Multidimensional population activity in an electrically coupled inhibitory circuit in the cerebellar cortex

Inhibitory neurons orchestrate the activity of excitatory neurons and play key roles in circuit function. Although individual interneurons have been studied extensively, little is known about their properties at the population level. Using random-access 3D two-photon microscopy, we imaged local populations of cerebellar Golgi cells (GoCs), which deliver inhibition to granule cells. We show that population activity is organized into multiple modes during spontaneous behaviors. A slow, network-wide common modulation of GoC activity correlates with the level of whisking and locomotion, while faster (<1 s) differential population activity, arising from spatially mixed heterogeneous GoC responses, encodes more precise information. A biologically detailed GoC circuit model reproduced the common population mode and the dimensionality observed experimentally, but these properties disappeared when electrical coupling was removed. Our results establish that local GoC circuits exhibit multidimensional activity patterns that could be used for inhibition-mediated adaptive gain control and spatiotemporal patterning of downstream granule cells.

Automated summary

Inhibitory neurons, specifically cerebellar Golgi cells (GoCs), exhibit multidimensional activity patterns that could be utilized for inhibition-mediated adaptive gain control and spatiotemporal patterning. The activity of GoCs is organized into multiple modes during spontaneous behaviors, with a slow, network-wide modulation correlating with whisking and locomotion, and faster differential population activity encoding more precise information. Modeling these circuits demonstrated the importance of electrical coupling for maintaining these population activity patterns.