Shared connectome and organization in the human cortex irrespective of sensory experience
Poster No:
2543
Submission Type:
Abstract Submission
Authors:
Guo Jiahui1, Francesca Setti2, Ma Feilong1, Davide Bottari2, M. Ida Gobbini3, Pietro Pietrini2, Emiliano Ricciardi2, James Haxby1
Institutions:
1Dartmouth College, Hanover, NH, 2IMT School for Advanced Studies Lucca, Lucca, Italy, 3University of Bologna, Bologna, Italy
First Author:
Co-Author(s):
Introduction:
Human high-level visual cortex selectively responds to different visual categories (e.g., faces, places). Category-selective topographies exist in the ventral visual cortex, superior temporal sulcus, and extend to the frontal regions. The general layout of these topographies is similar across individuals, but idiosyncrasies exist in their precise conformation and location. Category-specific activations in response to tactile and auditory stimuli in both typically developed and sensory-deprived individuals (1–3) suggest a supramodal functional organization in these ventro-temporal and occipital areas. It has not been possible previously, however, to map individual-specific visual category-selective topographies in congenitally-blind participants.
Methods:
Congenitally blind (BD, N = 11, mean age 46 years, 3 females) and deaf participants (DF, N = 9, mean age 24 years, 5 females) were presented with audio-only and video-only versions of the movie 101 Dalmatians (4), respectively. Three control groups either watched and/or listened to the audiovisual (AV, N = 10, mean age 35 years, 8 females), the audio-only (AD, N = 10, mean age 39 years, 7 females), and the video-only (VD, N = 10, mean age 37 years, 5 females) versions of the movie. It has been established that individualized category-selective topographies can be estimated with high fidelity across movies using connectivity hyperalignment (CHA) (5). Another fMRI data (6) from an independent group of participants who watched the movie, The Grand Budapest Hotel, and performed a visual category functional localizer task (N = 20, mean age 27 years, 10 females), was included to predict the individualized topographies. The predictions were validated with another independent dataset (N = 24, mean age 26 years, 15 females), in which participants watched the movie Monkey Kingdom and also completed a similar functional localizer task.
Results:
With CHA, category-selective topographies were successfully predicted in both congenitally blind and deaf participants by projecting the localizer data into their individual cortical space using transformation matrices derived from functional connectivity calculated from the movie data (Figure 1). The predicted topographies were distinctive for individuals in all groups (BD, DF, AV, AD, & VD). Notably, individual variability of category-selective topographies in the ventral visual pathway in congenitally blind participants was highly comparable to that of sighted participants (Figure 2). Functional connectomes were notably similar across the entire cortex, regardless of the modality of sensory input. When visual or auditory information was shared between groups, participants' connectomes showed higher similarity in the corresponding visual and auditory cortices. Connectomes in the bilateral superior temporal cortices, which are involved in multisensory information processing, were analogous across all groups.
In the validation analysis with the Monkey Kingdom dataset, when we randomized the labels for the movie-localizer pairs across participants, prediction accuracy significantly dropped from near-noise-ceiling levels to baseline, demonstrating that our predictions using the correct labels are precise and specific to each individual.
In the validation analysis with the Monkey Kingdom dataset, when we randomized the labels for the movie-localizer pairs across participants, prediction accuracy significantly dropped from near-noise-ceiling levels to baseline, demonstrating that our predictions using the correct labels are precise and specific to each individual.
Conclusions:
With real-world, naturalistic stimuli, this study demonstrates that the functional connectome maintains a similar organization across input from different sensory modalities and with different histories of congenital sensory deprivation. The structure of the part of the connectome that is associated with visual category-selective topographies is conserved even in adults with no history of visual experience. These results show that development of the functional organization of the human high-level visual cortex can occur independently of visual experience and introduce a method for identifying category-selective areas in adults who have never seen those categories.
Modeling and Analysis Methods:
Multivariate Approaches 2
Perception, Attention and Motor Behavior:
Perception: Visual 1
Keywords:
Other - Naturalistic movie, Hyperalignment, Development, Sensory deprivation, Connectivity
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2. S. L. Fairhall. (2017), 'Plastic reorganization of neural systems for perception of others in the congenitally blind', NeuroImage 158, 126–135
3. S. Mattioni. (2020), 'Categorical representation from sound and sight in the ventral occipito-temporal cortex of sighted and blind'. eLife 9, e50732.
4. F. Setti. (2023), 'A modality-independent proto-organization of human multisensory areas', Nat. Hum. Behav., 1–14
5. G. Jiahui. (2023), 'Cross-movie prediction of individualized functional topography'. eLife 12, e86037
6. M. Visconti di Oleggio Castello. (2020), 'An fMRI dataset in response to “The Grand Budapest Hotel”, a socially-rich, naturalistic movie', Sci. Data 7, 383