IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-39732-7.html
   My bibliography  Save this article

Cell-type-specific plasticity of inhibitory interneurons in the rehabilitation of auditory cortex after peripheral damage

Author

Listed:
  • Manoj Kumar

    (University of Pittsburgh)

  • Gregory Handy

    (University of Chicago)

  • Stylianos Kouvaros

    (University of Pittsburgh)

  • Yanjun Zhao

    (University of Pittsburgh)

  • Lovisa Ljungqvist Brinson

    (University of Pittsburgh)

  • Eric Wei

    (University of Pittsburgh)

  • Brandon Bizup

    (University of Pittsburgh)

  • Brent Doiron

    (University of Chicago)

  • Thanos Tzounopoulos

    (University of Pittsburgh)

Abstract

Peripheral sensory organ damage leads to compensatory cortical plasticity that is associated with a remarkable recovery of cortical responses to sound. The precise mechanisms that explain how this plasticity is implemented and distributed over a diverse collection of excitatory and inhibitory cortical neurons remain unknown. After noise trauma and persistent peripheral deficits, we found recovered sound-evoked activity in mouse A1 excitatory principal neurons (PNs), parvalbumin- and vasoactive intestinal peptide-expressing neurons (PVs and VIPs), but reduced activity in somatostatin-expressing neurons (SOMs). This cell-type-specific recovery was also associated with cell-type-specific intrinsic plasticity. These findings, along with our computational modelling results, are consistent with the notion that PV plasticity contributes to PN stability, SOM plasticity allows for increased PN and PV activity, and VIP plasticity enables PN and PV recovery by inhibiting SOMs.

Suggested Citation

  • Manoj Kumar & Gregory Handy & Stylianos Kouvaros & Yanjun Zhao & Lovisa Ljungqvist Brinson & Eric Wei & Brandon Bizup & Brent Doiron & Thanos Tzounopoulos, 2023. "Cell-type-specific plasticity of inhibitory interneurons in the rehabilitation of auditory cortex after peripheral damage," Nature Communications, Nature, vol. 14(1), pages 1-23, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39732-7
    DOI: 10.1038/s41467-023-39732-7
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-39732-7
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-39732-7?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Bilal Haider & Michael Häusser & Matteo Carandini, 2013. "Inhibition dominates sensory responses in the awake cortex," Nature, Nature, vol. 493(7430), pages 97-100, January.
    2. Daniel B. Polley & John H. Thompson & Wei Guo, 2013. "Brief hearing loss disrupts binaural integration during two early critical periods of auditory cortex development," Nature Communications, Nature, vol. 4(1), pages 1-13, December.
    3. Meenakshi M. Asokan & Ross S. Williamson & Kenneth E. Hancock & Daniel B. Polley, 2018. "Sensory overamplification in layer 5 auditory corticofugal projection neurons following cochlear nerve synaptic damage," Nature Communications, Nature, vol. 9(1), pages 1-10, December.
    4. Yoko Yazaki-Sugiyama & Siu Kang & Hideyuki Câteau & Tomoki Fukai & Takao K. Hensch, 2009. "Bidirectional plasticity in fast-spiking GABA circuits by visual experience," Nature, Nature, vol. 462(7270), pages 218-221, November.
    5. Hillel Adesnik & William Bruns & Hiroki Taniguchi & Z. Josh Huang & Massimo Scanziani, 2012. "A neural circuit for spatial summation in visual cortex," Nature, Nature, vol. 490(7419), pages 226-231, October.
    6. Meenakshi M. Asokan & Ross S. Williamson & Kenneth E. Hancock & Daniel B. Polley, 2018. "Publisher Correction: Sensory overamplification in layer 5 auditory corticofugal projection neurons following cochlear nerve synaptic damage," Nature Communications, Nature, vol. 9(1), pages 1-1, December.
    7. B. Haider & M. Häusser & M. Carandini, 2013. "Correction: Corrigendum: Inhibition dominates sensory responses in awake cortex," Nature, Nature, vol. 500(7464), pages 612-612, August.
    8. Sandra J. Kuhlman & Nicholas D. Olivas & Elaine Tring & Taruna Ikrar & Xiangmin Xu & Joshua T. Trachtenberg, 2013. "A disinhibitory microcircuit initiates critical-period plasticity in the visual cortex," Nature, Nature, vol. 501(7468), pages 543-546, September.
    9. Michael Wehr & Anthony M. Zador, 2003. "Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex," Nature, Nature, vol. 426(6965), pages 442-446, November.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Panagiotis Fotiadis & Matthew Cieslak & Xiaosong He & Lorenzo Caciagli & Mathieu Ouellet & Theodore D. Satterthwaite & Russell T. Shinohara & Dani S. Bassett, 2023. "Myelination and excitation-inhibition balance synergistically shape structure-function coupling across the human cortex," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    2. Koun Onodera & Hiroyuki K. Kato, 2022. "Translaminar recurrence from layer 5 suppresses superficial cortical layers," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    3. Tristan G. Heintz & Antonio J. Hinojosa & Sina E. Dominiak & Leon Lagnado, 2022. "Opposite forms of adaptation in mouse visual cortex are controlled by distinct inhibitory microcircuits," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    4. Shan Shen & Xiaolong Jiang & Federico Scala & Jiakun Fu & Paul Fahey & Dmitry Kobak & Zhenghuan Tan & Na Zhou & Jacob Reimer & Fabian Sinz & Andreas S. Tolias, 2022. "Distinct organization of two cortico-cortical feedback pathways," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    5. Lloyd E. Russell & Mehmet Fişek & Zidan Yang & Lynn Pei Tan & Adam M. Packer & Henry W. P. Dalgleish & Selmaan N. Chettih & Christopher D. Harvey & Michael Häusser, 2024. "The influence of cortical activity on perception depends on behavioral state and sensory context," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    6. Bryce D. Grier & Samuel Parkins & Jarra Omar & Hey-Kyoung Lee, 2023. "Selective plasticity of fast and slow excitatory synapses on somatostatin interneurons in adult visual cortex," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    7. Margot C Bjoring & C Daniel Meliza, 2019. "A low-threshold potassium current enhances sparseness and reliability in a model of avian auditory cortex," PLOS Computational Biology, Public Library of Science, vol. 15(1), pages 1-20, January.
    8. David Pérez-González & Olga Hernández & Ellen Covey & Manuel S Malmierca, 2012. "GABAA-Mediated Inhibition Modulates Stimulus-Specific Adaptation in the Inferior Colliculus," PLOS ONE, Public Library of Science, vol. 7(3), pages 1-14, March.
    9. Catalina Vich & Rafel Prohens & Antonio E. Teruel & Antoni Guillamon, 2020. "Estimation of Synaptic Activity during Neuronal Oscillations," Mathematics, MDPI, vol. 8(12), pages 1-22, December.
    10. Thomas Miconi & Rufin VanRullen, 2016. "A Feedback Model of Attention Explains the Diverse Effects of Attention on Neural Firing Rates and Receptive Field Structure," PLOS Computational Biology, Public Library of Science, vol. 12(2), pages 1-18, February.
    11. Christopher Ebsch & Robert Rosenbaum, 2018. "Imbalanced amplification: A mechanism of amplification and suppression from local imbalance of excitation and inhibition in cortical circuits," PLOS Computational Biology, Public Library of Science, vol. 14(3), pages 1-28, March.
    12. Alireza Saeedi & Kun Wang & Ghazaleh Nikpourian & Andreas Bartels & Nikos K. Logothetis & Nelson K. Totah & Masataka Watanabe, 2024. "Brightness illusions drive a neuronal response in the primary visual cortex under top-down modulation," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    13. Tomáš Hromádka & Michael R DeWeese & Anthony M Zador, 2008. "Sparse Representation of Sounds in the Unanesthetized Auditory Cortex," PLOS Biology, Public Library of Science, vol. 6(1), pages 1-14, January.
    14. Vicente Reyes-Puerta & Suam Kim & Jyh-Jang Sun & Barbara Imbrosci & Werner Kilb & Heiko J Luhmann, 2015. "High Stimulus-Related Information in Barrel Cortex Inhibitory Interneurons," PLOS Computational Biology, Public Library of Science, vol. 11(6), pages 1-32, June.
    15. Mizusaki, Beatriz E.P. & Agnes, Everton J. & Erichsen, Rubem & Brunnet, Leonardo G., 2017. "Learning and retrieval behavior in recurrent neural networks with pre-synaptic dependent homeostatic plasticity," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 479(C), pages 279-286.
    16. Kelsey L. Anbuhl & Justin D. Yao & Robert A. Hotz & Todd M. Mowery & Dan H. Sanes, 2022. "Auditory processing remains sensitive to environmental experience during adolescence in a rodent model," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    17. Sean T Kelly & Jens Kremkow & Jianzhong Jin & Yushi Wang & Qi Wang & Jose-Manuel Alonso & Garrett B Stanley, 2014. "The Role of Thalamic Population Synchrony in the Emergence of Cortical Feature Selectivity," PLOS Computational Biology, Public Library of Science, vol. 10(1), pages 1-13, January.
    18. Jack Phu & Michael Kalloniatis & Sieu K Khuu, 2016. "The Effect of Attentional Cueing and Spatial Uncertainty in Visual Field Testing," PLOS ONE, Public Library of Science, vol. 11(3), pages 1-18, March.
    19. Takafumi Arakaki & G Barello & Yashar Ahmadian, 2019. "Inferring neural circuit structure from datasets of heterogeneous tuning curves," PLOS Computational Biology, Public Library of Science, vol. 15(4), pages 1-38, April.
    20. Katie H. Long & Justin D. Lieber & Sliman J. Bensmaia, 2022. "Texture is encoded in precise temporal spiking patterns in primate somatosensory cortex," Nature Communications, Nature, vol. 13(1), pages 1-12, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39732-7. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.