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Reactivation of critical period plasticity in adult auditory cortex through chemogenetic silencing of parvalbumin-positive interneurons

Cisneros-Franco, J. Miguel, de Villers-Sidani, Étienne·2019·Proceedings of the National Academy of Sciences
DOI 10.1073/pnas.1913227117PMC PMC6936688
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Abstract

Sensory experience during early developmental critical periods (CPs) has profound and long-lasting effects on cortical sensory processing perduring well into adulthood. Although recent evidence has shown that reducing cortical inhibition during adulthood reinstates CP plasticity, the precise cellular mechanisms are not well understood. Here, we show that chemogenetic inactivation of parvalbumin-positive (PV + ) interneurons is sufficient to reinstate CP plasticity in the adult auditory cortex. Bidirectional manipulation of PV + cell activity affected neuronal spectral and sound intensity selectivity and, in the case of PV + interneuron inactivation, was mirrored by anatomical changes in PV and associated perineuronal net expression. These findings underscore the importance of sustained PV-mediated inhibitory neurotransmission throughout life and highlight the potential of chemogenetic approaches for harnessing cortical plasticity with the ultimate goal of aiding recovery from brain injury or disease.

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  • PNNs have an important role in the maturation and stabilization of the connectivity of PV1 interneurons in critical periods such as those of the visual and auditory systems.

    “The PNNs have an important role in the maturation and stabilization of the connectivity of PV1 interneurons in critical periods such as those of the visual and auditory systems (Pizzorusso et al., 2002;Cisneros-Franco and de Villers-Sidani, 2019).”

    From Perineuronal Nets Regulate the Inhibitory Perisomatic Input onto Parvalbumin Interneurons and γ Activity in the Prefrontal Cortex (2020) · cites this paper as Cisneros-Franco and de Villers-Sidani, 2019

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Research works printed but not linked: 11

  1. [1]Fagiolini M., Specific GABAA circuits for visual cortical plasticity. Science 303, 1681– 1683 (2004). 15017002
  2. [4]Takesian A. E., Hensch T. K., Balancing plasticity/stability across brain development. Prog. Brain Res. 207, 3– 34 (2013). 24309249
  3. [7]Caillard O., Role of the calcium-binding protein parvalbumin in short-term synaptic plasticity. Proc. Natl. Acad. Sci. U.S.A. 97, 13372– 13377 (2000). 11069288 PMC27231
  4. [9]Donato F., Rompani S. B., Caroni P., Parvalbumin-expressing basket-cell network plasticity induced by experience regulates adult learning. Nature 504, 272– 276 (2013). 24336286
  5. [11]Favuzzi E., Activity-dependent gating of parvalbumin interneuron function by the perineuronal net protein brevican. Neuron 95, 639– 655.e10 (2017). 28712654
  6. [13]Cisneros-Franco J. M., Ouellet L., Kamal B., de Villers-Sidani E., A brain without brakes: Reduced inhibition is associated with enhanced but dysregulated plasticity in the aged rat auditory cortex. eNeuro 5, ENEURO.0051-18.2018 (2018). PMC6140119 30225357
  7. [14]Cisneros-Franco M., de Villers-Sidani E., SI Appendix for Manuscript: Reactivation of critical period plasticity in adult auditory cortex through chemogenetic silencing of parvalbumin-positive interneurons. Figshare. 10.6084/m9.figshare.10248878.v3. Deposited 14 November 2019. PMC6936688 31843881 · DOI
  8. [16]Thomas M. E., Friedman N. H. M., Cisneros-Franco J. M., Ouellet L., de Villers-Sidani É., The prolonged masking of temporal acoustic inputs with noise drives plasticity in the adult rat auditory cortex. Cereb. Cortex 29, 1032– 1046 (2019). 29420680
  9. [17]Mao Y.-T., Pallas S. L., Cross-modal plasticity results in increased inhibition in primary auditory cortical areas. Neural Plast. 2013, 530651 (2013). 24288625 PMC3833201
  10. [18]de Villers-Sidani E., Chang E. F., Bao S., Merzenich M. M., Critical period window for spectral tuning defined in the primary auditory cortex (A1) in the rat. J. Neurosci. 27, 180– 189 (2007). 17202485 PMC6672294
  11. [19]Zhao Y., Imbalance of excitation and inhibition at threshold level in the auditory cortex. Front. Neural Circuits 9, 11 (2015). 25852485 PMC4364151

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Authors
Cisneros-Franco, J. M., & de Villers-Sidani, É.
Affiliations
Montreal Neurological Institute, McGill University, Montreal, QC H3A 2B4, Canada;
ORCID
Cisneros-Franco, J. Miguel
Venue
Proceedings of the National Academy of Sciences
Publisher
National Academy of Sciences
Published
2019-12-16
Volume
116
Issue
52
Pages
26329-26331
ISSN
  • 0027-8424
  • 1091-6490
DOI
10.1073/pnas.1913227117
PMC
PMC6936688
Cited by
54
References
8
Language
en
Licence
creativecommons.org/licenses/by-nc-nd/4.0/ (vor)
Funders
Gouvernement du Canada | Canadian Institutes of Health Research (MOP-133426)

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