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J Neurosci. 2016 Aug 10;36(32):8425-40. doi: 10.1523/JNEUROSCI.4509-15.2016.

The Face-Processing Network Is Resilient to Focal Resection of Human Visual Cortex.

Author information

1
Department of Psychology, Stanford University, Stanford, California 94305, kweiner@stanford.edu.
2
Department of Neurology and Neurosurgery, University Hospital of Nancy, 54000 Nancy, France, Psychological Science Research Institute and Institute of Neuroscience, University of Louvain, 1348 Louvain-la-Neuve, Belgium, CRAN, UMR 7039, CNRS and University of Lorraine, 54000 Nancy, France.
3
Neurosciences Institute, Stanford University, Stanford, California 94305.
4
Department of Neurology and Neurosurgery, University Hospital of Nancy, 54000 Nancy, France, CRAN, UMR 7039, CNRS and University of Lorraine, 54000 Nancy, France.
5
Department of Neurology and Neurosurgery, University Hospital of Nancy, 54000 Nancy, France.
6
Clinical Investigation Centre Innovative Technology, University Hospital of Nancy, 54000 Nancy, France, and.
7
Psychological Science Research Institute and Institute of Neuroscience, University of Louvain, 1348 Louvain-la-Neuve, Belgium.
8
Department of Psychology, Pomona College, Claremont, California 91711.
9
Department of Psychology, Stanford University, Stanford, California 94305.
10
Department of Psychology, Stanford University, Stanford, California 94305, Neurosciences Institute, Stanford University, Stanford, California 94305.

Abstract

Human face perception requires a network of brain regions distributed throughout the occipital and temporal lobes with a right hemisphere advantage. Present theories consider this network as either a processing hierarchy beginning with the inferior occipital gyrus (occipital face area; IOG-faces/OFA) or a multiple-route network with nonhierarchical components. The former predicts that removing IOG-faces/OFA will detrimentally affect downstream stages, whereas the latter does not. We tested this prediction in a human patient (Patient S.P.) requiring removal of the right inferior occipital cortex, including IOG-faces/OFA. We acquired multiple fMRI measurements in Patient S.P. before and after a preplanned surgery and multiple measurements in typical controls, enabling both within-subject/across-session comparisons (Patient S.P. before resection vs Patient S.P. after resection) and between-subject/across-session comparisons (Patient S.P. vs controls). We found that the spatial topology and selectivity of downstream ipsilateral face-selective regions were stable 1 and 8 month(s) after surgery. Additionally, the reliability of distributed patterns of face selectivity in Patient S.P. before versus after resection was not different from across-session reliability in controls. Nevertheless, postoperatively, representations of visual space were typical in dorsal face-selective regions but atypical in ventral face-selective regions and V1 of the resected hemisphere. Diffusion weighted imaging in Patient S.P. and controls identifies white matter tracts connecting retinotopic areas to downstream face-selective regions, which may contribute to the stable and plastic features of the face network in Patient S.P. after surgery. Together, our results support a multiple-route network of face processing with nonhierarchical components and shed light on stable and plastic features of high-level visual cortex following focal brain damage.

SIGNIFICANCE STATEMENT:

Brain networks consist of interconnected functional regions commonly organized in processing hierarchies. Prevailing theories predict that damage to the input of the hierarchy will detrimentally affect later stages. We tested this prediction with multiple brain measurements in a rare human patient requiring surgical removal of the putative input to a network processing faces. Surprisingly, the spatial topology and selectivity of downstream face-selective regions are stable after surgery. Nevertheless, representations of visual space were typical in dorsal face-selective regions but atypical in ventral face-selective regions and V1. White matter connections from outside the face network may support these stable and plastic features. As processing hierarchies are ubiquitous in biological and nonbiological systems, our results have pervasive implications for understanding the construction of resilient networks.

KEYWORDS:

brain lesion; cortical plasticity; face perception; fusiform face area; hierarchical networks; occipital face area

PMID:
27511014
PMCID:
PMC4978802
DOI:
10.1523/JNEUROSCI.4509-15.2016
[Indexed for MEDLINE]
Free PMC Article

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