Structural and Functional Network-Level Reorganization in the Coding of Auditory Motion Directions and Sound Source Locations in the Absence of Vision

Epub 2022 May 2hMT+/V5 is a region in the middle occipitotemporal cortex that responds preferentially to visual motion in sighted people. In cases 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 cross-modal 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-weighted 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 direction and sound position 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-weighted 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 congenital blindness alters the response properties of occipitotemporal networks supporting spatial hearing in the sighted.SIGNIFICANCE STATEMENT Spatial 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 direction and sound position information was higher in hMT+/V5 and lower in human planum temporale 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 cross-modal responses between connected areas that share the same computational goals.The project was funded in part by a European Research Council starting grant MADVIS (Project 337573) awarded to O.C., the Belgian Excellence of Science (EOS) program (Project 30991544) awarded to O.C., a Flagship ERA-NET grant SoundSight (FRS-FNRS PINT-MULTI R.8008.19) awarded to O.C., and by the European Union Horizon 2020 research and innovation program under the Marie Skłodowska-Curie Grant Agreement No. 701250 awarded to V.O. Computational resources have been provided by the supercomputing facilities of the Université catholique de Louvain (CISM/UCL) and the Consortium des Équipements de Calcul Intensif en Fédération Wallonie Bruxelles (CÉCI) funded by the Fond de la Recherche Scientifique de Belgique (F.R.S.-FNRS) under convention 2.5020.11 and by the Walloon Region. A.G.-A. is supported by the Wallonie Bruxelles International Excellence Fellowship and the FSR Incoming PostDoc Fellowship by Université Catholique de Louvain. O.C. is a research associate, C.B. is postdoctoral researcher, and M.R. is a research fellow at the Fond National de la Recherche Scientifique de Belgique (FRS-FNRS)

Decoding Auditory Motion Direction And Location In hMT+/V5 And Planum Temporale Of Sighted And Blind Individuals

The research presented in this thesis addresses the neural mechanisms of auditory motion processing and the impact of early visual deprivation on motion-responsive brain regions, by using functional magnetic resonance imaging. Visual motion, and in particular direction selectivity, is one of the most investigated aspects of mammalian brain function. In comparison, little is known about how the brain processes moving sounds. More precisely, we have a poor understanding of how the human brain codes for the direction of auditory motion and how this process differs from auditory sound-source localization. In the first study, we characterized the neural representations of auditory motion within the Planum Temporale (PT), and how motion direction and sound source location are represented within this auditory motion responsive region. We further explore if the distribution of orientation responsive neurons (topographic representations) within the PT shares similar organizational features to what is observed within the visual motion area MT/V5. The spatial representations would, therefore, be more systematic for axis of motion/space, rather than for within-axis direction/location. Despite the shared representations between auditory spatial conditions, we show that motion directions and sound source locations generate highly distinct patterns of activity. The second study focused on the impact of early visual deprivation on auditory motion processing. Studying visual deprivation-induced plasticity sheds light on how sensory experience alters the functional organization of motion processing areas, and exploits intrinsic computational bias implemented in cortical regions. In addition to enhanced auditory motion responses within the hMT+/V5, we demonstrate that this region maintains direction selectivity tuning, but enhances its modality preference to auditory input in case of early blindness. Crucially, the enhanced computational role of hMT+/V5 is followed by a reduced role of PT for processing both motion direction and sound source location. These results suggest that early blindness triggers interplay between visual and auditory motion areas, and their computational roles could be re-distributed for effective processing of auditory spatial tasks. Overall, our findings suggest (1) auditory motion-specific processing in the typically developed auditory cortex, and (2) interplay between cross- and intra-modal plasticity to compute auditory motion and space in early blind individuals

Stimuli

Experimental Stimuli presented during auditory localization tas

Spatial Hearing in Congenitally Blind People

Behavioral data and script