads from different breeds. PLoS ONE 4, e4441 (2009).
Stephan, C., Wilkinson, A. & Huber, L. Have we met before? Pigeons recognise familiar human faces. Avian Biol. Res. 5, 75–80 (2012).
Newport, C., Wallis, G., Reshitnyk, Y. & Siebeck, U. E. Discrimination of human faces by archerfish (Toxotes chatareus). Sci. Rep. 6, 27523 (2016).
Tibbetts, E. A. Visual signals of individual identity in the wasp Polistes fuscatus. Proc. Biol. Sci. 269, 1423–1428 (2002).
Van der Velden, J., Zheng, Y., Patullo, B. W. & Macmillan, D. L. Crayfish recognize the faces of fight opponents. PLoS ONE 3, e1695 (2008).
Rajimehr, R., Young, J. C. & Tootell, R. B. An anterior temporal face patch in human cortex, predicted by macaque maps. Proc. Natl Acad. Sci. USA 106, 1995–2000 (2009).
Grill-Spector, K., Knouf, N. & Kanwisher, N. The fusiform face area subserves face perception, not generic within-category identification. Nat. Neurosci. 7, 555–562 (2004).
Fox, C. J., Moon, S. Y., Iaria, G. & Barton, J. J. The correlates of subjective perception of identity and expression in the face network: an fMRI adaptation study. Neuroimage 44, 569–580 (2009).
Anzellotti, S., Fairhall, S. L. & Caramazza, A. Decoding representations of face identity that are tolerant to rotation. Cereb. Cortex 24, 1988–1995 (2014).
Axelrod, V. & Yovel, G. Successful decoding of famous faces in the fusiform face area. PLoS ONE 10, e0117126 (2015).
Yovel, G. & Freiwald, W. A. Face recognition systems in monkey and human: are they the same thing? F1000prime Rep. 5, 10 (2013).
Pitcher, D., Dilks, D. D., Saxe, R. R., Triantafyllou, C. & Kanwisher, N. Differential selectivity for dynamic versus static information in face-selective cortical regions. Neuroimage 56, 2356–2363 (2011).
Haxby, J. V., Hoffman, E. A. & Gobbini, M. I. The distributed human neural system for face perception. Trends Cogn. Sci. 4, 223–233 (2000).
Rotshtein, P., Henson, R. N., Treves, A., Driver, J. & Dolan, R. J. Morphing Marilyn into Maggie dissociates physical and identity face representations in the brain. Nat. Neurosci. 8, 107–113 (2005).
Polosecki, P. et al. Faces in motion: selectivity of macaque and human face processing areas for dynamic stimuli. J. Neurosci. 33, 11768–11773 (2013).
Dehaene, S. et al. How learning to read changes the cortical networks for vision and language. Science 330, 1359–1364 (2010). This paper demonstrated an important role for experience in driving the formation of category-selective regions in ventral temporal cortex. Illiterate adults develop selective activation for words in the left fusiform gyrus after they learn to read and this induces a competition with faces in this region.
Deen, B. et al. Organization of high-level visual cortex in human infants. Nat. Commun. 8, 13995 (2017).
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).
Arcaro, M. J. & Livingstone, M. S. A hierarchical, retinotopic proto-organization of the primate visual system at birth. eLife 6, e26196 (2017).
Srihasam, K., Vincent, J. L. & Livingstone, M. S. Novel domain formation reveals proto-architecture in inferotemporal cortex. Nat. Neurosci. 17, 1776–1783 (2014).
Hasson, U., Harel, M., Levy, I. & Malach, R. Large-scale mirror-symmetry organization of human occipito-temporal object areas. Neuron 37, 1027–1041 (2003).
Levy, I., Hasson, U., Avidan, G., Hendler, T. & Malach, R. Center–periphery organization of human object areas. Nat. Neurosci. 4, 533 (2001).
Erickson, C. A., Jagadeesh, B. & Desimone, R. Clustering of perirhinal neurons with similar properties following visual experience in adult monkeys. Nat. Neurosci. 3, 1143–1148 (2000).
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).
Op de Beeck, H. P., Pillet, I. & Ritchie, J. B. Factors determining where category-selective areas emerge in visual cortex. Trends Cogn. Sci. 23, 784–797 (2019). This review discusses experience-related factors that determine the location of category-selective areas such as face patches.
Ratan 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).
Acknowledgements
This work was supported by NIH (R01-EY030650), the Howard Hughes Medical Institute and the Tianqiao and Chrissy Chen Institute for Neuroscience at Caltech. We thank M. Livingstone and A. Varshavsky and members of the Tsao lab for helpful comments.
Author information
Authors and Affiliations
Contributions
The authors contributed equally to all aspects of the article.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Glossary
- Face patch
-
A cortical region in the macaque brain that responds selectively to viewed faces. Besides the six canonical face patches in each hemisphere that are found in the inferotemporal cortex, face patches have been reported outside of this cortical region such as in the upper bank of the superior temporal sulcus, the perirhinal cortex and the prefrontal cortex.
- Prosopagnosia
-
A cognitive disorder in which the ability to recognize faces is impaired while other forms of visual processing remain intact. Prosopagnosia, also called face blindness, may be present from birth or acquired as a result of brain damage.
- Grandmother cells
-
Hypothetical cells that respond selectively to only one concept (such as one’s grandmother) and thus implement an extreme case of sparse coding.
- Inferotemporal cortex
-
A cortical region in the inferior convexity of the temporal lobe of the macaque brain thought to be homologous to the human ventral temporal cortex. The inferotemporal cortex is part of the ventral visual stream and important for object recognition.
- Fusiform face area
-
(FFA). A cortical region in the human lateral fusiform gyrus that responds selectively to viewed faces. The FFA has been suggested to be homologous to the macaque middle face patches.
- Multi-voxel pattern analysis
-
An analysis method for fMRI data that tries to infer what a population of voxels encodes by decoding the stimuli or conditions on different trials from the population response vector.
- Holistic processing
-
A mode of processing in which the brain obligatorily recognizes a face as whole, postulated to occur due to several psychophysical phenomena, including the inversion effect, the whole-part effect and the composite effect; in each case, the same set of parts is not identified appropriately unless arranged to form an upright face.
- Ramp-shaped tuning
-
A coding scheme in which the response of a neuron increases monotonically as a feature is changed in one direction.
- Binocular rivalry
-
The phenomenon that, if two incompatible inputs are presented to the left and right eyes, respectively, rather than seeing a superimposition of the two, one’s perception stochastically alternates between the two images.
Rights and permissions
About this article
Cite this article
Hesse, J.K., Tsao, D.Y. The macaque face patch system: a turtle’s underbelly for the brain. Nat Rev Neurosci 21, 695–716 (2020). https://doi.org/10.1038/s41583-020-00393-w
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/s41583-020-00393-w
This article is cited by
-
Abstract representations emerge naturally in neural networks trained to perform multiple tasks
Nature Communications (2023)
-
A tripartite view of the posterior cingulate cortex
Nature Reviews Neuroscience (2023)
-
Functionally analogous body- and animacy-responsive areas are present in the dog (Canis familiaris) and human occipito-temporal lobe
Communications Biology (2023)
-
Socially meaningful visual context either enhances or inhibits vocalisation processing in the macaque brain
Nature Communications (2022)
-
Bidirectional and parallel relationships in macaque face circuit revealed by fMRI and causal pharmacological inactivation
Nature Communications (2022)
