The whisking oscillator circuit

Jun Takatoh (), Vincent Prevosto, P. M. Thompson, Jinghao Lu, Leeyup Chung, Andrew Harrahill, Shun Li, Shengli Zhao, Zhigang He, David Golomb, David Kleinfeld and Fan Wang ()
Additional contact information
Jun Takatoh: McGovern Institute for Brain Research, Massachusetts Institute of Technology
Vincent Prevosto: McGovern Institute for Brain Research, Massachusetts Institute of Technology
P. M. Thompson: McGovern Institute for Brain Research, Massachusetts Institute of Technology
Jinghao Lu: McGovern Institute for Brain Research, Massachusetts Institute of Technology
Leeyup Chung: Boston Children’s Hospital
Andrew Harrahill: McGovern Institute for Brain Research, Massachusetts Institute of Technology
Shun Li: Duke University
Shengli Zhao: Duke University
Zhigang He: Boston Children’s Hospital
David Golomb: Ben Gurion University
David Kleinfeld: University of California at San Diego
Fan Wang: McGovern Institute for Brain Research, Massachusetts Institute of Technology

Nature, 2022, vol. 609, issue 7927, 560-568

Abstract: Abstract Central oscillators are primordial neural circuits that generate and control rhythmic movements1,2. Mechanistic understanding of these circuits requires genetic identification of the oscillator neurons and their synaptic connections to enable targeted electrophysiological recording and causal manipulation during behaviours. However, such targeting remains a challenge with mammalian systems. Here we delimit the oscillator circuit that drives rhythmic whisking—a motor action that is central to foraging and active sensing in rodents3,4. We found that the whisking oscillator consists of parvalbumin-expressing inhibitory neurons located in the vibrissa intermediate reticular nucleus (vIRtPV) in the brainstem. vIRtPV neurons receive descending excitatory inputs and form recurrent inhibitory connections among themselves. Silencing vIRtPV neurons eliminated rhythmic whisking and resulted in sustained vibrissae protraction. In vivo recording of opto-tagged vIRtPV neurons in awake mice showed that these cells spike tonically when animals are at rest, and transition to rhythmic bursting at the onset of whisking, suggesting that rhythm generation is probably the result of network dynamics, as opposed to intrinsic cellular properties. Notably, ablating inhibitory synaptic inputs to vIRtPV neurons quenched their rhythmic bursting, impaired the tonic-to-bursting transition and abolished regular whisking. Thus, the whisking oscillator is an all-inhibitory network and recurrent synaptic inhibition has a key role in its rhythmogenesis.

Date: 2022
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DOI: 10.1038/s41586-022-05144-8

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