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Research Articles, Behavioral/Cognitive

Multiple Adjoining Word- and Face-Selective Regions in Ventral Temporal Cortex Exhibit Distinct Dynamics

Matthew J. Boring, Edward H. Silson, Michael J. Ward, R. Mark Richardson, Julie A. Fiez, Chris I. Baker and Avniel Singh Ghuman
Journal of Neuroscience 21 July 2021, 41 (29) 6314-6327; DOI: https://doi.org/10.1523/JNEUROSCI.3234-20.2021
Matthew J. Boring
1Center for Neuroscience at the University of Pittsburgh, University of Pittsburgh, Pittsburgh, Pennsylvania 15260
2Center for the Neural Basis of Cognition, Pittsburgh, Pennsylvania 15213
3Department of Neurological Surgery, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania 15213
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Edward H. Silson
4National Institute of Mental Health, National Institutes of Health, Magnuson Clinical Center, Bethesda, Maryland 20814
5School of Philosophy, Psychology and Language Sciences, University of Edinburgh, Edinburgh, EH8 9JZ, United Kingdom
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Michael J. Ward
3Department of Neurological Surgery, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania 15213
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R. Mark Richardson
3Department of Neurological Surgery, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania 15213
6Department of Neurosurgery, Massachusetts General Hospital, Boston, Massachusetts 02144
7Harvard Medical School, Boston, Massachusetts 02115
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Julie A. Fiez
1Center for Neuroscience at the University of Pittsburgh, University of Pittsburgh, Pittsburgh, Pennsylvania 15260
2Center for the Neural Basis of Cognition, Pittsburgh, Pennsylvania 15213
8Department of Psychology, University of Pittsburgh, Pittsburgh, Pennsylvania 15260
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Chris I. Baker
4National Institute of Mental Health, National Institutes of Health, Magnuson Clinical Center, Bethesda, Maryland 20814
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Avniel Singh Ghuman
1Center for Neuroscience at the University of Pittsburgh, University of Pittsburgh, Pittsburgh, Pennsylvania 15260
2Center for the Neural Basis of Cognition, Pittsburgh, Pennsylvania 15213
3Department of Neurological Surgery, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania 15213
8Department of Psychology, University of Pittsburgh, Pittsburgh, Pennsylvania 15260
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Abstract

The map of category-selectivity in human ventral temporal cortex (VTC) provides organizational constraints to models of object recognition. One important principle is lateral-medial response biases to stimuli that are typically viewed in the center or periphery of the visual field. However, little is known about the relative temporal dynamics and location of regions that respond preferentially to stimulus classes that are centrally viewed, such as the face- and word-processing networks. Here, word- and face-selective regions within VTC were mapped using intracranial recordings from 36 patients. Partially overlapping, but also anatomically dissociable patches of face- and word-selectivity, were found in VTC. In addition to canonical word-selective regions along the left posterior occipitotemporal sulcus, selectivity was also located medial and anterior to face-selective regions on the fusiform gyrus at the group level and within individual male and female subjects. These regions were replicated using 7 Tesla fMRI in healthy subjects. Left hemisphere word-selective regions preceded right hemisphere responses by 125 ms, potentially reflecting the left hemisphere bias for language, with no hemispheric difference in face-selective response latency. Word-selective regions along the posterior fusiform responded first, then spread medially and laterally, then anteriorally. Face-selective responses were first seen in posterior fusiform regions bilaterally, then proceeded anteriorally from there. For both words and faces, the relative delay between regions was longer than would be predicted by purely feedforward models of visual processing. The distinct time courses of responses across these regions, and between hemispheres, suggest that a complex and dynamic functional circuit supports face and word perception.

SIGNIFICANCE STATEMENT Representations of visual objects in the human brain have been shown to be organized by several principles, including whether those objects tend to be viewed centrally or peripherally in the visual field. However, it remains unclear how regions that process objects that are viewed centrally, such as words and faces, are organized relative to one another. Here, invasive and noninvasive neuroimaging suggests that there is a mosaic of regions in ventral temporal cortex that respond selectively to either words or faces. These regions display differences in the strength and timing of their responses, both within and between brain hemispheres, suggesting that they play different roles in perception. These results illuminate extended, bilateral, and dynamic brain pathways that support face perception and reading.

  • electrocorticography
  • fMRI
  • fusiform-face area
  • intracranial electroencephalography
  • ventral stream
  • visual word-form area

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The Journal of Neuroscience: 41 (29)
Journal of Neuroscience
Vol. 41, Issue 29
21 Jul 2021
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Multiple Adjoining Word- and Face-Selective Regions in Ventral Temporal Cortex Exhibit Distinct Dynamics
Matthew J. Boring, Edward H. Silson, Michael J. Ward, R. Mark Richardson, Julie A. Fiez, Chris I. Baker, Avniel Singh Ghuman
Journal of Neuroscience 21 July 2021, 41 (29) 6314-6327; DOI: 10.1523/JNEUROSCI.3234-20.2021

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Multiple Adjoining Word- and Face-Selective Regions in Ventral Temporal Cortex Exhibit Distinct Dynamics
Matthew J. Boring, Edward H. Silson, Michael J. Ward, R. Mark Richardson, Julie A. Fiez, Chris I. Baker, Avniel Singh Ghuman
Journal of Neuroscience 21 July 2021, 41 (29) 6314-6327; DOI: 10.1523/JNEUROSCI.3234-20.2021
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Keywords

  • electrocorticography
  • fMRI
  • fusiform-face area
  • intracranial electroencephalography
  • ventral stream
  • visual word-form area

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