Striatal cholinergic interneuron membrane voltage tracks locomotor rhythms in mice

Rhythmic neural network activity has been broadly linked to behavior. However, it is unclear how membrane potentials of individual neurons track behavioral rhythms, even though many neurons exhibit pace-making properties in isolated brain circuits. To examine whether single-cell voltage rhythmicity is coupled to behavioral rhythms, we focused on delta-frequencies (1-4 Hz) that are known to occur at both the neural network and behavioral levels. We performed membrane voltage imaging of individual striatal neurons simultaneously with network-level local field potential recordings in mice during voluntary movement. We report sustained delta oscillations in the membrane potentials of many striatal neurons, particularly cholinergic interneurons, which organize spikes and network oscillations at beta-frequencies (20-40 Hz) associated with locomotion. Furthermore, the delta-frequency patterned cellular dynamics are coupled to animals' stepping cycles. Thus, delta-rhythmic cellular dynamics in cholinergic interneurons, known for their autonomous pace-making capabilities, play an important role in regulating network rhythmicity and movement patterning. Behaviorally relevant neural rhythms have been mainly studied at the neural population level. Here, the authors show that subthreshold membrane voltage delta-frequency oscillations in individual striatal cholinergic neurons modulate spike timing, striatal network beta rhythmicity, and track patterned stepping movement.

Automated summary

This study demonstrates that the membrane potentials of striatal cholinergic neurons exhibit sustained delta-frequency oscillations, which are coupled to animals' stepping cycles and regulate network rhythmicity and movement patterning.