Functional connectivity of visual cortex in the blind follows retinotopic organization principles

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 co...

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Published inBrain (London, England : 1878) Vol. 138; no. 6; pp. 1679 - 1695
Main Authors Striem-Amit, Ella, Ovadia-Caro, Smadar, Caramazza, Alfonso, Margulies, Daniel S., Villringer, Arno, Amedi, Amir
Format Journal Article
LanguageEnglish
Published England Oxford University Press 01.06.2015
Subjects
Online AccessGet full text
ISSN0006-8950
1460-2156
DOI10.1093/brain/awv083

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Abstract 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.
AbstractList Although early visual experience is essential for the proper development of visual cortex, Striem-Amit et al. show that the underlying connectivity structure of retinotopic mapping is retained even in congenitally blind individuals. This basic organisational principle emerges independently of visual input and persists despite lifelong experience-dependent plasticity. Although early visual experience is essential for the proper development of visual cortex, Striem-Amit et al. show that the underlying connectivity structure of retinotopic mapping is retained even in congenitally blind individuals. This basic organisational principle emerges independently of visual input and persists despite lifelong experience-dependent plasticity. 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.
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.
Author Ovadia-Caro, Smadar
Striem-Amit, Ella
Margulies, Daniel S.
Villringer, Arno
Amedi, Amir
Caramazza, Alfonso
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/25869851$$D View this record in MEDLINE/PubMed
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Issue 6
Keywords vision
plasticity
development
blindness
Language English
License The Author (2015). Published by Oxford University Press on behalf of the Guarantors of Brain.
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These authors contributed equally to this work.
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Snippet Is visual input during critical periods of development crucial for the emergence of the fundamental topographical mapping of the visual cortex? And would this...
Although early visual experience is essential for the proper development of visual cortex, Striem-Amit et al. show that the underlying connectivity structure...
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StartPage 1679
SubjectTerms Adult
Blindness - physiopathology
Case-Control Studies
Functional Neuroimaging
Humans
Magnetic Resonance Imaging
Male
Middle Aged
Original
Retina - physiology
Visual Cortex - physiology
Visual Pathways - physiology
Young Adult
Title Functional connectivity of visual cortex in the blind follows retinotopic organization principles
URI https://www.ncbi.nlm.nih.gov/pubmed/25869851
https://www.proquest.com/docview/1683757289
https://pubmed.ncbi.nlm.nih.gov/PMC4614142
Volume 138
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