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Research Articles, Development/Plasticity/Repair

Preserving Inhibition during Developmental Hearing Loss Rescues Auditory Learning and Perception

Todd M. Mowery, Melissa L. Caras, Syeda I. Hassan, Derek J. Wang, Jordane Dimidschstein, Gord Fishell and Dan H. Sanes
Journal of Neuroscience 16 October 2019, 39 (42) 8347-8361; DOI: https://doi.org/10.1523/JNEUROSCI.0749-19.2019
Todd M. Mowery
1Center for Neural Science,
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Melissa L. Caras
1Center for Neural Science,
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Syeda I. Hassan
1Center for Neural Science,
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Derek J. Wang
1Center for Neural Science,
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Jordane Dimidschstein
6Stanley Center for Psychiatric Research, Broad Institute of Massachusetts Institute of Technology and Harvard, Boston, Massachusetts 02142
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Gord Fishell
5Department of Neurobiology, Harvard Medical School, Boston, Massachusetts 02115,
6Stanley Center for Psychiatric Research, Broad Institute of Massachusetts Institute of Technology and Harvard, Boston, Massachusetts 02142
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Dan H. Sanes
1Center for Neural Science,
2Department of Psychology,
3Department of Biology,
4Neuroscience Institute at New York University Langone School of Medicine, New York University, New York, New York 10003,
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Abstract

Transient periods of childhood hearing loss can induce deficits in aural communication that persist long after auditory thresholds have returned to normal, reflecting long-lasting impairments to the auditory CNS. Here, we asked whether these behavioral deficits could be reversed by treating one of the central impairments: reduction of inhibitory strength. Male and female gerbils received bilateral earplugs to induce a mild, reversible hearing loss during the critical period of auditory cortex development. After earplug removal and the return of normal auditory thresholds, we trained and tested animals on an amplitude modulation detection task. Transient developmental hearing loss induced both learning and perceptual deficits, which were entirely corrected by treatment with a selective GABA reuptake inhibitor (SGRI). To explore the mechanistic basis for these behavioral findings, we recorded the amplitudes of GABAA and GABAB receptor-mediated IPSPs in auditory cortical and thalamic brain slices. In hearing loss-reared animals, cortical IPSP amplitudes were significantly reduced within a few days of hearing loss onset, and this reduction persisted into adulthood. SGRI treatment during the critical period prevented the hearing loss-induced reduction of IPSP amplitudes; but when administered after the critical period, it only restored GABAB receptor-mediated IPSP amplitudes. These effects were driven, in part, by the ability of SGRI to upregulate α1 subunit-dependent GABAA responses. Similarly, SGRI prevented the hearing loss-induced reduction of GABAA and GABAB IPSPs in the ventral nucleus of the medial geniculate body. Thus, by maintaining, or subsequently rescuing, GABAergic transmission in the central auditory thalamocortical pathway, some perceptual and cognitive deficits induced by developmental hearing loss can be prevented.

SIGNIFICANCE STATEMENT Even a temporary period of childhood hearing loss can induce communication deficits that persist long after auditory thresholds return to normal. These deficits may arise from long-lasting central impairments, including the loss of synaptic inhibition. Here, we asked whether hearing loss-induced behavioral deficits could be reversed by reinstating normal inhibitory strength. Gerbils reared with transient hearing loss displayed both learning and perceptual deficits. However, when animals were treated with a selective GABA reuptake inhibitor during or after hearing loss, behavioral deficits were entirely corrected. This behavioral recovery was correlated with the return of normal thalamic and cortical inhibitory function. Thus, some perceptual and cognitive deficits induced by developmental hearing loss were prevented with a treatment that rescues a central synaptic property.

  • auditory cortex
  • auditory perception
  • hearing loss
  • plasticity
  • synaptic inhibition
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The Journal of Neuroscience: 39 (42)
Journal of Neuroscience
Vol. 39, Issue 42
16 Oct 2019
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Preserving Inhibition during Developmental Hearing Loss Rescues Auditory Learning and Perception
Todd M. Mowery, Melissa L. Caras, Syeda I. Hassan, Derek J. Wang, Jordane Dimidschstein, Gord Fishell, Dan H. Sanes
Journal of Neuroscience 16 October 2019, 39 (42) 8347-8361; DOI: 10.1523/JNEUROSCI.0749-19.2019

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Preserving Inhibition during Developmental Hearing Loss Rescues Auditory Learning and Perception
Todd M. Mowery, Melissa L. Caras, Syeda I. Hassan, Derek J. Wang, Jordane Dimidschstein, Gord Fishell, Dan H. Sanes
Journal of Neuroscience 16 October 2019, 39 (42) 8347-8361; DOI: 10.1523/JNEUROSCI.0749-19.2019
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Keywords

  • auditory cortex
  • auditory perception
  • hearing loss
  • plasticity
  • synaptic inhibition

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