Dataset Information

Functional selectivity for face processing in the temporal voice area of early deaf individuals.

ABSTRACT: Brain systems supporting face and voice processing both contribute to the extraction of important information for social interaction (e.g., person identity). How does the brain reorganize when one of these channels is absent? Here, we explore this question by combining behavioral and multimodal neuroimaging measures (magneto-encephalography and functional imaging) in a group of early deaf humans. We show enhanced selective neural response for faces and for individual face coding in a specific region of the auditory cortex that is typically specialized for voice perception in hearing individuals. In this region, selectivity to face signals emerges early in the visual processing hierarchy, shortly after typical face-selective responses in the ventral visual pathway. Functional and effective connectivity analyses suggest reorganization in long-range connections from early visual areas to the face-selective temporal area in individuals with early and profound deafness. Altogether, these observations demonstrate that regions that typically specialize for voice processing in the hearing brain preferentially reorganize for face processing in born-deaf people. Our results support the idea that cross-modal plasticity in the case of early sensory deprivation relates to the original functional specialization of the reorganized brain regions.

SUBMITTER: Benetti S

PROVIDER: S-EPMC5547585 | biostudies-literature | 2017 Aug

REPOSITORIES: biostudies-literature

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Functional selectivity for face processing in the temporal voice area of early deaf individuals.

Benetti Stefania S van Ackeren Markus J MJ Rabini Giuseppe G Zonca Joshua J Foa Valentina V Baruffaldi Francesca F Rezk Mohamed M Pavani Francesco F Rossion Bruno B Collignon Olivier O

Proceedings of the National Academy of Sciences of the United States of America 20170626 31

Brain systems supporting face and voice processing both contribute to the extraction of important information for social interaction (e.g., person identity). How does the brain reorganize when one of these channels is absent? Here, we explore this question by combining behavioral and multimodal neuroimaging measures (magneto-encephalography and functional imaging) in a group of early deaf humans. We show enhanced selective neural response for faces and for individual face coding in a specific re ...[more]

PMID: 28652333

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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:A central question in affective science and one that is relevant for its clinical applications is how emotions provided by different stimuli are experienced and represented in the brain. Following the traditional view emotional signals are recognized with the help of emotion concepts that are typically used in descriptions of mental states and emotional experiences, irrespective of the sensory modality. This perspective motivated the search for abstract representations of emotions in the brain, shared across variations in stimulus type (face, body, voice) and sensory origin (visual, auditory). On the other hand, emotion signals like for example an aggressive gesture, trigger rapid automatic behavioral responses and this may take place before or independently of full abstract representation of the emotion. This pleads in favor specific emotion signals that may trigger rapid adaptative behavior only by mobilizing modality and stimulus specific brain representations without relying on higher order abstract emotion categories. To test this hypothesis, we presented participants with naturalistic dynamic emotion expressions of the face, the whole body, or the voice in a functional magnetic resonance (fMRI) study. To focus on automatic emotion processing and sidestep explicit concept-based emotion recognition, participants performed an unrelated target detection task presented in a different sensory modality than the stimulus. By using multivariate analyses to assess neural activity patterns in response to the different stimulus types, we reveal a stimulus category and modality specific brain organization of affective signals. Our findings are consistent with the notion that under ecological conditions emotion expressions of the face, body and voice may have different functional roles in triggering rapid adaptive behavior, even if when viewed from an abstract conceptual vantage point, they may all exemplify the same emotion. This has implications for a neuroethologically grounded emotion research program that should start from detailed behavioral observations of how face, body, and voice expressions function in naturalistic contexts.

Dataset Information

Functional selectivity for face processing in the temporal voice area of early deaf individuals.

Publications

Functional selectivity for face processing in the temporal voice area of early deaf individuals.

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