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Cross-modal plasticity in specific auditory cortices underlies visual compensations in the deaf

Abstract

When the brain is deprived of input from one sensory modality, it often compensates with supranormal performance in one or more of the intact sensory systems. In the absence of acoustic input, it has been proposed that cross-modal reorganization of deaf auditory cortex may provide the neural substrate mediating compensatory visual function. We tested this hypothesis using a battery of visual psychophysical tasks and found that congenitally deaf cats, compared with hearing cats, have superior localization in the peripheral field and lower visual movement detection thresholds. In the deaf cats, reversible deactivation of posterior auditory cortex selectively eliminated superior visual localization abilities, whereas deactivation of the dorsal auditory cortex eliminated superior visual motion detection. Our results indicate that enhanced visual performance in the deaf is caused by cross-modal reorganization of deaf auditory cortex and it is possible to localize individual visual functions in discrete portions of reorganized auditory cortex.

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Figure 1: Performance of hearing and deaf cats on seven visual psychophysical tasks.
Figure 2: Cortical areas deactivated in deaf auditory cortex.
Figure 3: Visual localization task data from deaf cats during bilateral reversible deactivation of PAF, DZ, A1 and AAF.
Figure 4: Motion detection thresholds for the deaf cats before and after cooling deactivation and during bilateral reversible deactivation.
Figure 5: Performance of hearing cats on seven visual psychophysical tasks during simultaneous bilateral deactivation of PAF, DZ, A1 and AAF.
Figure 6: Thermal cortical maps constructed by generating Voronoi tessellations21 from 335 temperature recording sites during deactivation of each individual cooling loop.
Figure 7: Summary diagram illustrating the double-dissociation of visual functions in auditory cortex of the deaf cat.

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Acknowledgements

We thank B.D. Corneil, M.A. Goodale, W.A. Roberts, D.F. Sherry, B. Timney and J. Snow for helpful discussions and comments on the project and manuscript. We thank A.J. McMillan and A. Carrasco for preparing all of the figures and for help with the preparation of the manuscript. We also thank A.J. McMillan for assistance with the fabrication of the cooling loops, surgical implantations and care of the animals. J.G. Mellott graciously assisted with the histological processing of the brains. We gratefully acknowledge the support of the Canadian Institutes of Health Research, Natural Sciences and Engineering Research Council of Canada, Deutsche Forschungsgemeinschaft and the US National Institutes of Health.

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S.G.L. and A.K. conceived and designed the project. A.K. bred and provided the cats. All psychophysical work was performed or supervised by S.G.L. M.A.M. provided assistance with data analysis and interpretation. The manuscript was written and edited by all of the authors.

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Correspondence to Stephen G Lomber.

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The authors declare no competing financial interests.

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Lomber, S., Meredith, M. & Kral, A. Cross-modal plasticity in specific auditory cortices underlies visual compensations in the deaf. Nat Neurosci 13, 1421–1427 (2010). https://doi.org/10.1038/nn.2653

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