Log in

One object, two networks? Assessing the relationship between the face and body-selective regions in the primate visual system

  • Review
  • Published:
Brain Structure and Function Aims and scope Submit manuscript

Abstract

Faces and bodies are often treated as distinct categories that are processed separately by face- and body-selective brain regions in the primate visual system. These regions occupy distinct regions of visual cortex and are often thought to constitute independent functional networks. Yet faces and bodies are part of the same object and their presence inevitably covary in naturalistic settings. Here, we re-evaluate both the evidence supporting the independent processing of faces and bodies and the organizational principles that have been invoked to explain this distinction. We outline four hypotheses ranging from completely separate networks to a single network supporting the perception of whole people or animals. The current evidence, especially in humans, is compatible with all of these hypotheses, making it presently unclear how the representation of faces and bodies is organized in the cortex.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Canada)

Instant access to the full article PDF.

Fig. 1

© Arne Olav Gurvin Fredriksen. B Accidental visual fusions of faces and bodies

Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

Not applicable.

References

  • Afraz SR, Kiani R, Esteky H (2006) Microstimulation of inferotemporal cortex influences face categorization. Nature 442(7103):692–695

    Article  CAS  PubMed  Google Scholar 

  • Afraz A, Boyden ES, DiCarlo JJ (2015) Optogenetic and pharmacological suppression of spatial clusters of face neurons reveal their causal role in face gender discrimination. Proc Natl Acad Sci 112(21):6730–6735

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Almeida J, Freixo A, Tábuas-Pereira M, Herald SB, Valério D, Schu G, Duro D, Cunha G, Bukhari Q, Duchaine B, Santana I (2020) Face-specific perceptual distortions reveal a view-and orientation-independent face template. Curr Biol 30(20):4071–4077

    Article  CAS  PubMed  Google Scholar 

  • Aparicio PL, Issa EB, DiCarlo JJ (2016) Neurophysiological organization of the middle face patch in macaque inferior temporal cortex. J Neurosci 36(50):12729–12745

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arcaro MJ, Schade PF, Vincent JL, Ponce CR, Livingstone MS (2017) Seeing faces is necessary for face-domain formation. Nat Neurosci 20(10):1404–1412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arcaro MJ, Ponce C, Livingstone M (2020) The neurons that mistook a hat for a face. Elife 9:e53798

    Article  PubMed  PubMed Central  Google Scholar 

  • Baeck A, Wagemans J, de Beeck HPO (2013) The distributed representation of random and meaningful object pairs in human occipitotemporal cortex: the weighted average as a general rule. Neuroimage 70:37–47

    Article  PubMed  Google Scholar 

  • Bao P, She L, McGill M, Tsao DY (2020) A map of object space in primate inferotemporal cortex. Nature 583(7814):103–108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barton JJ (2003) Disorders of face perception and recognition. Neurol Clin 21(2):521–548

    Article  PubMed  Google Scholar 

  • Bates E, Wilson SM, Saygin AP, Dick F, Sereno MI, Knight RT, Dronkers NF (2003) Voxel-based lesion–symptom map**. Nat Neurosci 6(5):448–450

    Article  CAS  PubMed  Google Scholar 

  • Beauchamp MS, Lee KE, Haxby JV, Martin A (2003) FMRI responses to video and point-light displays of moving humans and manipulable objects. J Cogn Neurosci 15(7):991–1001

    Article  PubMed  Google Scholar 

  • Bell AH, Malecek NJ, Morin EL, Hadj-Bouziane F, Tootell RB, Ungerleider LG (2011) Relationship between functional magnetic resonance imaging-identified regions and neuronal category selectivity. J Neurosci 31(34):12229–12240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bernstein M, Oron J, Sadeh B, Yovel G (2014) An integrated face–body representation in the fusiform gyrus but not the lateral occipital cortex. J Cogn Neurosci 26(11):2469–2478

    Article  PubMed  Google Scholar 

  • Biotti F, Gray KL, Cook R (2017) Impaired body perception in developmental prosopagnosia. Cortex 93:41–49

    Article  PubMed  Google Scholar 

  • Blom JD, Ter Meulen BC, Dool J (2021) A century of prosopometamorphopsia studies. Cortex 139:298–308

    Article  PubMed  Google Scholar 

  • Bornstein MH, Mash C, Arterberry ME (2011) Young infants’ eye movements over “natural” scenes and “experimental” scenes. Infant Behav Dev 34(1):206–210

    Article  PubMed  Google Scholar 

  • Bracci S, Caramazza A, Peelen MV (2015) Representational similarity of body parts in human occipitotemporal cortex. J Neurosci 35(38):12977–12985

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bracci S, Ritchie JB, de Beeck HO (2017) On the partnership between neural representations of object categories and visual features in the ventral visual pathway. Neuropsychologia 105:153–164

    Article  PubMed  PubMed Central  Google Scholar 

  • Buiatti M, Di Giorgio E, Piazza M, Polloni C, Menna G, Taddei F, Baldo E, Vallortigara G (2019) Cortical route for facelike pattern processing in human newborns. Proc Natl Acad Sci 116(10):4625–4630

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chan AW, Downing PE (2011) Faces and eyes in human lateral prefrontal cortex. Front Hum Neurosci 5:51

    Article  PubMed  PubMed Central  Google Scholar 

  • Collins JA, Olson IR (2014) Beyond the FFA: the role of the ventral anterior temporal lobes in face processing. Neuropsychologia 61:65–79

    Article  PubMed  Google Scholar 

  • Conway BR (2018) The organization and operation of inferior temporal cortex. Ann Rev Vis Sci 4:381–402

    Article  Google Scholar 

  • Cox D, Meyers E, Sinha P (2004) Contextually evoked object-specific responses in human visual cortex. Science 304(5667):115–117

    Article  CAS  PubMed  Google Scholar 

  • De Haas B, Schwarzkopf DS, Alvarez I, Lawson RP, Henriksson L, Kriegeskorte N, Rees G (2016) Perception and processing of faces in the human brain is tuned to typical feature locations. J Neurosci 36(36):9289–9302

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Deen B, Richardson H, Dilks DD, Takahashi A, Keil B, Wald LL, Kanwisher N, Saxe R (2017) Organization of high-level visual cortex in human infants. Nat Commun 8(1):1–10

    Article  CAS  Google Scholar 

  • Desimone R, Albright TD, Gross CG, Bruce C (1984) Stimulus-selective properties of inferior temporal neurons in the macaque. J Neurosci 4(8):2051–2062

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dorr M, Martinetz T, Gegenfurtner KR, Barth E (2010) Variability of eye movements when viewing dynamic natural scenes. J vis 10(10):28–28

    Article  PubMed  Google Scholar 

  • Downing PE, Peelen MV (2016) Body selectivity in occipitotemporal cortex: Causal evidence. Neuropsychologia 83:138–148

    Article  PubMed  Google Scholar 

  • Downing PE, Jiang Y, Shuman M, Kanwisher N (2001) A cortical area selective for visual processing of the human body. Science 293(5539):2470–2473

    Article  CAS  PubMed  Google Scholar 

  • Duchaine B, Yovel G (2015) A revised neural framework for face processing. Ann Rev Vis Sci 1:393–416

    Article  Google Scholar 

  • Epstein RA, Baker CI (2019) Scene perception in the human brain. Ann Rev Vis Sci 5:373–397

    Article  Google Scholar 

  • Fairhall SL, Ishai A (2007) Effective connectivity within the distributed cortical network for face perception. Cereb Cortex 17(10):2400–2406

    Article  PubMed  Google Scholar 

  • Farroni T, Chiarelli AM, Lloyd-Fox S, Massaccesi S, Merla A, Di Gangi V, Mattarello T, Faraguna D, Johnson MH (2013) Infant cortex responds to other humans from shortly after birth. Sci Rep 3(1):1–5

    Article  Google Scholar 

  • Felleman DJ, Van Essen DC (1991) Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex 1(1):1–47

    Article  CAS  PubMed  Google Scholar 

  • Feusner JD, Townsend J, Bystritsky A, Bookheimer S (2007) Visual information processing of faces in body dysmorphic disorder. Arch Gen Psychiatry 64(12):1417–1425

    Article  PubMed  Google Scholar 

  • Fisher C, Freiwald WA (2015a) Contrasting specializations for facial motion within the macaque face-processing system. Curr Biol 25(2):261–266

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fisher C, Freiwald WA (2015b) Whole-agent selectivity within the macaque face-processing system. Proc Natl Acad Sci 112(47):14717–14722

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Foster C, Zhao M, Bolkart T, Black MJ, Bartels A, Buelthoff I (2021) Separated and overlap** neural coding of face and body identity. Hum Brain Mapp 42(13):4242–4260

    Article  PubMed  PubMed Central  Google Scholar 

  • Freiwald WA, Tsao DY (2010) Functional compartmentalization and viewpoint generalization within the macaque face-processing system. Science 330(6005):845–851

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Freiwald WA, Tsao DY, Livingstone MS (2009) A face feature space in the macaque temporal lobe. Nat Neurosci 12(9):1187–1196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Freiwald W, Duchaine B, Yovel G (2016) Face processing systems: from neurons to real-world social perception. Annu Rev Neurosci 39:325–346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujita I, Fujita T (1996) Intrinsic connections in the macaque inferior temporal cortex. J Comp Neurol 368(4):467–486

    Article  CAS  PubMed  Google Scholar 

  • Fujita I, Tanaka K, Ito M, Cheng K (1992) Columns for visual features of objects in monkey inferotemporal cortex. Nature 360(6402):343–346

    Article  CAS  PubMed  Google Scholar 

  • Gauthier I, Skudlarski P, Gore JC, Anderson AW (2000) Expertise for cars and birds recruits brain areas involved in face recognition. Nat Neurosci 3(2):191–197

    Article  CAS  PubMed  Google Scholar 

  • Gerlach C, Starrfelt R (2021) Patterns of perceptual performance in developmental prosopagnosia: an in-depth case series. Cogn Neuropsychol 38(1):27–49

    Article  PubMed  Google Scholar 

  • Ghuman AS, McDaniel JR, Martin A (2010) Face adaptation without a face. Curr Biol 20(1):32–36

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Golomb JD, Kanwisher N (2012) Higher level visual cortex represents retinotopic, not spatiotopic, object location. Cereb Cortex 22(12):2794–2810

    Article  PubMed  Google Scholar 

  • Gomez J, Barnett M, Grill-Spector K (2019) Extensive childhood experience with Pokémon suggests eccentricity drives organization of visual cortex. Nat Hum Behav 3(6):611–624

    Article  PubMed  PubMed Central  Google Scholar 

  • Goren CC, Sarty M, Wu PY (1975) Visual following and pattern discrimination of face-like stimuli by newborn infants. Pediatrics 56(4):544–549

    Article  CAS  PubMed  Google Scholar 

  • Grill-Spector K, Weiner KS (2014) The functional architecture of the ventral temporal cortex and its role in categorization. Nat Rev Neurosci 15(8):536–548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grimaldi P, Saleem KS, Tsao D (2016) Anatomical connections of the functionally defined “face patches” in the macaque monkey. Neuron 90(6):1325–1342

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gross CG, Rocha-Miranda CD, Bender DB (1972) Visual properties of neurons in inferotemporal cortex of the macaque. J Neurophysiol 35(1):96–111

    Article  CAS  PubMed  Google Scholar 

  • Grossman ED, Blake R (2002) Brain areas active during visual perception of biological motion. Neuron 35(6):1167–1175

    Article  CAS  PubMed  Google Scholar 

  • Guntupalli JS, Wheeler KG, Gobbini MI (2017) Disentangling the representation of identity from head view along the human face processing pathway. Cereb Cortex 27(1):46–53

    Article  PubMed  Google Scholar 

  • Hadj-Bouziane F, Liu N, Bell AH, Gothard KM, Luh WM, Tootell RB, Murray EA, Ungerleider LG (2012) Amygdala lesions disrupt modulation of functional MRI activity evoked by facial expression in the monkey inferior temporal cortex. Proc Natl Acad Sci 109(52):E3640–E3648

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Handwerker DA, Ianni G, Gutierrez B, Roopchansingh V, Gonzalez-Castillo J, Chen G, Bandettini PA, Ungerleider LG, Pitcher D (2020) Theta-burst TMS to the posterior superior temporal sulcus decreases resting-state fMRI connectivity across the face processing network. Netw Neurosci 4(3):746–760

    Article  PubMed  PubMed Central  Google Scholar 

  • Harry BB, Umla-Runge K, Lawrence AD, Graham KS, Downing PE (2016) Evidence for integrated visual face and body representations in the anterior temporal lobes. J Cogn Neurosci 28(8):1178–1193

    Article  PubMed  Google Scholar 

  • Haxby JV, Hoffman EA, Gobbini MI (2000) The distributed human neural system for face perception. Trends Cogn Sci 4(6):223–233

    Article  CAS  PubMed  Google Scholar 

  • Haxby JV, Hoffman EA, Gobbini MI (2002) Human neural systems for face recognition and social communication. Biol Psychiat 51(1):59–67

    Article  PubMed  Google Scholar 

  • Haxby JV, Gobbini MI, Nastase SA (2020) Naturalistic stimuli reveal a dominant role for agentic action in visual representation. Neuroimage 216:116561

    Article  PubMed  Google Scholar 

  • Henriksson L, Mur M, Kriegeskorte N (2015) Faciotopy—a face-feature map with face-like topology in the human occipital face area. Cortex 72:156–167

    Article  PubMed  PubMed Central  Google Scholar 

  • Hoffman EA, Haxby JV (2000) Distinct representations of eye gaze and identity in the distributed human neural system for face perception. Nat Neurosci 3(1):80–84

    Article  CAS  PubMed  Google Scholar 

  • Hu Y, Baragchizadeh A, O’Toole AJ (2020) Integrating faces and bodies: Psychological and neural perspectives on whole person perception. Neurosci Biobehav Rev 112:472–486

    Article  PubMed  Google Scholar 

  • Hung CC, Yen CC, Ciuchta JL, Papoti D, Bock NA, Leopold DA, Silva AC (2015) Functional map** of face-selective regions in the extrastriate visual cortex of the marmoset. J Neurosci 35(3):1160–1172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hutchison RM, Culham JC, Everling S, Flanagan JR, Gallivan JP (2014) Distinct and distributed functional connectivity patterns across cortex reflect the domain-specific constraints of object, face, scene, body, and tool category-selective modules in the ventral visual pathway. Neuroimage 96:216–236

    Article  PubMed  Google Scholar 

  • Issa EB, Papanastassiou AM, DiCarlo JJ (2013) Large-scale, high-resolution neurophysiological maps underlying FMRI of macaque temporal lobe. J Neurosci 33(38):15207–15219

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jack RE, Schyns PG (2015) The human face as a dynamic tool for social communication. Curr Biol 25(14):R621–R634

    Article  CAS  PubMed  Google Scholar 

  • Jonas J, Descoins M, Koessler L, Colnat-Coulbois S, Sauvée M, Guye M, Vignal JP, Vespignani H, Rossion B, Maillard L (2012) Focal electrical intracerebral stimulation of a face-sensitive area causes transient prosopagnosia. Neuroscience 222:281–288

    Article  CAS  PubMed  Google Scholar 

  • Kaas JH (1997) Topographic maps are fundamental to sensory processing. Brain Res Bull 44(2):107–112

    Article  CAS  PubMed  Google Scholar 

  • Kaiser D, Strnad L, Seidl KN, Kastner S, Peelen MV (2014) Whole person-evoked fMRI activity patterns in human fusiform gyrus are accurately modeled by a linear combination of face-and body-evoked activity patterns. J Neurophysiol 111(1):82–90

    Article  PubMed  Google Scholar 

  • Kamps FS, Morris EJ, Dilks DD (2019) A face is more than just the eyes, nose, and mouth: fMRI evidence that face-selective cortex represents external features. Neuroimage 184:90–100

    Article  PubMed  Google Scholar 

  • Kamps FS, Hendrix CL, Brennan PA, Dilks DD (2020) Connectivity at the origins of domain specificity in the cortical face and place networks. Proc Natl Acad Sci 117(11):6163–6169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kanwisher N (2000) Domain specificity in face perception. Nat Neurosci 3(8):759–763

    Article  CAS  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kay KN, Weiner KS, Grill-Spector K (2015) Attention reduces spatial uncertainty in human ventral temporal cortex. Curr Biol 25(5):595–600

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kiani R, Esteky H, Mirpour K, Tanaka K (2007) Object category structure in response patterns of neuronal population in monkey inferior temporal cortex. J Neurophysiol 97(6):4296–4309

    Article  PubMed  Google Scholar 

  • Kliger L, Yovel G (2020) The functional organization of high-level visual cortex determines the representation of complex visual stimuli. J Neurosci 40(39):7545–7558

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klink PC, Aubry JF, Ferrera VP, Fox AS, Froudist-Walsh S, Jarraya B, Konofagou EE, Krauzlis RJ, Messinger A, Mitchell AS, Ortiz-Rios M (2021) Combining brain perturbation and neuroimaging in non-human primates. NeuroImage 235:118017

    Article  PubMed  Google Scholar 

  • Konkle T, Oliva A (2012) A real-world size organization of object responses in occipitotemporal cortex. Neuron 74(6):1114–1124

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kosakowski H, Cohen M, Takahashi A, Keil B, Kanwisher N, Saxe R (2021) Selective responses to faces, scenes, and bodies in the ventral visual pathway of infants. PsyArxiv. https://psyarxiv.com/7hqcu/.

  • Kriegeskorte N, Mur M, Ruff DA, Kiani R, Bodurka J, Esteky H, Tanaka K, Bandettini PA (2008) Matching categorical object representations in inferior temporal cortex of man and monkey. Neuron 60(6):1126–1141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar S, Popivanov ID, Vogels R (2019) Transformation of visual representations across ventral stream body-selective patches. Cereb Cortex 29(1):215–229

    Article  PubMed  Google Scholar 

  • Lafer-Sousa R, Conway BR (2013) Parallel, multi-stage processing of colors, faces and shapes in macaque inferior temporal cortex. Nat Neurosci 16(12):1870–1878

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Le Grand R, Mondloch CJ, Maurer D, Brent HP (2001) Early visual experience and face processing. Nature 410(6831):890–890

    Article  PubMed  Google Scholar 

  • Leopold DA, Park SH (2020) Studying the visual brain in its natural rhythm. NeuroImage 216:116790

    Article  PubMed  Google Scholar 

  • Levy I, Hasson U, Avidan G, Hendler T, Malach R (2001) Center–periphery organization of human object areas. Nat Neurosci 4(5):533–539

    Article  CAS  PubMed  Google Scholar 

  • Lisboa IC, Miguel H, Sampaio A, Mouta S, Santos JA, Pereira AF (2020) Right STS responses to biological motion in infancy—an fNIRS study using point-light walkers. Neuropsychologia 149:107668

    Article  PubMed  Google Scholar 

  • Livingstone MS, Vincent JL, Arcaro MJ, Srihasam K, Schade PF, Savage T (2017) Development of the macaque face-patch system. Nat Commun 8(1):1–12

    Article  CAS  Google Scholar 

  • Malaspina M, Albonico A, Daini R (2019) Self-face and self-body advantages in congenital prosopagnosia: evidence for a common mechanism. Exp Brain Res 237(3):673–686

    Article  PubMed  Google Scholar 

  • McCarthy G, Puce A, Gore JC, Allison T (1997) Face-specific processing in the human fusiform gyrus. J Cogn Neurosci 9(5):605–610

    Article  CAS  PubMed  Google Scholar 

  • McKone E, Kanwisher N, Duchaine BC (2007) Can generic expertise explain special processing for faces? Trends Cogn Sci 11(1):8–15

    Article  PubMed  Google Scholar 

  • Minnebusch DA, Daum I (2009) Neuropsychological mechanisms of visual face and body perception. Neurosci Biobehav Rev 33(7):1133–1144

    Article  PubMed  Google Scholar 

  • Moeller F, Siebner HR, Wolff S, Muhle H, Boor R, Granert O, Jansen O, Stephani U, Siniatchkin M (2008) Changes in activity of striato–thalamo–cortical network precede generalized spike wave discharges. Neuroimage 39(4):1839–1849

    Article  PubMed  Google Scholar 

  • Moro V, Urgesi C, Pernigo S, Lanteri P, Pazzaglia M, Aglioti SM (2008) The neural basis of body form and body action agnosia. Neuron 60(2):235–246

    Article  CAS  PubMed  Google Scholar 

  • Moro V, Pernigo S, Avesani R, Bulgarelli C, Urgesi C, Candidi M, Aglioti SM (2012) Visual body recognition in a prosopagnosic patient. Neuropsychologia 50(1):104–117

    Article  CAS  PubMed  Google Scholar 

  • Morris JP, Pelphrey KA, McCarthy G (2006) Occipitotemporal activation evoked by the perception of human bodies is modulated by the presence or absence of the face. Neuropsychologia 44(10):1919–1927

    Article  PubMed  PubMed Central  Google Scholar 

  • Mur M, Meys M, Bodurka J, Goebel R, Bandettini PA, Kriegeskorte N (2013) Human object-similarity judgments reflect and transcend the primate-IT object representation. Front Psychol 4:128

    Article  PubMed  PubMed Central  Google Scholar 

  • Murty NAR, Teng S, Beeler D, Mynick A, Oliva A, Kanwisher N (2020) Visual experience is not necessary for the development of face-selectivity in the lateral fusiform gyrus. Proc Natl Acad Sci 117(37):23011–23020

    Article  CAS  Google Scholar 

  • O’Neil EB, Hutchison RM, McLean DA, Köhler S (2014) Resting-state fMRI reveals functional connectivity between face-selective perirhinal cortex and the fusiform face area related to face inversion. Neuroimage 92:349–355

    Article  PubMed  Google Scholar 

  • Op de Beeck HP, Haushofer J, Kanwisher NG (2008) Interpreting fMRI data: maps, modules and dimensions. Nat Rev Neurosci 9(2):123–135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Op de Beeck HP, Pillet I, Ritchie JB (2019) Factors determining where category-selective areas emerge in visual cortex. Trends Cogn Sci 23(9):784–797

    Article  PubMed  Google Scholar 

  • Orlov T, Makin TR, Zohary E (2010) Topographic representation of the human body in the occipitotemporal cortex. Neuron 68(3):586–600

    Article  CAS  PubMed  Google Scholar 

  • Osher DE, Saxe RR, Koldewyn K, Gabrieli JD, Kanwisher N, Saygin ZM (2016) Structural connectivity fingerprints predict cortical selectivity for multiple visual categories across cortex. Cereb Cortex 26(4):1668–1683

    Article  PubMed  Google Scholar 

  • O’Toole AJ, Roark DA, Abdi H (2002) Recognizing moving faces: A psychological and neural synthesis. Trends Cogn Sci 6(6):261–266

    Article  PubMed  Google Scholar 

  • Parr LA, Hecht E, Barks SK, Preuss TM, Votaw JR (2009) Face processing in the chimpanzee brain. Curr Biol 19(1):50–53

    Article  CAS  PubMed  Google Scholar 

  • Parvizi J, Jacques C, Foster BL, Withoft N, Rangarajan V, Weiner KS, Grill-Spector K (2012) Electrical stimulation of human fusiform face-selective regions distorts face perception. J Neurosci 32(43):14915–14920

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peelen MV, Downing PE (2005) Selectivity for the human body in the fusiform gyrus. J Neurophysiol 93(1):603–608

    Article  PubMed  Google Scholar 

  • Peelen MV, Downing PE (2007) The neural basis of visual body perception. Nat Rev Neurosci 8(8):636–648

    Article  CAS  PubMed  Google Scholar 

  • Peelen MV, Glaser B, Vuilleumier P, Eliez S (2009) Differential development of selectivity for faces and bodies in the fusiform gyrus. Dev Sci 12(6):F16–F25

    Article  PubMed  Google Scholar 

  • Perrett DI, Rolls ET, Caan W (1982) Visual neurones responsive to faces in the monkey temporal cortex. Exp Brain Res 47(3):329–342

    Article  CAS  PubMed  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 102(19):6996–7001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pinsk MA, Arcaro M, Weiner KS, Kalkus JF, Inati SJ, Gross CG, Kastner S (2009) Neural representations of faces and body parts in macaque and human cortex: a comparative FMRI study. J Neurophysiol 101(5):2581–2600

    Article  PubMed  PubMed Central  Google Scholar 

  • Pitcher D, Ungerleider LG (2021) Evidence for a third visual pathway specialized for social perception. Trends Cogn Sci 25(2):100–110

    Article  PubMed  Google Scholar 

  • Pitcher D, Charles L, Devlin JT, Walsh V, Duchaine B (2009) Triple dissociation of faces, bodies, and objects in extrastriate cortex. Curr Biol 19(4):319–324

    Article  CAS  PubMed  Google Scholar 

  • Pitcher D, Dilks DD, Saxe RR, Triantafyllou C, Kanwisher N (2011) Differential selectivity for dynamic versus static information in face-selective cortical regions. Neuroimage 56(4):2356–2363

    Article  PubMed  Google Scholar 

  • Pitcher D, Japee S, Rauth L, Ungerleider LG (2017) The superior temporal sulcus is causally connected to the amygdala: a combined TBS-fMRI study. J Neurosci 37(5):1156–1161

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pitcher D, Ianni G, Ungerleider LG (2019) A functional dissociation of face-, body-and scene-selective brain areas based on their response to moving and static stimuli. Sci Rep 9(1):1–9

    Article  CAS  Google Scholar 

  • Popivanov ID, Jastorff J, Vanduffel W, Vogels R (2012) Stimulus representations in body-selective regions of the macaque cortex assessed with event-related fMRI. Neuroimage 63(2):723–741

    Article  PubMed  Google Scholar 

  • Popivanov ID, Jastorff J, Vanduffel W, Vogels R (2014) Heterogeneous single-unit selectivity in an fMRI-defined body-selective patch. J Neurosci 34(1):95–111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Popivanov ID, Schyns PG, Vogels R (2016) Stimulus features coded by single neurons of a macaque body category selective patch. Proc Natl Acad Sci 113(17):E2450–E2459

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Premereur E, Taubert J, Janssen P, Vogels R, Vanduffel W (2016) Effective connectivity reveals largely independent parallel networks of face and body patches. Curr Biol 26(24):3269–3279

    Article  CAS  PubMed  Google Scholar 

  • Puce A, Allison T, Asgari M, Gore JC, McCarthy G (1996) Differential sensitivity of human visual cortex to faces, letterstrings, and textures: a functional magnetic resonance imaging study. J Neurosci 16(16):5205–5215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Puce A, Allison T, Bentin S, Gore JC, McCarthy G (1998) Temporal cortex activation in humans viewing eye and mouth movements. J Neurosci 18(6):2188–2199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pyles JA, Verstynen TD, Schneider W, Tarr MJ (2013) Explicating the face perception network with white matter connectivity. PloS One 8(4):e61611

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ramot M, Walsh C, Martin A (2019) Multifaceted integration: memory for faces is subserved by widespread connections between visual, memory, auditory, and social networks. J Neurosci 39(25):4976–4985

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rangarajan V, Hermes D, Foster BL, Weiner KS, Jacques C, Grill-Spector K, Parvizi J (2014) Electrical stimulation of the left and right human fusiform gyrus causes different effects in conscious face perception. J Neurosci 34(38):12828–12836

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reed CL, Stone VE, Bozova S, Tanaka J (2003) The body-inversion effect. Psychol Sci 14(4):302–308

    Article  CAS  PubMed  Google Scholar 

  • Rivolta D, Lawson RP, Palermo R (2017) More than just a problem with faces: altered body perception in a group of congenital prosopagnosics. Quarterly Journal of Experimental Psychology 70(2):276–286

    Article  Google Scholar 

  • Ross P, George E (2021) Are face masks a problem for emotion recognition? Not when the whole body is visible. PsyArxiv. https://psyarxiv.com/c5x97

  • Rossion B, Caldara R, Seghier M, Schuller AM, Lazeyras F, Mayer E (2003) A network of occipito-temporal face-sensitive areas besides the right middle fusiform gyrus is necessary for normal face processing. Brain 126(11):2381–2395

    Article  PubMed  Google Scholar 

  • Russ BE, Leopold DA (2015) Functional MRI map** of dynamic visual features during natural viewing in the macaque. Neuroimage 109:84–94

    Article  PubMed  Google Scholar 

  • Sadagopan S, Zarco W, Freiwald WA (2017) A causal relationship between face-patch activity and face-detection behavior. Elife 6:e18558

    Article  PubMed  PubMed Central  Google Scholar 

  • Saygin ZM, Osher DE, Koldewyn K, Reynolds G, Gabrieli JD, Saxe RR (2012) Anatomical connectivity patterns predict face selectivity in the fusiform gyrus. Nat Neurosci 15(2):321–327

    Article  CAS  Google Scholar 

  • Schaeffer DJ, Selvanayagam J, Johnston KD, Menon RS, Freiwald WA, Everling S (2020) Face selective patches in marmoset frontal cortex. Nat Commun 11(1):1–8

    Article  CAS  Google Scholar 

  • Schalk G, Kapeller C, Guger C, Ogawa H, Hiroshima S, Lafer-Sousa R, Saygin ZM, Kamada K, Kanwisher N (2017) Facephenes and rainbows: Causal evidence for functional and anatomical specificity of face and color processing in the human brain. Proc Natl Acad Sci 114(46):12285–12290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmalzl L, Zopf R, Williams MA (2012) From head to toe: evidence for selective brain activation reflecting visual perception of whole individuals. Front Hum Neurosci 6:108

    Article  PubMed  PubMed Central  Google Scholar 

  • Schwarzlose RF, Baker CI, Kanwisher N (2005) Separate face and body selectivity on the fusiform gyrus. J Neurosci 25(47):11055–11059

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schwiedrzik CM, Zarco W, Everling S, Freiwald WA (2015) Face patch resting state networks link face processing to social cognition. PLoS Biol 13(9):e1002245

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sereno MI, Dale AM, Reppas JB, Kwong KK, Belliveau JW, Brady TJ, Rosen BR, Tootell RB (1995) Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. Science 268(5212):889–893

    Article  CAS  PubMed  Google Scholar 

  • Shah P, Gaule A, Gaigg SB, Bird G, Cook R (2015) Probing short-term face memory in developmental prosopagnosia. Cortex 64:115–122

    Article  PubMed  Google Scholar 

  • Silson EH, Chan AWY, Reynolds RC, Kravitz DJ, Baker CI (2015) A retinotopic basis for the division of high-level scene processing between lateral and ventral human occipitotemporal cortex. J Neurosci 35(34):11921–11935

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Silson EH, Groen II, Kravitz DJ, Baker CI (2016) Evaluating the correspondence between face-, scene-, and object-selectivity and retinotopic organization within lateral occipitotemporal cortex. J Vis 16(6):14–14

    Article  PubMed  PubMed Central  Google Scholar 

  • Slaughter V, Stone VE, Reed C (2004) Perception of faces and bodies: similar or different? Curr Dir Psychol Sci 13(6):219–223

    Article  Google Scholar 

  • Sliwa J, Freiwald WA (2017) A dedicated network for social interaction processing in the primate brain. Science 356(6339):745–749

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song Y, Luo YL, Li X, Xu M, Liu J (2013) Representation of contextually related multiple objects in the human ventral visual pathway. J Cogn Neurosci 25(8):1261–1269

    Article  PubMed  Google Scholar 

  • Sonkusare S, Breakspear M, Guo C (2019) Naturalistic stimuli in neuroscience: critically acclaimed. Trends Cogn Sci 23(8):699–714

    Article  PubMed  Google Scholar 

  • Sorger B, Goebel R, Schiltz C, Rossion B (2007) Understanding the functional neuroanatomy of acquired prosopagnosia. Neuroimage 35(2):836–852

    Article  PubMed  Google Scholar 

  • Spiridon M, Fischl B, Kanwisher N (2006) Location and spatial profile of category-specific regions in human extrastriate cortex. Hum Brain Mapp 27(1):77–89

    Article  PubMed  Google Scholar 

  • Suchan B, Bauser DS, Busch M, Schulte D, Grönemeyer D, Herpertz S, Vocks S (2013) Reduced connectivity between the left fusiform body area and the extrastriate body area in anorexia nervosa is associated with body image distortion. Behav Brain Res 241:80–85

    Article  PubMed  Google Scholar 

  • Sugita Y (2008) Face perception in monkeys reared with no exposure to faces. Proc Natl Acad Sci 105(1):394–398

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Susilo T, Yovel G, Barton JJ, Duchaine B (2013) Face perception is category-specific: evidence from normal body perception in acquired prosopagnosia. Cognition 129(1):88–94

    Article  PubMed  Google Scholar 

  • Susilo T, Yang H, Potter Z, Robbins R, Duchaine B (2015) Normal body perception despite the loss of right fusiform gyrus. J Cogn Neurosci 27(3):614–622

    Article  PubMed  Google Scholar 

  • Tarhan L, Konkle T (2020) Sociality and interaction envelope organize visual action representations. Nat Commun 11(1):1–11

    Article  CAS  Google Scholar 

  • Taubert J, Van Belle G, Vanduffel W, Rossion B, Vogels R (2015) The effect of face inversion for neurons inside and outside fMRI-defined face-selective cortical regions. J Neurophysiol 113(5):1644–1655

    Article  PubMed  Google Scholar 

  • Taubert J, Flessert M, Wardle SG, Basile BM, Murphy AP, Murray EA, Ungerleider LG (2018) Amygdala lesions eliminate viewing preferences for faces in rhesus monkeys. Proc Natl Acad Sci 115(31):8043–8048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taubert J, Japee S, Murphy AP, Tardiff CT, Koele EA, Kumar S, Leopold DA, Ungerleider LG (2020) Parallel processing of facial expression and head orientation in the macaque brain. J Neurosci 40(42):8119–8131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor JC, Downing PE (2011) Division of labor between lateral and ventral extrastriate representations of faces, bodies, and objects. J Cogn Neurosci 23(12):4122–4137

    Article  PubMed  Google Scholar 

  • Thompson JC, Hardee JE, Panayiotou A, Crewther D, Puce A (2007) Common and distinct brain activation to viewing dynamic sequences of face and hand movements. Neuroimage 37(3):966–973

    Article  PubMed  Google Scholar 

  • Tsao DY, Livingstone MS (2008) Mechanisms of face perception. Annu Rev Neurosci 31:411–437

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsao DY, Freiwald WA, Knutsen TA, Mandeville JB, Tootell RB (2003) Faces and objects in macaque cerebral cortex. Nat Neurosci 6(9):989–995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsao DY, Freiwald WA, Tootell RB, Livingstone MS (2006) A cortical region consisting entirely of face-selective cells. Science 311(5761):670–674

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsao DY, Schweers N, Moeller S, Freiwald WA (2008) Patches of face-selective cortex in the macaque frontal lobe. Nat Neurosci 11(8):877

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsunoda K, Yamane Y, Nishizaki M, Tanifuji M (2001) Complex objects are represented in macaque inferotemporal cortex by the combination of feature columns. Nat Neurosci 4(8):832–838

    Article  CAS  PubMed  Google Scholar 

  • van den Hurk J, Van Baelen M, Op de Beeck HP (2017) Development of visual category selectivity in ventral visual cortex does not require visual experience. Proc Natl Acad Sci 114(22):E4501–E4510

    PubMed  PubMed Central  Google Scholar 

  • van Koningsbruggen MG, Peelen MV, Downing PE (2013) A causal role for the extrastriate body area in detecting people in real-world scenes. J Neurosci 33(16):7003–7010

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vangeneugden J, Peelen MV, Tadin D, Battelli L (2014) Distinct neural mechanisms for body form and body motion discriminations. J Neurosci 34(2):574–585

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vinken K, Vogels R (2019) A behavioral face preference deficit in a monkey with an incomplete face patch system. Neuroimage 189:415–424

    Article  PubMed  Google Scholar 

  • Vuilleumier P, Pourtois G (2007) Distributed and interactive brain mechanisms during emotion face perception: evidence from functional neuroimaging. Neuropsychologia 45(1):174–194

    Article  PubMed  Google Scholar 

  • Wachsmuth E, Oram MW, Perrett DI (1994) Recognition of objects and their component parts: responses of single units in the temporal cortex of the macaque. Cereb Cortex 4(5):509–522

    Article  CAS  PubMed  Google Scholar 

  • Wandell BA, Dumoulin SO, Brewer AA (2007) Visual field maps in human cortex. Neuron 56(2):366–383

    Article  CAS  PubMed  Google Scholar 

  • Webster MJ, Ungerleider LG, Bachevalier J (1991) Connections of inferior temporal areas TE and TEO with medial temporal-lobe structures in infant and adult monkeys. J Neurosci 11(4):1095–1116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weiner KS, Grill-Spector K (2010) Sparsely-distributed organization of face and limb activations in human ventral temporal cortex. Neuroimage 52(4):1559–1573

    Article  PubMed  Google Scholar 

  • Weiner KS, Grill-Spector K (2013) Neural representations of faces and limbs neighbor in human high-level visual cortex: evidence for a new organization principle. Psychol Res 77(1):74–97

    Article  PubMed  Google Scholar 

  • Zhang H, Japee S, Stacy A, Flessert M, Ungerleider LG (2020) Anterior superior temporal sulcus is specialized for non-rigid facial motion in both monkeys and humans. NeuroImage 218:116878

    Article  PubMed  Google Scholar 

  • Zhu Q, Zhang J, Luo YL, Dilks DD, Liu J (2011) Resting-state neural activity across face-selective cortical regions is behaviorally relevant. J Neurosci 31(28):10323–10330

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This research was supported by the Intramural Research Program of the National Institute of Mental Health (ZIAMH002909 to C.I.B). J.T. was supported by funding from the Australian Research Council (FT200100843).

Author information

Authors and Affiliations

Authors

Contributions

JT, JBR, and LGU developed the ideas for the original draft; JT, JBR, and CIB, wrote and edited the final version of the manuscript.

Corresponding author

Correspondence to J. Brendan Ritchie.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Ethical approval

Not applicable.

Additional information

Publisher's Note

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

Leslie G. Ungerleider passed away suddenly on the 11th of December 2020 after hel** to prepare the original manuscript for submission with the expectation of authorship.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Taubert, J., Ritchie, J.B., Ungerleider, L.G. et al. One object, two networks? Assessing the relationship between the face and body-selective regions in the primate visual system. Brain Struct Funct 227, 1423–1438 (2022). https://doi.org/10.1007/s00429-021-02420-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-021-02420-7

Keywords

Navigation