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Cortical and thalamic connectivity to the second auditory cortex of the cat is resilient to the onset of deafness

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Abstract

It has been well established that following sensory loss, cortical areas that would normally be involved in perceiving stimuli in the absent modality are recruited to subserve the remaining senses. Despite this compensatory functional reorganization, there is little evidence to date for any substantial change in the patterns of anatomical connectivity between sensory cortices. However, while many auditory areas are contracted in the deaf, the second auditory cortex (A2) of the cat undergoes a volumetric expansion following hearing loss, suggesting this cortical area may demonstrate a region-specific pattern of structural reorganization. To address this hypothesis, and to complement existing literature on connectivity within auditory cortex, we injected a retrograde neuronal tracer across the breadth and cortical thickness of A2 to provide the first comprehensive quantification of projections from cortical and thalamic auditory and non-auditory regions to the second auditory cortex, and to determine how these patterns are affected by the onset of deafness. Neural projections arising from auditory, visual, somatomotor, and limbic cortices, as well as thalamic nuclei, were compared across normal hearing, early-deaf, and late-deaf animals. The results demonstrate that, despite previously identified changes in A2 volume, the pattern of projections into this cortical region are unaffected by the onset of hearing loss. These results fail to support the idea that crossmodal plasticity reflects changes in the pattern of projections between cortical regions and provides evidence that the pattern of connectivity that supports normal hearing is retained in the deaf brain.

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Modified from the findings of Wong et al. (2014)

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Abbreviations

AAF:

Anterior auditory field

AES:

Anterior ectosylvian sulcus

AEV:

Anterior ectosylvian visual area

ABR:

Auditory brainstem response

ALLS:

Anterolateral lateral suprasylvian area

AMLS:

Anteromedial lateral suprasylvian area

A1:

Primary auditory cortex

A2:

Second auditory cortex

BDA:

Biotinylated dextran amine

CGP:

Posterior cingulate area

CVA:

Cingulate visual area

dB:

Decibel

DLS:

Dorsal lateral suprasylvian area

dPE:

Dorsal division of the posterior ectosylvian gyrus

DZ:

Dorsal zone of auditory cortex

ED:

Early-deaf

EEG:

Electroencephalography

EPp:

Posterior aspect of the posterior ectosylvian gyrus

fAES:

Auditory field of the anterior ectosylvian sulcus

IN:

Insular auditory cortical area

iPE:

Intermediate division of the posterior ectosylvian gyrus

LD:

Late-deaf

LP:

Lateral posterior nucleus

MGBd:

Dorsal division of the medial geniculate body

MGBm:

Medial division of the medial geniculate body

MGBv:

Ventral division of the medial geniculate body

MZ:

Multisensory zone

NH:

Normal hearing

nHL:

Normal hearing level

PAF:

Posterior auditory field

PES:

Posterior ectosylvian sulcus

PLLS:

Posterolateral lateral suprasylvian area

PMLS:

Posteromedial lateral suprasylvian area

PO:

Posterior complex

PS:

Posterior suprasylvian area

Psb:

Presubiculum

Rsp:

Posterior limb of the rostral suprasylvian sulcus

SGN:

Suprageniculate nucleus

SVA:

Splenial visual area

S2:

Second somatosensory area

S2m:

Medial division of the second somatosensory area

S3:

Third somatosensory area

S4:

Fourth somatosensory area

S5:

Fifth somatosensory area

T:

Temporal auditory cortical area

VAF:

Ventral auditory field

VLS:

Ventral lateral suprasylvian area

VPAF:

Ventral posterior auditory field

vPE:

Ventral division of the posterior ectosylvian gyrus

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Acknowledgements

The authors would like to thank Pam Nixon for technical and surgical assistance. Thanks also to Benson Li, Chris Lee, and Kevin Ly for assistance with tissue processing. Funding for this work was provided by the Natural Sciences and Engineering Research Council of Canada, the Canadian Institutes of Health Research, and the Canada Foundation for Innovation.

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Authors and Affiliations

  1. Cerebral Systems Laboratory, University of Western Ontario, London, ON, N6A 5C2, Canada

    Blake E. Butler, Alexandra de la Rua, Taylor Ward-Able & Stephen G. Lomber

  2. Department of Psychology, University of Western Ontario, London, ON, N6A 5C2, Canada

    Blake E. Butler & Stephen G. Lomber

  3. Brain and Mind Institute, University of Western Ontario, London, ON, N6A 5B7, Canada

    Blake E. Butler & Stephen G. Lomber

  4. National Centre for Audiology, University of Western Ontario, London, ON, N6G 1H1, Canada

    Blake E. Butler & Stephen G. Lomber

  5. Neuroscience Undergraduate Program, University of Western Ontario, London, ON, N6A 3K7, Canada

    Alexandra de la Rua & Taylor Ward-Able

  6. Department of Physiology and Pharmacology, University of Western Ontario, London, ON, N6A 5C1, Canada

    Stephen G. Lomber

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  1. Blake E. Butler
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Correspondence to Blake E. Butler.

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Funding for this work was provided by the Natural Sciences and Engineering Research Council of Canada, the Canadian Institutes of Health Research, and the Canada Foundation for Innovation.

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The authors declare that they have no conflict of interest.

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All surgical and experimental procedures were conducted in accordance with the Canadian Council on Animal Care’s Guide to the Care and Use of Experimental Animals (Olfert et al. 1993) and were approved by the University of Western Ontario Animal Use Subcommittee of the University Council on Animal Care.

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Butler, B.E., de la Rua, A., Ward-Able, T. et al. Cortical and thalamic connectivity to the second auditory cortex of the cat is resilient to the onset of deafness. Brain Struct Funct 223, 819–835 (2018). https://doi.org/10.1007/s00429-017-1523-y

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