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Driving fast-spiking cells induces gamma rhythm and controls sensory responses

Author

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  • Jessica A. Cardin

    (MIT, Cambridge, Massachusetts 02139, USA
    University of Pennsylvania, Philadelphia, Pennsylvania 19104, USA)

  • Marie Carlén

    (Picower Institute for Learning and Memory, MIT, Cambridge, Massachusetts 02139, USA
    Stanley Center for Psychiatric Research, Broad Institute of Harvard and Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA)

  • Konstantinos Meletis

    (Picower Institute for Learning and Memory, MIT, Cambridge, Massachusetts 02139, USA
    Stanley Center for Psychiatric Research, Broad Institute of Harvard and Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA)

  • Ulf Knoblich

    (MIT, Cambridge, Massachusetts 02139, USA)

  • Feng Zhang

    (Stanford University, Stanford, California 94305, USA)

  • Karl Deisseroth

    (Stanford University, Stanford, California 94305, USA)

  • Li-Huei Tsai

    (Picower Institute for Learning and Memory, MIT, Cambridge, Massachusetts 02139, USA
    Stanley Center for Psychiatric Research, Broad Institute of Harvard and Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA
    Howard Hughes Medical Institute, Cambridge, Massachusetts 02139, USA)

  • Christopher I. Moore

    (MIT, Cambridge, Massachusetts 02139, USA)

Abstract

Cortical gamma oscillations (20-80 Hz) predict increases in focused attention, and failure in gamma regulation is a hallmark of neurological and psychiatric disease. Current theory predicts that gamma oscillations are generated by synchronous activity of fast-spiking inhibitory interneurons, with the resulting rhythmic inhibition producing neural ensemble synchrony by generating a narrow window for effective excitation. We causally tested these hypotheses in barrel cortex in vivo by targeting optogenetic manipulation selectively to fast-spiking interneurons. Here we show that light-driven activation of fast-spiking interneurons at varied frequencies (8-200 Hz) selectively amplifies gamma oscillations. In contrast, pyramidal neuron activation amplifies only lower frequency oscillations, a cell-type-specific double dissociation. We found that the timing of a sensory input relative to a gamma cycle determined the amplitude and precision of evoked responses. Our data directly support the fast-spiking-gamma hypothesis and provide the first causal evidence that distinct network activity states can be induced in vivo by cell-type-specific activation.

Suggested Citation

  • Jessica A. Cardin & Marie Carlén & Konstantinos Meletis & Ulf Knoblich & Feng Zhang & Karl Deisseroth & Li-Huei Tsai & Christopher I. Moore, 2009. "Driving fast-spiking cells induces gamma rhythm and controls sensory responses," Nature, Nature, vol. 459(7247), pages 663-667, June.
  • Handle: RePEc:nat:nature:v:459:y:2009:i:7247:d:10.1038_nature08002
    DOI: 10.1038/nature08002
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    4. Vadivel, R. & Hammachukiattikul, P. & Gunasekaran, Nallappan & Saravanakumar, R. & Dutta, Hemen, 2021. "Strict dissipativity synchronization for delayed static neural networks: An event-triggered scheme," Chaos, Solitons & Fractals, Elsevier, vol. 150(C).
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    7. Sorinel A Oprisan & Xandre Clementsmith & Tamas Tompa & Antonieta Lavin, 2019. "Dopamine receptor antagonists effects on low-dimensional attractors of local field potentials in optogenetic mice," PLOS ONE, Public Library of Science, vol. 14(10), pages 1-39, October.
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    11. Kai Zhou & Wei Wei & Dan Yang & Hui Zhang & Wei Yang & Yunpeng Zhang & Yingnan Nie & Mingming Hao & Pengcheng Wang & Hang Ruan & Ting Zhang & Shouyan Wang & Yaobo Liu, 2024. "Dual electrical stimulation at spinal-muscular interface reconstructs spinal sensorimotor circuits after spinal cord injury," Nature Communications, Nature, vol. 15(1), pages 1-26, December.
    12. Lou T. Blanpain & Eric R. Cole & Emily Chen & James K. Park & Michael Y. Walelign & Robert E. Gross & Brian T. Cabaniss & Jon T. Willie & Annabelle C. Singer, 2024. "Multisensory flicker modulates widespread brain networks and reduces interictal epileptiform discharges," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    13. Supratim Ray & Amy M Ni & John H R Maunsell, 2013. "Strength of Gamma Rhythm Depends on Normalization," PLOS Biology, Public Library of Science, vol. 11(2), pages 1-12, February.
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