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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
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    References listed on IDEAS

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    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. 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.
    6. 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.
    7. Anthony Leonardo & Masakazu Konishi, 1999. "Decrystallization of adult birdsong by perturbation of auditory feedback," Nature, Nature, vol. 399(6735), pages 466-470, June.
    8. 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.
    9. 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.
    10. 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.
    11. 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.
    12. 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.
    13. 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.
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