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Acute off-target effects of neural circuit manipulations

Author

Listed:
  • Timothy M. Otchy

    (Center for Brain Science, Harvard University
    Program in Neuroscience, Harvard University)

  • Steffen B. E. Wolff

    (Center for Brain Science, Harvard University)

  • Juliana Y. Rhee

    (Center for Brain Science, Harvard University)

  • Cengiz Pehlevan

    (Center for Computational Biology, Simons Foundation)

  • Risa Kawai

    (Center for Brain Science, Harvard University)

  • Alexandre Kempf

    (Center for Brain Science, Harvard University
    †Present addresses: Institut de Biologie, Ecole Normale Supérieure, Paris, France (A.K.); Neuroscience Program, Wellesley College, Wellesley, Massachusetts 02481, USA (S.M.H.G.).)

  • Sharon M. H. Gobes

    (Center for Brain Science, Harvard University
    †Present addresses: Institut de Biologie, Ecole Normale Supérieure, Paris, France (A.K.); Neuroscience Program, Wellesley College, Wellesley, Massachusetts 02481, USA (S.M.H.G.).)

  • Bence P. Ölveczky

    (Center for Brain Science, Harvard University
    Harvard University)

Abstract

Rapid and reversible manipulations of neural activity in behaving animals are transforming our understanding of brain function. An important assumption underlying much of this work is that evoked behavioural changes reflect the function of the manipulated circuits. We show that this assumption is problematic because it disregards indirect effects on the independent functions of downstream circuits. Transient inactivations of motor cortex in rats and nucleus interface (Nif) in songbirds severely degraded task-specific movement patterns and courtship songs, respectively, which are learned skills that recover spontaneously after permanent lesions of the same areas. We resolve this discrepancy in songbirds, showing that Nif silencing acutely affects the function of HVC, a downstream song control nucleus. Paralleling song recovery, the off-target effects resolved within days of Nif lesions, a recovery consistent with homeostatic regulation of neural activity in HVC. These results have implications for interpreting transient circuit manipulations and for understanding recovery after brain lesions.

Suggested Citation

  • Timothy M. Otchy & Steffen B. E. Wolff & Juliana Y. Rhee & Cengiz Pehlevan & Risa Kawai & Alexandre Kempf & Sharon M. H. Gobes & Bence P. Ölveczky, 2015. "Acute off-target effects of neural circuit manipulations," Nature, Nature, vol. 528(7582), pages 358-363, December.
    • Handle: RePEc:nat:nature:v:528:y:2015:i:7582:d:10.1038_nature16442
    DOI: 10.1038/nature16442
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    Cited by:

    1. Thomas C Südhof, 2016. "Truth in Science Publishing: A Personal Perspective," PLOS Biology, Public Library of Science, vol. 14(8), pages 1-4, August.
    2. 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.
    3. Pierre-Marie Gardères & Sébastien Gal & Charly Rousseau & Alexandre Mamane & Dan Alin Ganea & Florent Haiss, 2024. "Coexistence of state, choice, and sensory integration coding in barrel cortex LII/III," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    4. Matthijs N. Oude Lohuis & Jean L. Pie & Pietro Marchesi & Jorrit S. Montijn & Christiaan P. J. Kock & Cyriel M. A. Pennartz & Umberto Olcese, 2022. "Multisensory task demands temporally extend the causal requirement for visual cortex in perception," Nature Communications, Nature, vol. 13(1), pages 1-19, December.

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