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Research Articles, Development/Plasticity/Repair

Pairing with Enriched Sound Exposure Restores Auditory Processing Degraded by an Antidepressant

Yuan Cheng, Ruru Chen, Bowen Su, Guimin Zhang, Yutian Sun, Pengying An, Yue Fang, Yifan Zhang, Ye Shan, Étienne de Villers-Sidani, Yunfeng Wang and Xiaoming Zhou
Journal of Neuroscience 19 April 2023, 43 (16) 2850-2859; DOI: https://doi.org/10.1523/JNEUROSCI.2027-22.2023
Yuan Cheng
1Key Laboratory of Brain Functional Genomics of Ministry of Education, Shanghai Key Laboratory of Brain Functional Genomics, School of Life Sciences, East China Normal University, Shanghai, 200062, China
2New York University-East China Normal University Institute of Brain and Cognitive Science, New York University-Shanghai, Shanghai, 200062, China
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Ruru Chen
1Key Laboratory of Brain Functional Genomics of Ministry of Education, Shanghai Key Laboratory of Brain Functional Genomics, School of Life Sciences, East China Normal University, Shanghai, 200062, China
2New York University-East China Normal University Institute of Brain and Cognitive Science, New York University-Shanghai, Shanghai, 200062, China
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Bowen Su
1Key Laboratory of Brain Functional Genomics of Ministry of Education, Shanghai Key Laboratory of Brain Functional Genomics, School of Life Sciences, East China Normal University, Shanghai, 200062, China
2New York University-East China Normal University Institute of Brain and Cognitive Science, New York University-Shanghai, Shanghai, 200062, China
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Guimin Zhang
1Key Laboratory of Brain Functional Genomics of Ministry of Education, Shanghai Key Laboratory of Brain Functional Genomics, School of Life Sciences, East China Normal University, Shanghai, 200062, China
2New York University-East China Normal University Institute of Brain and Cognitive Science, New York University-Shanghai, Shanghai, 200062, China
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Yutian Sun
1Key Laboratory of Brain Functional Genomics of Ministry of Education, Shanghai Key Laboratory of Brain Functional Genomics, School of Life Sciences, East China Normal University, Shanghai, 200062, China
2New York University-East China Normal University Institute of Brain and Cognitive Science, New York University-Shanghai, Shanghai, 200062, China
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Pengying An
1Key Laboratory of Brain Functional Genomics of Ministry of Education, Shanghai Key Laboratory of Brain Functional Genomics, School of Life Sciences, East China Normal University, Shanghai, 200062, China
2New York University-East China Normal University Institute of Brain and Cognitive Science, New York University-Shanghai, Shanghai, 200062, China
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Yue Fang
1Key Laboratory of Brain Functional Genomics of Ministry of Education, Shanghai Key Laboratory of Brain Functional Genomics, School of Life Sciences, East China Normal University, Shanghai, 200062, China
2New York University-East China Normal University Institute of Brain and Cognitive Science, New York University-Shanghai, Shanghai, 200062, China
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Yifan Zhang
1Key Laboratory of Brain Functional Genomics of Ministry of Education, Shanghai Key Laboratory of Brain Functional Genomics, School of Life Sciences, East China Normal University, Shanghai, 200062, China
2New York University-East China Normal University Institute of Brain and Cognitive Science, New York University-Shanghai, Shanghai, 200062, China
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Ye Shan
1Key Laboratory of Brain Functional Genomics of Ministry of Education, Shanghai Key Laboratory of Brain Functional Genomics, School of Life Sciences, East China Normal University, Shanghai, 200062, China
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Étienne de Villers-Sidani
3Department of Neurology and Neurosurgery, Montreal Neurological Institute, McGill University, Montreal, Quebec Canada
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Yunfeng Wang
4ENT institute and Department of Otorhinolaryngology of Eye & ENT Hospital, NHC Key Laboratory of Hearing Medicine, Fudan University, Shanghai, 200031, China
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Xiaoming Zhou
1Key Laboratory of Brain Functional Genomics of Ministry of Education, Shanghai Key Laboratory of Brain Functional Genomics, School of Life Sciences, East China Normal University, Shanghai, 200062, China
2New York University-East China Normal University Institute of Brain and Cognitive Science, New York University-Shanghai, Shanghai, 200062, China
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Abstract

Antidepressants, while effective in treating depression and anxiety disorders, also induce deficits in sensory (particularly auditory) processing, which in turn may exacerbate psychiatric symptoms. How antidepressants cause auditory signature deficits remains largely unknown. Here, we found that fluoxetine-treated adult female rats were significantly less accurate when performing a tone-frequency discrimination task compared with age-matched control rats. Their cortical neurons also responded less selectively to sound frequencies. The degraded behavioral and cortical processing was accompanied by decreased cortical perineuronal nets, particularly those wrapped around parvalbumin-expressing inhibitory interneurons. Furthermore, fluoxetine induced critical period-like plasticity in their already mature auditory cortices; therefore, a brief rearing of these drug-treated rats under an enriched acoustic environment renormalized auditory processing degraded by fluoxetine. The altered cortical expression of perineuronal nets was also reversed as a result of enriched sound exposure. These findings suggest that the adverse effects of antidepressants on auditory processing, possibly because of a reduction in intracortical inhibition, can be substantially alleviated by simply pairing drug treatment with passive, enriched sound exposure. They have important implications for understanding the neurobiological basis of antidepressant effects on hearing and for designing novel pharmacological treatment strategies for psychiatric disorders.

SIGNIFICANCE STATEMENT Clinical experience suggests that antidepressants adversely affect sensory (particularly auditory) processing, which can exacerbate patients' psychiatric symptoms. Here, we show that the antidepressant fluoxetine reduces cortical inhibition in adult rats, leading to degraded behavioral and cortical spectral processing of sound. Importantly, fluoxetine induces a critical period-like state of plasticity in the mature cortex; therefore, a brief rearing under an enriched acoustic environment is sufficient to reverse the changes in auditory processing caused by the administration of fluoxetine. These results provide a putative neurobiological basis for the effects of antidepressants on hearing and indicate that antidepressant treatment combined with enriched sensory experiences could optimize clinical outcomes.

  • antidepressant
  • auditory cortex
  • cortical plasticity
  • frequency tuning
  • inhibition

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The Journal of Neuroscience: 43 (16)
Journal of Neuroscience
Vol. 43, Issue 16
19 Apr 2023
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Pairing with Enriched Sound Exposure Restores Auditory Processing Degraded by an Antidepressant
Yuan Cheng, Ruru Chen, Bowen Su, Guimin Zhang, Yutian Sun, Pengying An, Yue Fang, Yifan Zhang, Ye Shan, Étienne de Villers-Sidani, Yunfeng Wang, Xiaoming Zhou
Journal of Neuroscience 19 April 2023, 43 (16) 2850-2859; DOI: 10.1523/JNEUROSCI.2027-22.2023

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Pairing with Enriched Sound Exposure Restores Auditory Processing Degraded by an Antidepressant
Yuan Cheng, Ruru Chen, Bowen Su, Guimin Zhang, Yutian Sun, Pengying An, Yue Fang, Yifan Zhang, Ye Shan, Étienne de Villers-Sidani, Yunfeng Wang, Xiaoming Zhou
Journal of Neuroscience 19 April 2023, 43 (16) 2850-2859; DOI: 10.1523/JNEUROSCI.2027-22.2023
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Keywords

  • antidepressant
  • auditory cortex
  • cortical plasticity
  • frequency tuning
  • inhibition

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