Dataset Information

Retinotopic-like maps of spatial sound in primary 'visual' cortex of blind human echolocators.

ABSTRACT: The functional specializations of cortical sensory areas were traditionally viewed as being tied to specific modalities. A radically different emerging view is that the brain is organized by task rather than sensory modality, but it has not yet been shown that this applies to primary sensory cortices. Here, we report such evidence by showing that primary 'visual' cortex can be adapted to map spatial locations of sound in blind humans who regularly perceive space through sound echoes. Specifically, we objectively quantify the similarity between measured stimulus maps for sound eccentricity and predicted stimulus maps for visual eccentricity in primary 'visual' cortex (using a probabilistic atlas based on cortical anatomy) to find that stimulus maps for sound in expert echolocators are directly comparable to those for vision in sighted people. Furthermore, the degree of this similarity is positively related with echolocation ability. We also rule out explanations based on top-down modulation of brain activity-e.g. through imagery. This result is clear evidence that task-specific organization can extend even to primary sensory cortices, and in this way is pivotal in our reinterpretation of the functional organization of the human brain.

SUBMITTER: Norman LJ

PROVIDER: S-EPMC6790759 | biostudies-literature | 2019 Oct

REPOSITORIES: biostudies-literature

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Publications

Retinotopic-like maps of spatial sound in primary 'visual' cortex of blind human echolocators.

Norman Liam J LJ Thaler Lore L

Proceedings. Biological sciences 20191002 1912

The functional specializations of cortical sensory areas were traditionally viewed as being tied to specific modalities. A radically different emerging view is that the brain is organized by task rather than sensory modality, but it has not yet been shown that this applies to primary sensory cortices. Here, we report such evidence by showing that primary 'visual' cortex can be adapted to map spatial locations of sound in blind humans who regularly perceive space through sound echoes. Specificall ...[more]

PMID: 31575359

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Project description:Is visual input during critical periods of development crucial for the emergence of the fundamental topographical mapping of the visual cortex? And would this structure be retained throughout life-long blindness or would it fade as a result of plastic, use-based reorganization? We used functional connectivity magnetic resonance imaging based on intrinsic blood oxygen level-dependent fluctuations to investigate whether significant traces of topographical mapping of the visual scene in the form of retinotopic organization, could be found in congenitally blind adults. A group of 11 fully and congenitally blind subjects and 18 sighted controls were studied. The blind demonstrated an intact functional connectivity network structural organization of the three main retinotopic mapping axes: eccentricity (centre-periphery), laterality (left-right), and elevation (upper-lower) throughout the retinotopic cortex extending to high-level ventral and dorsal streams, including characteristic eccentricity biases in face- and house-selective areas. Functional connectivity-based topographic organization in the visual cortex was indistinguishable from the normally sighted retinotopic functional connectivity structure as indicated by clustering analysis, and was found even in participants who did not have a typical retinal development in utero (microphthalmics). While the internal structural organization of the visual cortex was strikingly similar, the blind exhibited profound differences in functional connectivity to other (non-visual) brain regions as compared to the sighted, which were specific to portions of V1. Central V1 was more connected to language areas but peripheral V1 to spatial attention and control networks. These findings suggest that current accounts of critical periods and experience-dependent development should be revisited even for primary sensory areas, in that the connectivity basis for visual cortex large-scale topographical organization can develop without any visual experience and be retained through life-long experience-dependent plasticity. Furthermore, retinotopic divisions of labour, such as that between the visual cortex regions normally representing the fovea and periphery, also form the basis for topographically-unique plastic changes in the blind.

Project description:The localization of visual areas in the human cortex is typically based on mapping the retinotopic organization with functional magnetic resonance imaging (fMRI). The most common approach is to encode the response phase for a slowly moving visual stimulus and to present the result on an individual's reconstructed cortical surface. The main aims of this study were to develop complementary general linear model (GLM)-based retinotopic mapping methods and to characterize the inter-individual variability of the visual area positions on the cortical surface. We studied 15 subjects with two methods: a 24-region multifocal checkerboard stimulus and a blocked presentation of object stimuli at different visual field locations. The retinotopic maps were based on weighted averaging of the GLM parameter estimates for the stimulus regions. In addition to localizing visual areas, both methods could be used to localize multiple retinotopic regions-of-interest. The two methods yielded consistent retinotopic maps in the visual areas V1, V2, V3, hV4, and V3AB. In the higher-level areas IPS0, VO1, LO1, LO2, TO1, and TO2, retinotopy could only be mapped with the blocked stimulus presentation. The gradual widening of spatial tuning and an increase in the responses to stimuli in the ipsilateral visual field along the hierarchy of visual areas likely reflected the increase in the average receptive field size. Finally, after registration to Freesurfer's surface-based atlas of the human cerebral cortex, we calculated the mean and variability of the visual area positions in the spherical surface-based coordinate system and generated probability maps of the visual areas on the average cortical surface. The inter-individual variability in the area locations decreased when the midpoints were calculated along the spherical cortical surface compared with volumetric coordinates. These results can facilitate both analysis of individual functional anatomy and comparisons of visual cortex topology across studies.

Dataset Information

Retinotopic-like maps of spatial sound in primary 'visual' cortex of blind human echolocators.

Publications

Retinotopic-like maps of spatial sound in primary 'visual' cortex of blind human echolocators.

Similar Datasets

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