Neocortical inhibitory imbalance predicts successful sensory detection

Cell Rep. 2024 Jul 23;43(7):114233. doi: 10.1016/j.celrep.2024.114233. Epub 2024 Jun 20.

Abstract

Perceptual success depends on fast-spiking, parvalbumin-positive interneurons (FS/PVs). However, competing theories of optimal rate and correlation in pyramidal (PYR) firing make opposing predictions regarding the underlying FS/PV dynamics. We addressed this with population calcium imaging of FS/PVs and putative PYR neurons during threshold detection. In primary somatosensory and visual neocortex, a distinct PYR subset shows increased rate and spike-count correlations on detected trials ("hits"), while most show no rate change and decreased correlations. A larger fraction of FS/PVs predicts hits with either rate increases or decreases. Using computational modeling, we found that inhibitory imbalance, created by excitatory "feedback" and interactions between FS/PV pools, can account for the data. Rate-decreasing FS/PVs increase rate and correlation in a PYR subset, while rate-increasing FS/PVs reduce correlations and offset enhanced excitation in PYR neurons. These findings indicate that selection of informative PYR ensembles, through transient inhibitory imbalance, is a common motif of optimal neocortical processing.

Keywords: CP: Neuroscience.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials / physiology
  • Animals
  • Female
  • Interneurons* / metabolism
  • Interneurons* / physiology
  • Male
  • Mice
  • Neocortex* / physiology
  • Neural Inhibition / physiology
  • Parvalbumins / metabolism
  • Pyramidal Cells* / metabolism
  • Pyramidal Cells* / physiology

Substances

  • Parvalbumins