Dataset Information

Looking beyond the face area: lesion network mapping of prosopagnosia.

ABSTRACT: Damage to the right fusiform face area can disrupt the ability to recognize faces, a classic example of how damage to a specialized brain region can disrupt a specialized brain function. However, similar symptoms can arise from damage to other brain regions, and face recognition is now thought to depend on a distributed brain network. The extent of this network and which regions are critical for facial recognition remains unclear. Here, we derive this network empirically based on lesion locations causing clinically significant impairments in facial recognition. Cases of acquired prosopagnosia were identified through a systematic literature search and lesion locations were mapped to a common brain atlas. The network of brain regions connected to each lesion location was identified using resting state functional connectivity from healthy participants (n = 1000), a technique termed lesion network mapping. Lesion networks were overlapped to identify connections common to lesions causing prosopagnosia. Reproducibility was assessed using split-half replication. Specificity was assessed through comparison with non-specific control lesions (n = 135) and with control lesions associated with symptoms other than prosopagnosia (n = 155). Finally, we tested whether our facial recognition network derived from clinically evident cases of prosopagnosia could predict subclinical facial agnosia in an independent lesion cohort (n = 31). Our systematic literature search identified 44 lesions causing prosopagnosia, only 29 of which intersected the right fusiform face area. However, all 44 lesion locations fell within a single brain network defined by connectivity to the right fusiform face area. Less consistent connectivity was found to other face-selective regions. Surprisingly, all 44 lesion locations were also functionally connected, through negative correlation, with regions in the left frontal cortex. This connectivity pattern was highly reproducible and specific to lesions causing prosopagnosia. Positive connectivity to the right fusiform face area and negative connectivity to left frontal regions were independent predictors of prosopagnosia and predicted subclinical facial agnosia in an independent lesion cohort. We conclude that lesions causing prosopagnosia localize to a single functionally connected brain network defined by connectivity to the right fusiform face area and to left frontal regions. Implications of these findings for models of facial recognition deficits are discussed.

SUBMITTER: Cohen AL

PROVIDER: S-EPMC6906597 | biostudies-literature | 2019 Dec

REPOSITORIES: biostudies-literature

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Looking beyond the face area: lesion network mapping of prosopagnosia.

Cohen Alexander L AL Soussand Louis L Corrow Sherryse L SL Martinaud Olivier O Barton Jason J S JJS Fox Michael D MD

Brain : a journal of neurology 20191201 12

Damage to the right fusiform face area can disrupt the ability to recognize faces, a classic example of how damage to a specialized brain region can disrupt a specialized brain function. However, similar symptoms can arise from damage to other brain regions, and face recognition is now thought to depend on a distributed brain network. The extent of this network and which regions are critical for facial recognition remains unclear. Here, we derive this network empirically based on lesion location ...[more]

PMID: 31740940

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Project description:Rationale: Face expertise is a pivotal social skill. Developmental prosopagnosia (DP), i.e., the inability to recognize faces without a history of brain damage, affects about 2% of the general population, and is a renowned model system of the face-processing network. Within this network, the right Fusiform Face Area (FFA), is particularly involved in face identity processing and may therefore be a key element in DP. Neural representations within the FFA have been examined with Representational Similarity Analysis (RSA), a data-analytical framework in which multi-unit measures of brain activity are assessed with correlation analysis. Objectives: Our study intended to scrutinize modifications of FFA-activation during face encoding and maintenance based on RSA. Methods: Thirteen participants with DP (23-70 years) and 12 healthy control subjects (19-62 years) participated in a functional MRI study, including morphological MRI, a functional FFA-localizer and a modified Sternberg paradigm probing face memory encoding and maintenance. Memory maintenance of one, two, or four faces represented low, medium, and high memory load. We examined conventional activation differences in response to working memory load and applied RSA to compute individual correlation-matrices on the voxel level. Group correlation-matrices were compared via Donsker's random walk analysis. Results: On the functional level, increased memory load entailed both a higher absolute FFA-activation level and a higher degree of correlation between activated voxels. Both aspects were deficient in DP. Interestingly, control participants showed a homogeneous degree of correlation for successful trials during the experiment. In DP-participants, correlation levels between FFA-voxels were significantly lower and were less sustained during the experiment. In behavioral terms, DP-participants performed poorer and had longer reaction times in relation to DP-severity. Furthermore, correlation levels were negatively correlated with reaction times for the most demanding high load condition. Conclusion: We suggest that participants with DP fail to generate robust and maintained neural representations in the FFA during face encoding and maintenance, in line with poorer task performance and prolonged reaction times. In DP, alterations of neural coding in the FFA might therefore explain curtailing in working memory and contribute to impaired long-term memory and mental imagery.

Project description:Developmental prosopagnosia is a disorder characterized by profound and lifelong difficulties with face recognition in the absence of sensory or intellectual deficits or known brain injury. While there has been a surge in research on developmental prosopagnosia over the last decade and a half, the cognitive mechanisms behind the disorder and its neural underpinnings remain elusive. Most recently it has been proposed that developmental prosopagnosia may be a manifestation of widespread disturbance in neural migration which affects both face responsive brain regions as well as other category-sensitive visual areas. We present a combined behavioural and functional MRI study of face, object and word processing in a group of developmental prosopagnosics (N = 15). We show that developmental prosopagnosia is associated with reduced activation of core ventral face areas during perception of faces. The reductions were bilateral but tended to be more pronounced in the left hemisphere. As the first study to address category selectivity for word processing in developmental prosopagnosia, we do not, however, find evidence for reduced activation of the visual word form area during perception of orthographic material. We also find no evidence for reduced activation of the lateral occipital complex during perception of objects. These imaging findings correspond well with the behavioural performance of the developmental prosopagnosics, who show severe impairment for faces but normal reading and recognition of line drawings. Our findings suggest that a general deficit in neural migration across ventral occipito-temporal cortex is not a viable explanation for developmental prosopagnosia. The finding of left hemisphere involvement in our group of developmental prosopagnosics was at first surprising. However, a closer look at existing studies shows similar, but hitherto undiscussed, findings. These left hemisphere abnormalities seen in developmental prosopagnosia contrasts with lesion and imaging studies suggesting primarily right hemisphere involvement in acquired prosopagnosia, and this may reflect that the left hemisphere is important for the development of a normal face recognition network.

Dataset Information

Looking beyond the face area: lesion network mapping of prosopagnosia.

Publications

Looking beyond the face area: lesion network mapping of prosopagnosia.

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