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Differential Sensitivity of Human Visual Cortex to Faces, Letterstrings, and Textures: A Functional Magnetic Resonance Imaging Study
Open accessAbstract
Twelve normal subjects viewed alternating sequences of unfamiliar faces, unpronounceable nonword letterstrings, and textures while echoplanar functional magnetic resonance images were acquired in seven slices extending from the posterior margin of the splenium to near the occipital pole. These stimuli were chosen to elicit initial category-specific processing in extrastriate cortex while minimizing semantic processing. Overall, faces evoked more activation than did letterstrings. Comparing hemispheres, faces evoked greater activation in the right than the left hemisphere, whereas letterstrings evoked greater activation in the left than the right hemisphere. Faces primarily activated the fusiform gyrus bilaterally, and also activated the right occipitotemporal and inferior occipital sulci and a region of lateral cortex centered in the middle temporal gyrus. Letterstrings primarily activated the left occipitotemporal and inferior occipital sulci. Textures primarily activated portions of the collateral sulcus. In the left hemisphere, 9 of the 12 subjects showed a characteristic pattern in which faces activated a discrete region of the lateral fusiform gyrus, whereas letterstrings activated a nearby region of cortex within the occipitotemporal and inferior occipital sulci. These results suggest that different regions of ventral extrastriate cortex are specialized for processing the perceptual features of faces and letterstrings, and that these regions are intermediate between earlier processing in striate and peristriate cortex, and later lexical, semantic, and associative processing in downstream cortical regions.
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“Puce et al. (1996) report single-subject activations during passive presentation of visual words, faces, and textures. Nine out of twelve subjects showed greater activation to words than to faces in the left occipitotemporal sulcus, although a neighboring but slightly more mesial site conversely showed preferential activation to faces than to words.”
From Specialization within the ventral stream: the case for the visual word form area (2004) · cites this paper as Puce et al. (1996)
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“The region that activates to visual words is well delimited and occupies a fixed location relative to other regions that preferentially respond to faces, houses, or objects (Hasson et al., 2002, 2003; Puce et al., 1996).”
From Specialization within the ventral stream: the case for the visual word form area (2004) · cites this paper as Puce et al., 1996
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BackgroundInfluentialChange Blindness to Gradual Changes in Facial Expressions
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“…the ventral temporal cortex (VTC), the inferior occipital gyrus (IOG), and the posterior superior temporal sulcus (STS) have been suggested to respond preferentially to faces compared with other visual stimuli (Puce et al. 1996; Kanwisher 2010; Haxby and Gobbini 2011).”
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“…and PCiG are located in the occipitotemporal area, which is believed to play an important role as a gateway from lower to higher visual processes (Puce et al., 1996; Tarkiainen et al., 2002; Jobard et al., 2003), in particular the identification of landmarks and places (Aguirre and D’Esposito,…”
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“…ITG activation requires both perception of and attention to digits, digit processing in the ITG would function differently than letter or word processing in the VWFA, which responds to passive viewing of words or letter strings (Cohen et al., 2002; Mei et al., 2010; Puce et al., 1996).”
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“Nevertheless, the fact that the left fusiform gyrus responds to letters or letter strings more than to other objects like faces, digits or geometric shapes (Baker et al., 2007; Cohen et al., 2003; Polk et al., 2002; Puce et al., 1996) would indicate that the semantic associations of words are not required to activate…”
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“The observed category-specific face effect was consistent with the concept of category-specific model, which posits a neural module for face category as distinct from non-face (Allison et al., 1994b; Clark, Keil, Maisog, Courtney, Ungerleider, & Haxby, 1996; Haxby, Ungerleider, Clarke, Schouten, Hoffman, & Martin, 199…”
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“Indeed, there are large specialized face-processing areas in posterior occipital, fusiform, and superior temporal sulcus regions, which are distinct from those representing other parts of human body (Puce et al., 1996; Kanwisher et al., 1997; Allison et al., 2000; Thierry et al., 2006).”
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“Converging evidence has shown that STS is a fundamental hub for social cognition, being involved in the perception of faces (Puce et al., 1996), voices (Belin et al.”
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“Therefore, we suggest that the dissociations observed are more in line with the view that faces and words rely on entirely distinct neural circuits in the VOTC (Farah 1991; Puce et al. 1996; Dehaene-Lambertz et al. 2018).”
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Letter-specific processing in children and adults matched for reading level
Burgund, E. D., & Abernathy, A. E. (2008) · Acta Psychologica · doi:10.1016/j.actpsy.2008.04.007 · Cited by 16
“Greater neural activity for letters than non-letters has been observed in expert readers in the left occipito-temporal cortex in several studies (e.g., James et al., 2005; Pernet et al., 2005; Price et al., 1996; Puce et al., 1996 ), leading some to label this region a ‘visual word form area’ (Cohen & Dehaene, 2004; C…”
BackgroundA comparison of letter and digit processing in letter-by-letter reading
Ingles, J. L., & Eskes, G. A. (2007) · Journal of the International Neuropsychological Society · doi:10.1017/s1355617708080119 · Cited by 15
fMRI: applications to cognitive neuroscience
Owen, A. M., Epstein, R. A., & Johnsrude, I. S. (2001) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780192630711.003.0017 · Cited by 15
Tanaka, H., & Jiang, P. (2024) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_02167 · Cited by 14
“fMRI (Puce, Allison, Asgari, Gore, & McCarthy, 1996; Puce, Allison, Gore, & MacCarthy, 1995) studies have shown that the fusiform gyrus of the human brain is active in face perception processing.”
BackgroundGeneral object-based features account for letter perception
Janini, D., Hamblin, C. J., Deza, A., & Konkle, T. (2022) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1010522 · Cited by 18
“…adults, a region of inferotemporal cortex termed the visual word form area exhibits preferential responses to letter strings, with perhaps the highest responses reserved for the letters of one’s own alphabet (C. I. Baker et al., 2007; L. Cohen et al., 2002; Hasson et al., 2002; Puce et al., 1996).”
BackgroundSecond language research using magnetoencephalography: a review
Schmidt, G. L., & Roberts, T. P. L. (2009) · Second language Research · doi:10.1177/0267658308098999 · Cited by 14
“…interpreted with respect to the established lateralization of the fusiform gyrus, with the right side being primarily recruited for whole object processing, such as in face processing tasks, and the left in the processing of smaller parts of objects, such as with letter strings (Puce et al., 1996).”
BackgroundNeural Correlates of Face Detection
Xu, X., & Biederman, I. (2013) · Cerebral Cortex · doi:10.1093/cercor/bht005 · Cited by 14
“Specifically, the fusiform and occipital face areas (FFA and OFA, respectively) have been suggested as neural loci for the conscious perception of faces versus nonface objects: Higher activation in FFA has been found not only in viewing faces versus nonfaces (Puce et al. 1996; Kanwisher et al. 1997), but also in the c…”
BackgroundNeural sources of letter and Vernier acuity
Barzegaran, E., & Norcia, A. M. (2020) · Scientific Reports · doi:10.1038/s41598-020-72370-3 · Cited by 14
Sanada, T., Kapeller, C., Jordan, M., Grünwald, J., Mitsuhashi, T., Ogawa, H., Anei, R., & Guger, C. (2021) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2021.616591 · Cited by 13
Kajiyama, Y., Hattori, N., Nakano, T., Revankar, G. S., Otomune, H., Hashimoto, R., Mori, E., Ikeda, M., Mihara, M., & Mochizuki, H. (2021) · npj Parkinson s Disease · doi:10.1038/s41531-021-00237-z · Cited by 14
Investigations of the human visual system using functional magnetic resonance imaging (FMRI)
Kollias, S. (2003) · European Journal of Radiology · doi:10.1016/j.ejrad.2003.09.005 · Cited by 14
“Whereas area LO responds to all objects regardless of object recognition, other areas specialized for the perception of complex object categories as faces, letterstrings, buildings, have been identified within specialized regions of the ventral occipitotemporal extrastriate cortex [32,48–50].”
BackgroundThe Brain Network for Haptic Object Recogniton
Kitada, R. (2016) · Springer eBooks · doi:10.1007/978-4-431-55772-2_2 · Cited by 15
A voxel-wise assessment of growth differences in infants developing autism spectrum disorder
de la Parra, A. C., Lewis, J. D., Fonov, V., Botteron, K. N., McKinstry, R. C., Gerig, G., Pruett, J. R., Dager, S. R., Elison, J. T., Styner, M. A., et al. (2020) · NeuroImage Clinical · doi:10.1016/j.nicl.2020.102551 · Cited by 14
“The right fusiform gyrus has been consistently reported to be involved in face processing tasks (Allison et al., 1994; Puce et al., 1996), and has been found to have increased volume in adolescents and adults with ASD (Rojas et al.”
Different neural systems for recognizing plants, animals, and artifacts
Kawashima, R., Hatano, G., OIZUMI, K., Sugiura, M., Fukuda, H., Itoh, K., Kato, T., Nakamura, A., Hatano, K., & Kojima, S. (2001) · Brain Research Bulletin · doi:10.1016/s0361-9230(00)00440-8 · Cited by 14
Tassinari, C. A., Cantalupo, G., & Rubboli, G. (2015) · Epileptic Disorders · doi:10.1684/epd.2015.0760 · Cited by 14
Galván, A., & Tottenham, N. (2016) · Wiley eBooks · doi:10.1002/9781119125556.devpsy218 · Cited by 14
Increased Visual Stimulation Systematically Decreases Activity in Lateral Intermediate Cortex
Nasr, S., Stemmann, H., Vanduffel, W., & Tootell, R. B. H. (2014) · Cerebral Cortex · doi:10.1093/cercor/bhu290 · Cited by 13
“…(Haxby et al. 2000; Winston et al. 2004; Engell and Haxby 2007; Said et al. 2011), and also the visual interpretation of biological motion (Puce et al. 1996; Beauchamp et al. 2003; Thompson et al. 2007; Fox et al. 2009; Jastorff and Orban 2009; Pinsk et al. 2009; Furl et al. 2011; Julian…”
BackgroundFace Processing in Children: Novel MEG Findings
Taylor, M. J., Mills, T., Zhang, L., & Pang, E. W. (2010) · World Congress on Medical Physics and Biomedical Engineering, September 7 - 12, 2009, Munich, Germany · doi:10.1007/978-3-642-12197-5_73 · Cited by 13
Faces are special, but facial expressions aren’t: Insights from an oculomotor capture paradigm
Devue, C., & Grimshaw, G. M. (2017) · Attention Perception & Psychophysics · doi:10.3758/s13414-017-1313-x · Cited by 15
A longitudinal study of infant view-invariant face processing during the first 3–8 months of life
Ichikawa, H., Nakato, E., Igarashi, Y., Okada, M., Kanazawa, S., Yamaguchi, M. K., & Kakigi, R. (2018) · NeuroImage · doi:10.1016/j.neuroimage.2018.11.031 · Cited by 13
Watson, J. D. G. (2000) · Elsevier eBooks · doi:10.1016/b978-012692545-6/50011-8 · Cited by 13
Dynamic Brain Activation Patterns for Face Recognition: A Magnetoencephalography Study
Lee, D., Simos, P. G., Sawrie, S. M., Martin, R. C., & Knowlton, R. C. (2005) · Brain Topography · doi:10.1007/s10548-005-7897-9 · Cited by 13
Lambert, N. A., Swain, M. A., Miller, L. A., & Caine, D. (2006) · Neuropsychology · doi:10.1037/0894-4105.20.3.346 · Cited by 13
14 Animacy and Intention in the Brain: Neuroscience of Social Event Perception
Heberlein, A. S. (2008) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780195188370.003.0016 · Cited by 13
Human visual object recognition: What have we learned from neuroimaging?
Aguirre, G. K., & Farah, M. J. (1998) · Psychobiology · doi:10.3758/bf03330619 · Cited by 13
Distributed representations of behavior-derived object dimensions in the human visual systemPreprint
Contier, O., Baker, C. I., & Hebart, M. N. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.08.23.553812 · Cited by 13
“While effects of representational sparseness were less pronounced in scene-selective regions and largely absent in text-selective regions 10 , our encoding model significantly predicted brain responses in scene-selective regions (Suppl.”
Harel, A., & Shlomo Bentin, A. (2013) · PLoS ONE · doi:10.1371/journal.pone.0067024 · Cited by 12
“This remarkable ability has been attributed by some to specifically tuned neural mechanisms distinguished by behavioral [1], electrophysiological [2], and neuroimaging [3–4] markers.”
Thomsen, J. A., Kühn, C. D., Gerlach, C., Delfi, T., & Starrfelt, R. (2019) · Visual Cognition · doi:10.1080/13506285.2019.1599481 · Cited by 13
Jacobs, R. H. A. H., Haak, K. V., Thumfart, S., Renken, R. J., Henson, B. W., & Cornelissen, F. W. (2016) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2016.00343 · Cited by 12
“Using Textures to Examine Aesthetic Responses The study of texture processing is interesting in itself because evidence is accumulating that textures are processed in dedicated visual processing regions, which are located mainly along the medial visual cortex (Puce et al., 1996; Peuskens et al., 2004; Cant and Goodale…”
MethodBala, A., Iwański, S., Żyłkowski, J., Jaworski, M., Seniów, J. B., & Marchel, A. (2014) · Neurocase · doi:10.1080/13554794.2014.892999 · Cited by 12
Magnetic brain activity elicited by visually presented symbols and Japanese characters
Shirahama, Y., Ohta, K., Takashima, A., Matsushima, E., & Okubo, Y. (2004) · Neuroreport · doi:10.1097/00001756-200404090-00006 · Cited by 12
Kincses, Z. T., Chadaide, Z., Varga, E. T., Antal, A., & Paulus, W. (2006) · Brain Research · doi:10.1016/j.brainres.2006.07.044 · Cited by 12
Effects of Facial Identity, Facial Expression, and Subject's Sex on Laterality in Monkeys
Vermeire, B. A., & Hamilton, C. R. (1998) · Laterality Asymmetries of Body Brain and Cognition · doi:10.1080/713754290 · Cited by 12
The objects of action and perception
Goodale, M. A., & Humphrey, G. K. (1999) · The MIT Press eBooks · doi:10.7551/mitpress/5089.003.0007 · Cited by 12
Psychiatric sequelae of stroke affecting the non-dominant cerebral hemisphere
Guo, C. R., Stretz, C., Anderson, J., El-Husseini, N., Grory, B. M., Werner, B., & Yarnell, S. C. (2021) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2021.120007 · Cited by 11
Laurent, M.-A., Audurier, P., Castro, V. D., Gao, X., Durand, J., Jonas, J., Rossion, B., & Cottereau, B. R. (2023) · NeuroImage · doi:10.1016/j.neuroimage.2023.119959 · Cited by 11
“As in the very first human fMRI studies on face perception (Puce et al., 1995; Puce et al., 1996), this face localizer is based on the principle of frequency-tagging, with face-selective activity identified objectively in the frequency spectrum at a periodic rate of face stimulation among non-face…”
Neural correlates of subliminal and supraliminal letter processing—An event-related fMRI study
Heinzel, A., Hautzel, H., Poeppel, T. D., Boers, F., Beu, M., & Mueller, H.-W. (2008) · Consciousness and Cognition · doi:10.1016/j.concog.2008.01.008 · Cited by 11
“…single letter perception employing various types of tasks (Flowers et al., 2004; Joseph et al., 2006, 2003; Polk & Farah, 1998; Polk et al., 2002; Puce et al., 1996; Tagamets et al., 2000; Tarkiainen et al., 2002) as well as with our own results demonstrating conscious letter processing in BA 37.”
Metadata
- Authors
- Puce, A., Allison, T., Asgari, M., Gore, J. C., & McCarthy, G.
- Affiliations
- United States Department of Veterans Affairs (US)
- Yale University (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 1996-08-15
- Volume
- 16
- Issue
- 16
- Pages
- 5205-5215
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6579313
- OpenAlex
- W2172253232
- Cited by
- 987
- References
- 50
- Citations by year
- 2026: 7 · 2025: 14 · 2024: 20 · 2023: 19 · 2022: 19 · 2021: 20 · 2020: 24 · 2019: 21 · 2018: 27 · 2017: 26 · 2016: 21 · 2015: 32 · 2014: 33 · 2013: 54 · 2012: 43
- FWCI
- 16.33
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- IUScholarWorks (Indiana University) (submittedVersion, cc-by-nc-sa)
- Funders
- U.S. Department of Veterans Affairs
- National Institute of Mental Health (MH-05 286, R01MH005286)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Face Recognition and Perception
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Social Sciences › Psychology › Developmental and Educational Psychology › Reading and Literacy Development
- Keywords
- face processing, texture processing, fusiform gyrus, extrastriate cortex, hemispheric lateralization, right hemisphere, collateral sulcus, middle temporal gyrus, ventral stream
- MeSH terms
- Adult, Brain Mapping, Face, Female, Humans, Magnetic Resonance Imaging, Male, Pattern Recognition, Visual, Photic Stimulation, Visual Cortex, Visual Pathways
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