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

Journal name:
Nature Neuroscience
Volume:
13,
Pages:
1421–1427
Year published:
DOI:
doi:10.1038/nn.2653
Received
Accepted
Published online

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.

At a glance

Figures

  1. Performance of hearing and deaf cats on seven visual psychophysical tasks.
    Figure 1: Performance of hearing and deaf cats on seven visual psychophysical tasks.

    (a) Polar plot of the visual localization responses of hearing cats (light gray bars) and the superior performance of deaf cats (dark gray bars). The two concentric semicircles represent 50% and 100% correct response levels and the length of each colored line corresponds to the percentage of correct responses at each location tested. For both the hearing and deaf cats, data represent mean performance for 200 stimulus presentations at each peripheral target location and 400 stimulus presentations for the central target. (b) Histograms of combined data from left and right hemifields showing mean ± s.e.m. performance for the hearing (light gray) and deaf (dark gray) cats at each of the tested positions in the visual localization task. For both hearing and deaf cats, data represent mean performance for 400 stimulus presentations at each peripheral target location and 800 stimulus presentations for the central target (0°). (cg) Mean threshold ± s.e.m. for the hearing and deaf cats on the movement detection (c), grating acuity (d), Vernier acuity (e), orientation (f) and direction of motion (g) discrimination tasks. (h) Performance of the hearing and deaf cats on the velocity discrimination task. Data are presented as Weber fractions for six different stimulus velocities. *P < 0.01 between the hearing and deaf conditions. Sample stimuli are shown for each task.

  2. Cortical areas deactivated in deaf auditory cortex.
    Figure 2: Cortical areas deactivated in deaf auditory cortex.

    (a) Schematic illustration of the left hemisphere of the cat cerebrum showing all of the auditory areas (lateral view). The areas that we examined are highlighted in gray. A, anterior; A2, second auditory cortex; aes, anterior ectosylvian; D, dorsal; dPE, dorsal posterior ectosylvian area; FAES, auditory field of the anterior ectosylvian sulcus; IN, insular region; iPE, intermediate posterior ectosylvian area; P, posterior; pes, posterior ectosylvian; ss, suprasylvian; T, temporal region; V, ventral; VAF, ventral auditory field; VPAF, ventral posterior auditory field; vPE, ventral posterior ectosylvian area. The areal borders shown in this figure are based on a compilation of electrophysiological mapping and cytoarchitectonic studies. (b) Cooling loops in contact with areas AAF, DZ, A1 and PAF of the left hemisphere of a congenitally deaf cat at the time of implantation. Left is anterior. The areal borders presented in this figure are based on the post-mortem analysis of SMI-32 processed tissue from the brain shown here.

  3. Visual localization task data from deaf cats during bilateral reversible deactivation of PAF, DZ, A1 and AAF.
    Figure 3: Visual localization task data from deaf cats during bilateral reversible deactivation of PAF, DZ, A1 and AAF.

    (a) Polar plot of the visual localization responses of deaf cats while cortex was warm (dark gray) and active and during simultaneous cooling deactivation of PAF, DZ, A1, and AAF (black). (bf) Histogram of combined data from the left and right hemifields showing mean ± s.e.m. performance for deaf cats while cortex was warm (dark gray) and active and while it was cooled (black) and deactivated. Asterisks indicate a significant difference (P < 0.01) between the warm and cool conditions. (b) Data from the simultaneous deactivation of PAF, DZ, A1 and AAF. (cf) Data from individual area deactivations. (g) Visual localization data comparing performance at each position for hearing cats (light gray), deaf cats while PAF was warm (dark gray), and deaf cats while PAF was cooled (black). *P < 0.01 from the hearing and deaf PAF cool conditions.

  4. Motion detection thresholds for the deaf cats before and after cooling deactivation and during bilateral reversible deactivation.
    Figure 4: Motion detection thresholds for the deaf cats before and after cooling deactivation and during bilateral reversible deactivation.

    (ae) Histograms showing mean ± s.e.m. motion detection thresholds for deaf cats while cortex was warm (dark gray) and active and while it was cooled (black) and deactivated. *P < 0.01 between the warm and cool conditions. Motion detection thresholds from deaf cats during bilateral reversible deactivation of PAF, DZ, A1 and AAF are shown in a. Data from individual area deactivations are shown in be. (f) Motion detection thresholds to compare performance of hearing cats (light gray), deaf cats while DZ was warm (dark gray) and deaf cats while DZ was cooled (black). *P < 0.01 from the hearing and deaf DZ cool conditions.

  5. Performance of hearing cats on seven visual psychophysical tasks during simultaneous bilateral deactivation of PAF, DZ, A1 and AAF.
    Figure 5: Performance of hearing cats on seven visual psychophysical tasks during simultaneous bilateral deactivation of PAF, DZ, A1 and AAF.

    (a) Polar plot of the visual localization responses of the hearing cats (light gray bars) and during bilateral deactivation of all four cortical areas (black bars). The two concentric semicircles represent 50% and 100% correct response levels and the length of each bold line corresponds to the percentage of correct responses at each location tested. (b) Histograms of combined data from the left and right hemifields showing mean ± s.e.m. performance for the hearing cats when cortex was warm and active (light gray) and when all four areas were bilateraly cooled and deactivated (black). (cg) Mean threshold ± s.e.m. on the movement detection (c), grating acuity (d), Vernier acuity (e), orientation (f) and direction of motion (g) discrimination tasks for the hearing cats when cortex was warm and active (light gray) and when all four areas were bilateraly cooled and deactivated (black). Sample stimuli are shown for each task. (h) Performance on the velocity discrimination task. Data are presented as Weber fractions for six different stimulus velocities.

  6. Thermal cortical maps constructed by generating Voronoi tessellations from 335 temperature recording sites during deactivation of each individual cooling loop.
    Figure 6: Thermal cortical maps constructed by generating Voronoi tessellations21 from 335 temperature recording sites during deactivation of each individual cooling loop.

    Each image is a dorsolateral view of dorsal auditory cortex from the same brain pictured in Figure 2b. A color-coded temperature scale is provided on the right. (a) Line drawing showing the locations of the four cooling loops (wide black lines) on the cortical surface and the positions of the 335 temperature recording sites. At each site temperature was recorded 500 μm below the pial surface. (b) Cortical temperatures before cooling. (cf) Thermal profiles during cooling of each individual cryoloop to 3 °C. Sulci are indicated by thick black lines.

  7. Summary diagram illustrating the double-dissociation of visual functions in auditory cortex of the deaf cat.
    Figure 7: Summary diagram illustrating the double-dissociation of visual functions in auditory cortex of the deaf cat.

    Bilateral deactivation of PAF, but not DZ, resulted in the loss of enhanced visual localization in the far periphery. On the other hand, bilateral deactivation of DZ, but not PAF, resulted in higher movement detection thresholds. The lower panel shows a lateral view of the cat cerebrum highlighting the locations of PAF and DZ.

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Author information

Affiliations

  1. Centre for Brain and Mind, Department of Physiology and Pharmacology, Department of Psychology, University of Western Ontario, London, Ontario, Canada.

    • Stephen G Lomber
  2. Department of Anatomy and Neurobiology, School of Medicine, Virginia Commonwealth University, Richmond, Virginia, USA.

    • M Alex Meredith
  3. Department of Experimental Otology, Institute of Audioneurotechnology, Medical University Hannover, Hannover, Germany.

    • Andrej Kral

Contributions

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.

Competing financial interests

The authors declare no competing financial interests.

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