IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-51818-4.html
   My bibliography  Save this article

Disinhibition enables vocal repertoire expansion after a critical period

Author

Listed:
  • Fabian Heim

    (Max Planck Institute for Biological Intelligence)

  • Ezequiel Mendoza

    (Max Planck Institute for Biological Intelligence
    Freie Universität Berlin)

  • Avani Koparkar

    (Max Planck Institute for Biological Intelligence
    Indian Institute of Science Education and Research (IISER)
    Eberhard-Karls-Universität Tübingen)

  • Daniela Vallentin

    (Max Planck Institute for Biological Intelligence)

Abstract

The efficiency of motor skill acquisition is age-dependent, making it increasingly challenging to learn complex manoeuvres later in life. Zebra finches, for instance, acquire a complex vocal motor programme during a developmental critical period after which the learned song is essentially impervious to modification. Although inhibitory interneurons are implicated in critical period closure, it is unclear whether manipulating them can reopen heightened motor plasticity windows. Using pharmacology and a cell-type specific optogenetic approach, we manipulated inhibitory neuron activity in a premotor area of adult zebra finches beyond their critical period. When exposed to auditory stimulation in the form of novel songs, manipulated birds added new vocal syllables to their stable song sequence. By lifting inhibition in a premotor area during sensory experience, we reintroduced vocal plasticity, promoting an expansion of the syllable repertoire without compromising pre-existing song production. Our findings provide insights into motor skill learning capacities, offer potential for motor recovery after injury, and suggest avenues for treating neurodevelopmental disorders involving inhibitory dysfunctions.

Suggested Citation

  • Fabian Heim & Ezequiel Mendoza & Avani Koparkar & Daniela Vallentin, 2024. "Disinhibition enables vocal repertoire expansion after a critical period," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-51818-4
    DOI: 10.1038/s41467-024-51818-4
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-51818-4
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-51818-4?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. Evren C. Tumer & Michael S. Brainard, 2007. "Performance variability enables adaptive plasticity of ‘crystallized’ adult birdsong," Nature, Nature, vol. 450(7173), pages 1240-1244, December.
    2. Richard H. R. Hahnloser & Alexay A. Kozhevnikov & Michale S. Fee, 2002. "An ultra-sparse code underliesthe generation of neural sequences in a songbird," Nature, Nature, vol. 419(6902), pages 65-70, September.
    3. Dina Lipkind & Gary F. Marcus & Douglas K. Bemis & Kazutoshi Sasahara & Nori Jacoby & Miki Takahasi & Kenta Suzuki & Olga Feher & Primoz Ravbar & Kazuo Okanoya & Ofer Tchernichovski, 2013. "Stepwise acquisition of vocal combinatorial capacity in songbirds and human infants," Nature, Nature, vol. 498(7452), pages 104-108, June.
    4. Iris Adam & Katharina Riebel & Per Stål & Neil Wood & Michael J. Previs & Coen P. H. Elemans, 2023. "Daily vocal exercise is necessary for peak performance singing in a songbird," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    5. Yasemin B. Gultekin & Steffen R. Hage, 2017. "Limiting parental feedback disrupts vocal development in marmoset monkeys," Nature Communications, Nature, vol. 8(1), pages 1-9, April.
    6. Romain Nardou & Eastman M. Lewis & Rebecca Rothhaas & Ran Xu & Aimei Yang & Edward Boyden & Gül Dölen, 2019. "Oxytocin-dependent reopening of a social reward learning critical period with MDMA," Nature, Nature, vol. 569(7754), pages 116-120, May.
    7. Mark N. Miller & Chung Yan J. Cheung & Michael S. Brainard, 2017. "Vocal learning promotes patterned inhibitory connectivity," Nature Communications, Nature, vol. 8(1), pages 1-9, December.
    8. Anthony Leonardo & Masakazu Konishi, 1999. "Decrystallization of adult birdsong by perturbation of auditory feedback," Nature, Nature, vol. 399(6735), pages 466-470, June.
    9. Michael A. Long & Dezhe Z. Jin & Michale S. Fee, 2010. "Support for a synaptic chain model of neuronal sequence generation," Nature, Nature, vol. 468(7322), pages 394-399, November.
    10. Michael A. Long & Michale S. Fee, 2008. "Using temperature to analyse temporal dynamics in the songbird motor pathway," Nature, Nature, vol. 456(7219), pages 189-194, November.
    11. Brian Y. Chow & Xue Han & Allison S. Dobry & Xiaofeng Qian & Amy S. Chuong & Mingjie Li & Michael A. Henninger & Gabriel M. Belfort & Yingxi Lin & Patrick E. Monahan & Edward S. Boyden, 2010. "High-performance genetically targetable optical neural silencing by light-driven proton pumps," Nature, Nature, vol. 463(7277), pages 98-102, January.
    12. Michela Fagiolini & Takao K. Hensch, 2000. "Inhibitory threshold for critical-period activation in primary visual cortex," Nature, Nature, vol. 404(6774), pages 183-186, March.
    13. Jonnathan Singh Alvarado & Jack Goffinet & Valerie Michael & William Liberti & Jordan Hatfield & Timothy Gardner & John Pearson & Richard Mooney, 2021. "Neural dynamics underlying birdsong practice and performance," Nature, Nature, vol. 599(7886), pages 635-639, 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. Linda Bistere & Carlos M. Gomez-Guzman & Yirong Xiong & Daniela Vallentin, 2024. "Female calls promote song learning in male juvenile zebra finches," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    2. Benjamin M. Zemel & Alexander A. Nevue & Andre Dagostin & Peter V. Lovell & Claudio V. Mello & Henrique Gersdorff, 2021. "Resurgent Na+ currents promote ultrafast spiking in projection neurons that drive fine motor control," Nature Communications, Nature, vol. 12(1), pages 1-23, December.
    3. Matthew A Slayton & Juan L Romero-Sosa & Katrina Shore & Dean V Buonomano & Indre V Viskontas, 2020. "Musical expertise generalizes to superior temporal scaling in a Morse code tapping task," PLOS ONE, Public Library of Science, vol. 15(1), pages 1-9, January.
    4. Sravani Kondapavulur & Stefan M. Lemke & David Darevsky & Ling Guo & Preeya Khanna & Karunesh Ganguly, 2022. "Transition from predictable to variable motor cortex and striatal ensemble patterning during behavioral exploration," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    5. Dezhe Z Jin & Alexay A Kozhevnikov, 2011. "A Compact Statistical Model of the Song Syntax in Bengalese Finch," PLOS Computational Biology, Public Library of Science, vol. 7(3), pages 1-19, March.
    6. Joshua M Mueller & Primoz Ravbar & Julie H Simpson & Jean M Carlson, 2019. "Drosophila melanogaster grooming possesses syntax with distinct rules at different temporal scales," PLOS Computational Biology, Public Library of Science, vol. 15(6), pages 1-25, June.
    7. Shota Saito & Yoshito Hirata & Kazutoshi Sasahara & Hideyuki Suzuki, 2015. "Tracking Time Evolution of Collective Attention Clusters in Twitter: Time Evolving Nonnegative Matrix Factorisation," PLOS ONE, Public Library of Science, vol. 10(9), pages 1-17, September.
    8. Yosef Prat & Lindsay Azoulay & Roi Dor & Yossi Yovel, 2017. "Crowd vocal learning induces vocal dialects in bats: Playback of conspecifics shapes fundamental frequency usage by pups," PLOS Biology, Public Library of Science, vol. 15(10), pages 1-14, October.
    9. Patrick D McMullen & Erin Z Aprison & Peter B Winter & Luis A N Amaral & Richard I Morimoto & Ilya Ruvinsky, 2012. "Macro-level Modeling of the Response of C. elegans Reproduction to Chronic Heat Stress," PLOS Computational Biology, Public Library of Science, vol. 8(1), pages 1-12, January.
    10. Aujla, Navneet & Frost, Helen & Guthrie, Bruce & Hanratty, Barbara & Kaner, Eileen & O'Donnell, Amy & Ogden, Margaret E. & Pain, Helen G. & Shenkin, Susan D. & Mercer, Stewart W., 2023. "A comparative overview of health and social care policy for older people in England and Scotland, United Kingdom (UK)," Health Policy, Elsevier, vol. 132(C).
    11. A. Barri & M. T. Wiechert & M. Jazayeri & D. A. DiGregorio, 2022. "Synaptic basis of a sub-second representation of time in a neural circuit model," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    12. John Palmer & Adam Keane & Pulin Gong, 2017. "Learning and executing goal-directed choices by internally generated sequences in spiking neural circuits," PLOS Computational Biology, Public Library of Science, vol. 13(7), pages 1-23, July.
    13. Stanislav Ott & Sangyu Xu & Nicole Lee & Ivan Hong & Jonathan Anns & Danesha Devini Suresh & Zhiyi Zhang & Xianyuan Zhang & Raihanah Harion & Weiying Ye & Vaishnavi Chandramouli & Suresh Jesuthasan & , 2024. "Kalium channelrhodopsins effectively inhibit neurons," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    14. Chong Guo & Vincent Huson & Evan Z. Macosko & Wade G. Regehr, 2021. "Graded heterogeneity of metabotropic signaling underlies a continuum of cell-intrinsic temporal responses in unipolar brush cells," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    15. Takuto Kawaji & Mizuki Fujibayashi & Kentaro Abe, 2024. "Goal-directed and flexible modulation of syllable sequence within birdsong," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    16. Yang Yiling & Katharine Shapcott & Alina Peter & Johanna Klon-Lipok & Huang Xuhui & Andreea Lazar & Wolf Singer, 2023. "Robust encoding of natural stimuli by neuronal response sequences in monkey visual cortex," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    17. David Kappel & Bernhard Nessler & Wolfgang Maass, 2014. "STDP Installs in Winner-Take-All Circuits an Online Approximation to Hidden Markov Model Learning," PLOS Computational Biology, Public Library of Science, vol. 10(3), pages 1-22, March.
    18. Aki Takahashi & Romain Durand-de Cuttoli & Meghan E. Flanigan & Emi Hasegawa & Tomomi Tsunematsu & Hossein Aleyasin & Yoan Cherasse & Ken Miya & Takuya Okada & Kazuko Keino-Masu & Koshiro Mitsui & Lon, 2022. "Lateral habenula glutamatergic neurons projecting to the dorsal raphe nucleus promote aggressive arousal in mice," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    19. Lizhu Li & Lihui Lu & Yuqi Ren & Guo Tang & Yu Zhao & Xue Cai & Zhao Shi & He Ding & Changbo Liu & Dali Cheng & Yang Xie & Huachun Wang & Xin Fu & Lan Yin & Minmin Luo & Xing Sheng, 2022. "Colocalized, bidirectional optogenetic modulations in freely behaving mice with a wireless dual-color optoelectronic probe," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    20. Jonathan B Dingwell & Joby John & Joseph P Cusumano, 2010. "Do Humans Optimally Exploit Redundancy to Control Step Variability in Walking?," PLOS Computational Biology, Public Library of Science, vol. 6(7), pages 1-15, July.

    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:15:y:2024:i:1:d:10.1038_s41467-024-51818-4. 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.