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Loss of Brain-Derived Neurotrophic Factor Mediates Inhibition of Hippocampal Long-Term Potentiation by High-Intensity Sound

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Abstract

Exposure to noise produces cognitive and emotional disorders, and recent studies have shown that auditory stimulation or deprivation affects hippocampal function. Previously, we showed that exposure to high-intensity sound (110 dB, 1 min) strongly inhibits Schaffer-CA1 long-term potentiation (LTP). Here we investigated possible mechanisms involved in this effect. We found that exposure to 110 dB sound activates c-fos expression in hippocampal CA1 and CA3 neurons. Although sound stimulation did not affect glutamatergic or GABAergic neurotransmission in CA1, it did depress the level of brain-derived neurotrophic factor (BDNF), which is involved in promoting hippocampal synaptic plasticity. Moreover, perfusion of slices with BDNF rescued LTP in animals exposed to sound stimulation, whereas BDNF did not affect LTP in sham-stimulated rats. Furthermore, LM22A4, a TrkB receptor agonist, also rescued LTP from sound-stimulated animals. Our results indicate that depression of hippocampal BDNF mediates the inhibition of LTP produced by high-intensity sound stimulation.

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Acknowledgements

We thank the technical assistance of Mr. J. Fernando Aguiar and Mr. Rubens F. de Melo, and Dr. Christopher Kushmerick for reviewing the manuscript.

Funding

Work supported by São Paulo State Research Foundation (FAPESP) Grants 2015/22327-7, 2016/01607-4 and 2016/17681-9.

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Authors and Affiliations

  1. Department of Physiology, School of Medicine of Ribeirão Preto, University of São Paulo, Ribeirão Preto, SP, 14049-900, Brazil

    Júnia L. de Deus, Aline B. Ribeiro, Procópio C. G. Barcellos-Filho, César C. Ceballos, Alexandra O. S. Cunha & Ricardo M. Leão

  2. Department of Basic and Oral Biology, Dental School of Ribeirão Preto, University of São Paulo, Ribeirão Preto, SP, 14040-904, Brazil

    Júnia L. de Deus, Mateus R. Amorim & Luiz Guilherme S. Branco

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  1. Júnia L. de Deus
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  2. Mateus R. Amorim
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  3. Aline B. Ribeiro
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  8. Ricardo M. Leão
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Contributions

Conceptualization [RML, AOSC, JLD]; Investigation: [JLD, MRA, ABR, PCGB-F); Data Analysis: [JLD, MRA, ABR, PCGB-F, CCC]; Software [CCC]; Writing—original draft preparation: [RML, JLD, ABR]; Writing—review and editing: [RML, JLD, ABR, AOSC]; Funding acquisition: [RML, AOSC, LGSB]; Supervision: [RML, LGSB].

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Correspondence to Ricardo M. Leão.

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All experimental procedures involving animals were elaborated according to the rules of research in the National Council for Control of Animal Experimentation and approved by the Committee on Ethics in Animal Use of the Ribeirão Preto Medical School of the University of São Paulo, (protocol # 006/2-2015).

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de Deus, J.L., Amorim, M.R., Ribeiro, A.B. et al. Loss of Brain-Derived Neurotrophic Factor Mediates Inhibition of Hippocampal Long-Term Potentiation by High-Intensity Sound. Cell Mol Neurobiol 41, 751–763 (2021). https://doi.org/10.1007/s10571-020-00881-8

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