Categorical representation from sound and sight in the ventral occipito-temporal cortex of sighted and blind

Mattioni, Stefania; Rezk, Mohamed; Battal, Ceren; Bottini, Roberto; Mendoza, Karen E Cuculiza; Oosterhof, Nikolaas N.; Collignon, Olivier

doi:10.7554/elife.50732

Cited by 69 publications

(76 citation statements)

References 130 publications

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“…Our results suggest that the latter is not always true when quantitatively comparing VTC category representations from one individual to another between groups. Interestingly, the variability in the blind and also the variability in the sighted for auditory categorical representations in VTC are consistent with what was recently described as "qualitative nuances in the categorical organization of VOTC between modalities [vision and audition] and groups [sighted and blind]" (Mattioni et al, 2020). We build on these qualitative conclusions with our quantifications indicating that there are extensive individual differences of category information in VTC in the congenitally blind.…”

Section: Heterogeneity Of Distributed Category Representations In Vtcsupporting

confidence: 89%

Extensive individual differences of category information in ventral temporal cortex in the congenitally blind

Rosenke

Hurk

Margalit

et al. 2020

Preprint

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Human ventral temporal cortex (VTC) is a cortical expanse that performs different functions and computations, but is especially critical for visual categorization. Nevertheless, accumulating evidence shows that category-selective regions persist in VTC in the absence of visual experience -for example, in congenitally blind (CB) participants. Despite this evidence, a large body of previous work comparing functional representations in VTC between sighted and CB participants performed univariate analyses at the group level, which assume a homogeneous population -an assumption that has not been formally tested until the present study. Specifically, using fMRI in CB and sighted participants (male and female), we empirically show that at the group level, distributed category representations in VTC are more reliable in the sighted (when viewing visual stimuli) compared to the CB (when hearing auditorily-substituted visual stimuli). Despite these group differences, there is extensive heterogeneity in VTC category representations in the CB to the point that VTC category representations in a subset of CB participants (some who were born without eyes, but not all) are more similar to sighted individuals compared to other CB participants. Together, our findings support a novel idea that driving factors contributing to the formation of VTC category representations in the blind are subject-specific, which complements factors that may generalize across group members. More broadly, the present findings caution conclusions of homogeneity across subjects within a group when performing group neuroimaging analyses without explicitly quantifying individual differences.

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Section: Heterogeneity Of Distributed Category Representations In Vtcsupporting

confidence: 89%

Extensive individual differences of category information in ventral temporal cortex in the congenitally blind

Rosenke

Hurk

Margalit

et al. 2020

Preprint

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“…CC-BY-NC 4.0 International license available under a (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made The copyright holder for this preprint this version posted November 22, 2020. ; https://doi.org/10.1101/2020.11.22.393397 doi: bioRxiv preprint versus small artifacts (e.g., Mahon et al, 2009;Wolbers et al, 2011;He et al, 2013;Peelen et al, 2013;Bi et al, 2015;Mattioni et al, 2020). Since ontogenetic visual experience could not have contributed to the similar patterns of object-preferring effects in high-level visual areas in congenitally blind and sighted individuals, it invites the conclusion that the observed specialization predates such experience.…”

Section: What Drives This Object Organization?mentioning

confidence: 99%

The contribution of object size, manipulability, and stability on neural responses to inanimate objects

Magri

Konkle

Caramazza

2020

Preprint

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In human occipitotemporal cortex, brain responses to depicted inanimate objects have a large-scale organization by real-world object size. Critically, the size of objects in the world is systematically related to behaviorally-relevant properties: small objects are often grasped and manipulated (e.g., forks), while large objects tend to be less motor-relevant (e.g., tables), though this relationship does not always have to be true (e.g., picture frames and wheelbarrows). To determine how these two dimensions interact, we measured brain activity with functional magnetic resonance imaging while participants viewed a stimulus set of small and large objects with either low or high motor-relevance. The results revealed that the size organization was evident for objects with both low and high motor-relevance; further, a motor-relevance map was also evident across both large and small objects. Targeted contrasts revealed that typical combinations (small motor-relevant vs. large non-motor-relevant) yielded more robust topographies than the atypical covariance contrast (small non-motor-relevant vs. large motor-relevant). In subsequent exploratory analyses, a factor analysis revealed that the construct of motor-relevance was better explained by two underlying factors: one more related to manipulability, and the other to whether an object moves or is stable. The factor related to manipulability better explained responses in lateral small-object preferring regions, while the factor related to object stability (lack of movement) better explained responses in ventromedial large-object preferring regions. Taken together, these results reveal that the structure of neural responses to objects of different sizes further reflect behavior-relevant properties of manipulability and stability, and contribute to a deeper understanding of some of the factors that help the large-scale organization of object representation in high-level visual cortex.Highlights-Examined the relationship between real-world size and motor-relevant properties in the structure of responses to inanimate objects.-Large scale topography was more robust for contrast that followed natural covariance of small motor-relevant vs. large non-motor-relevant, over contrast that went against natural covariance.-Factor analysis revealed that manipulability and stability were, respectively, better explanatory predictors of responses in small- and large-object regions.

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“…A further important question that remains debated is whether and how the onset of blindness impacts on the reorganizations of the occipital regions and on their interplay with the coding of sounds implemented in temporal regions. We have recently suggested that crossmodal plasticity in early blind could be an extension of the intrinsic categorical organization of VOTC, that is partially independent from vision also in sighted (Mattioni et al, 2020; see also Amedi, Jacobson, Hendler, Malach, & Zohary, 2002; 2011 for similar suggestions). According to this view, one should assume that crossmodal plasticity would express similarly also when the onset of blindness occurs late in life.…”

Section: Introductionmentioning

confidence: 85%

“…Since this paper is submitted as a Research Advances format, it represents a substantial development that directly build upon a Research Article published previously by eLife (Mattioni et al, 2020). No extensive description of material and methods will appear when in directly overlaps with our previous publication.…”

Section: Methodsmentioning

confidence: 99%

“…Importantly, this mechanism of crossmodal plasticity (CMP) follows organizational principles known to be routed in the occipital cortex of sighted people (Amedi, Raz, Azulay, Malach, & Zohary, 2010;Dormal & Collignon, 2011;Ricciardi, Bonino, Pellegrini, & Pietrini, 2014;Striem-Amit, Dakwar, Reich, & Amedi, 2012). For instance, we have recently shown that the Ventral Occipito-Temporal Cortex (VOTC) reliably encodes sound categories in early blind, and to a lesser extent also in sighted people, using a representational structure and connectivity partially similar to the one found in vision (Mattioni et al, 2020). However, some important questions remain unsolved.…”

Section: Introductionmentioning

confidence: 99%

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Impact of blindness onset on the representation of sound categories in occipital and temporal cortices

Mattioni

Rezk

Battal

et al. 2020

Preprint

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Visual deprivation triggers enhanced dependence on auditory representation. It was suggested that (auditory) temporal regions sharpen their response to sounds in visually deprived people. In contrast with such view, we show that the coding of sound categories is enhanced in the occipital but, importantly, reduced in the temporal cortex of early and, to a lesser extent, of late blind people. Importantly, the representation of sound categories in occipital and temporal regions is characterized by a similar ‘human-centric’ structure in blind people, supporting the idea that these decreased intramodal and increased crossmodal representations are linked. We suggest that early, and to some extent late blindness, induces network-level reorganization of the neurobiology of sound categories by concomitantly increasing/decreasing the respective computational load of occipital/temporal regions.

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Categorical representation from sound and sight in the ventral occipito-temporal cortex of sighted and blind

Cited by 69 publications

References 130 publications

Extensive individual differences of category information in ventral temporal cortex in the congenitally blind

Extensive individual differences of category information in ventral temporal cortex in the congenitally blind

The contribution of object size, manipulability, and stability on neural responses to inanimate objects

Impact of blindness onset on the representation of sound categories in occipital and temporal cortices

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