Literature DB >> 35501150

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

Ceren Battal1,2, Ane Gurtubay-Antolin3,4, Mohamed Rezk3,2, Stefania Mattioni3,2, Giorgia Bertonati2, Valeria Occelli2,5, Roberto Bottini2, Stefano Targher3, Chiara Maffei6, Jorge Jovicich2, Olivier Collignon1,2,7,8.   

Abstract

hMT+/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.
Copyright © 2022 the authors.

Entities:  

Keywords:  Planum Temporale; auditory space; blindness; crossmodal plasticity; hMT+/V5; tractography

Mesh:

Year:  2022        PMID: 35501150      PMCID: PMC9186796          DOI: 10.1523/JNEUROSCI.1554-21.2022

Source DB:  PubMed          Journal:  J Neurosci        ISSN: 0270-6474            Impact factor:   6.709


  94 in total

1.  Expansion of the tonotopic area in the auditory cortex of the blind.

Authors:  Thomas Elbert; Annette Sterr; Brigitte Rockstroh; Christo Pantev; Matthias M Müller; Edward Taub
Journal:  J Neurosci       Date:  2002-11-15       Impact factor: 6.167

2.  A direct demonstration of functional specialization in human visual cortex.

Authors:  S Zeki; J D Watson; C J Lueck; K J Friston; C Kennard; R S Frackowiak
Journal:  J Neurosci       Date:  1991-03       Impact factor: 6.167

3.  Reorganisation of the right occipito-parietal stream for auditory spatial processing in early blind humans. A transcranial magnetic stimulation study.

Authors:  O Collignon; M Davare; E Olivier; A G De Volder
Journal:  Brain Topogr       Date:  2009-02-06       Impact factor: 3.020

4.  Probabilistic fibre tracking: differentiation of connections from chance events.

Authors:  David M Morris; Karl V Embleton; Geoff J M Parker
Journal:  Neuroimage       Date:  2008-06-20       Impact factor: 6.556

5.  Functional selectivity in sensory-deprived cortices.

Authors:  Giulia Dormal; Olivier Collignon
Journal:  J Neurophysiol       Date:  2011-03-23       Impact factor: 2.714

6.  Functional specialization for auditory-spatial processing in the occipital cortex of congenitally blind humans.

Authors:  Olivier Collignon; Gilles Vandewalle; Patrice Voss; Geneviève Albouy; Geneviève Charbonneau; Maryse Lassonde; Franco Lepore
Journal:  Proc Natl Acad Sci U S A       Date:  2011-02-28       Impact factor: 11.205

7.  Statistical inference and multiple testing correction in classification-based multi-voxel pattern analysis (MVPA): random permutations and cluster size control.

Authors:  Johannes Stelzer; Yi Chen; Robert Turner
Journal:  Neuroimage       Date:  2012-10-04       Impact factor: 6.556

8.  Area V5 of the human brain: evidence from a combined study using positron emission tomography and magnetic resonance imaging.

Authors:  J D Watson; R Myers; R S Frackowiak; J V Hajnal; R P Woods; J C Mazziotta; S Shipp; S Zeki
Journal:  Cereb Cortex       Date:  1993 Mar-Apr       Impact factor: 5.357

9.  Polymodal motion processing in posterior parietal and premotor cortex: a human fMRI study strongly implies equivalencies between humans and monkeys.

Authors:  F Bremmer; A Schlack; N J Shah; O Zafiris; M Kubischik; K Hoffmann; K Zilles; G R Fink
Journal:  Neuron       Date:  2001-01       Impact factor: 17.173

10.  An afferent white matter pathway from the pulvinar to the amygdala facilitates fear recognition.

Authors:  Jessica McFadyen; Jason B Mattingley; Marta I Garrido
Journal:  Elife       Date:  2019-01-16       Impact factor: 8.140

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  2 in total

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

Authors:  Stefania Mattioni; Mohamed Rezk; Ceren Battal; Jyothirmayi Vadlamudi; Olivier Collignon
Journal:  Elife       Date:  2022-09-07       Impact factor: 8.713

2.  Rethinking the representation of sound.

Authors:  Łukasz Bola
Journal:  Elife       Date:  2022-09-07       Impact factor: 8.713

  2 in total

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