Dataset Information

Experience Shapes the Development of Neural Substrates of Face Processing in Human Ventral Temporal Cortex.

ABSTRACT: In adult humans, the ventral temporal cortex (VTC) represents faces in a reproducible topology. However, it is unknown what role visual experience plays in the development of this topology. Using functional magnetic resonance imaging in children and adults, we found a sequential development, in which the topology of face-selective activations across the VTC was matured by age 7, but the spatial extent and degree of face selectivity continued to develop past age 7 into adulthood. Importantly, own- and other-age faces were differentially represented, both in the distributed multivoxel patterns across the VTC, and also in the magnitude of responses of face-selective regions. These results provide strong evidence that experience shapes cortical representations of faces during development from childhood to adulthood. Our findings have important implications for the role of experience and age in shaping the neural substrates of face processing in the human VTC.

SUBMITTER: Golarai G

PROVIDER: S-EPMC6161183 | biostudies-literature | 2017 Feb

REPOSITORIES: biostudies-literature

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Experience Shapes the Development of Neural Substrates of Face Processing in Human Ventral Temporal Cortex.

Golarai Golijeh G Liberman Alina A Grill-Spector Kalanit K

Cerebral cortex (New York, N.Y. : 1991) 20170201 2

In adult humans, the ventral temporal cortex (VTC) represents faces in a reproducible topology. However, it is unknown what role visual experience plays in the development of this topology. Using functional magnetic resonance imaging in children and adults, we found a sequential development, in which the topology of face-selective activations across the VTC was matured by age 7, but the spatial extent and degree of face selectivity continued to develop past age 7 into adulthood. Importantly, own ...[more]

PMID: 26683171

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Project description: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, like 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 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, like words and faces, are organized relative to one another. Here, invasive and non-invasive neuroimaging suggests 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 they play different roles in perception. These results illuminate extended, bilateral, and dynamic brain pathways that support face perception and reading.

Project description:Putting a name to a face is a highly common activity in our daily life that greatly enriches social interactions. Although this specific person-identity association becomes automatic with learning, it remains difficult and can easily be disrupted in normal circumstances or neurological conditions. To shed light on the neural basis of this important and yet poorly understood association between different input modalities in the human brain, we designed a crossmodal frequency-tagging paradigm coupled to brain activity recording via scalp and intracerebral electroencephalography. In Experiment 1, 12 participants were presented with variable pictures of faces and written names of a single famous identity at a 4-Hz frequency rate while performing an orthogonal task. Every 7 items, another famous identity appeared, either as a face or a name. Robust electrophysiological responses were found exactly at the frequency of identity change (i.e., 4 Hz / 7 = 0.571 Hz), suggesting a crossmodal neural response to person identity. In Experiment 2 with twenty participants, two control conditions with periodic changes of identity for faces or names only were added to estimate the contribution of unimodal neural activity to the putative crossmodal face-name responses. About 30% of the response occurring at the frequency of crossmodal identity change over the left occipito-temporal cortex could not be accounted for by the linear sum of unimodal responses. Finally, intracerebral recordings in the left ventral anterior temporal lobe (ATL) in 7 epileptic patients tested with this paradigm revealed a small number of "pure" crossmodal responses, i.e., with no response to changes of identity for faces or names only. Altogether, these observations provide evidence for integration of verbal and nonverbal person identity-specific information in the human brain, highlighting the contribution of the left ventral ATL in the automatic retrieval of face-name identity associations.

Dataset Information

Experience Shapes the Development of Neural Substrates of Face Processing in Human Ventral Temporal Cortex.

Publications

Experience Shapes the Development of Neural Substrates of Face Processing in Human Ventral Temporal Cortex.

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