Structural and functional network-level reorganization in the coding of auditory motion directions and sound source locations in the absence of vision

Battal, C.; Gurtubay-Antolin, A.; Rezk, M.; Mattioni, S.; Bertonati, G.; Occelli, V.; Bottini, R.; Targher, S.; Maffei, C.; Jovicich, J.; Collignon, O.

doi:10.1101/2021.07.28.454106

bioRxiv · 10.1101/2021.07.28.454106

Structural and functional network-level reorganization in the coding of auditory motion directions and sound source locations in the absence of vision

Battal, C.·Gurtubay-Antolin, A.·Rezk, M.·Mattioni, S.·Bertonati, G.·Occelli, V.·Bottini, R.·Targher, S.·Maffei, C.·Jovicich, J.·Collignon, O.

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Abstract

hMT+/V5 is a region in the middle occipito-temporal cortex that responds preferentially to visual motion in sighted people. In case of early visual deprivation, hMT+/V5 enhances its response to moving sounds. Whether hMT+/V5 contains information about motion directions and whether the functional enhancement observed in the blind is motion specific, or also involves sound source location, remains unsolved. Moreover, the impact of this crossmodal reorganization of hMT+/V5 on the regions typically supporting auditory motion processing, like the human Planum Temporale (hPT), remains equivocal. We used a combined functional and diffusion MRI approach and individual in-ear recordings to study the impact of early blindness on the brain networks supporting spatial hearing, in male and female humans. Whole-brain univariate analysis revealed that the anterior portion of hMT+/V5 responded to moving sounds in sighted and blind people, while the posterior portion was selective to moving sounds only in blind participants. Multivariate decoding analysis revealed that the presence of motion directions and sound positions information was higher in hMT+/V5 and lower in hPT in the blind group. While both groups showed axis-of-motion organization in hMT+/V5 and hPT, this organization was reduced in the hPT of blind people. Diffusion MRI revealed that the strength of hMT+/V5 - hPT connectivity did not differ between groups, whereas the microstructure of the connections was altered by blindness. Our results suggest that the axis-of-motion organization of hMT+/V5 does not depend on visual experience, but that blindness alters the response properties of occipito-temporal networks supporting spatial hearing in the sighted. Significance StatementSpatial hearing helps living organisms navigate their environment. This is certainly even more true in people born blind. How does blindness affect the brain network supporting auditory motion and sound source location? Our results show that the presence of motion directions and sound positions information was higher in hMT+/V5 and lower in hPT in blind relative to sighted people; and that this functional reorganization is accompanied by microstructural (but not macrostructural) alterations in their connections. These findings suggest that blindness alters crossmodal responses between connected areas that share the same computational goals.

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Battal, C., Gurtubay-Antolin, A., Rezk, M., Mattioni, S., Bertonati, G., Occelli, V., Bottini, R., Targher, S., Maffei, C., Jovicich, J., Collignon, O.. 2021-07-28. Structural and functional network-level reorganization in the coding of auditory motion directions and sound source locations in the absence of vision. https://doi.org/10.1101/2021.07.28.454106

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