Cell Reports
Volume 37, Issue 8, 23 November 2021, 110035
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Article
Inhibitory control of synaptic signals preceding locomotion in mouse frontal cortex

https://doi.org/10.1016/j.celrep.2021.110035Get rights and content
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Highlights

  • MOs principal neurons show slow membrane potential and spike ramps before running

  • Membrane potential and spike ramps are faster and larger after goal-directed training

  • Inactivation of PV+ and SOM+ interneurons differentially affects ramping signals

  • Modeling suggests that external inputs and local inhibition shape prerunning ramps

Summary

The frontal cortex is essential for organizing voluntary movement. The secondary motor cortex (MOs) is a frontal subregion thought to integrate internal and external inputs before motor action. However, how excitatory and inhibitory synaptic inputs to MOs neurons are integrated preceding movement remains unclear. Here, we address this question by performing in vivo whole-cell recordings from MOs neurons of head-fixed mice moving on a treadmill. We find that principal neurons produce slowly increasing membrane potential and spike ramps preceding spontaneous running. After goal-directed training, ramps show larger amplitudes and accelerated kinetics. Chemogenetic suppression of interneurons combined with modeling suggests that the interplay between parvalbumin-positive (PV+) and somatostatin-positive (SOM+) interneurons, along with principal neuron recurrent connectivity, shape ramping signals. Plasticity of excitatory synapses on SOM+ interneurons can explain the ramp acceleration after training. Altogether, our data reveal that local interneurons differentially control task-dependent ramping signals when MOs neurons integrate inputs preceding movement.

Keywords

frontal cortex
motor preparation
in vivo patch clamp
parvalbumin-expressing interneuron
somatostatin-expressing interneuron
virtual reality
go/no-go task

Data and code availability

  • All data reported in this paper will be shared by the lead contact upon request.

  • All original code has been deposited at Zenodo and is publicly available as of the date of publication. The DOI is listed in the Key resources table.

  • Any additional information required to reanalyze the data reported in this paper is available from the lead contact upon request.

Cited by (0)

7

These authors contributed equally

8

Present address: Neuroscience Institute, National Research Council (IN-CNR), Viale Giuseppe Colombo 3, 35131 Padua, Italy

9

Lead contact