Rhythmic oscillations in the midbrain dopaminergic nuclei in mice

Front Cell Neurosci. 2023 Jun 23:17:1131313. doi: 10.3389/fncel.2023.1131313. eCollection 2023.

Abstract

Introduction: Dopamine release in the forebrain by midbrain ventral tegmental nucleus (VTA) and substantia nigra pars compacta (SNc) neurons is implicated in reward processing, goal-directed learning, and decision-making. Rhythmic oscillations of neural excitability underlie coordination of network processing, and have been reported in these dopaminergic nuclei at several frequency bands. This paper provides a comparative characterization of several frequencies of oscillations of local field potential and single unit activity, highlighting some behavioral correlates.

Methods: We recorded from optogenetically identified dopaminergic sites in four mice training in operant olfactory and visual discrimination tasks.

Results: Rayleigh and Pairwise Phase Consistency (PPC) analyses revealed some VTA/SNc neurons phase-locked to each frequency range, with fast spiking interneurons (FSIs) prevalent at 1-2.5 Hz (slow) and 4 Hz bands, and dopaminergic neurons predominant in the theta band. More FSIs than dopaminergic neurons were phase-locked in the slow and 4 Hz bands during many task events. The highest incidence of phase-locking in neurons was in the slow and 4 Hz bands, and occurred during the delay between the operant choice and trial outcome (reward or punishment) signals.

Discussion: These data provide a basis for further examination of rhythmic coordination of activity of dopaminergic nuclei with other brain structures, and its impact for adaptive behavior.

Keywords: 4 Hz; awake delta rhythm; slow rhythm; substantia nigra pars compacta; ventral tegmental area.

Grants and funding

This study was supported by grants from Uehara Memorial Foundation (to JM) and the Takeda Science Foundation (to JM and HN). Thanks to the Labex Memolife, Fondation Bettencourt Schueller, and International Research Project DALoops (Toyama University and CNRS) for the funding support.