Thalamus and claustrum control parallel layer 1 circuits in retrosplenial cortex

The granular retrosplenial cortex (RSG) is critical for both spatial and non-spatial behaviors, but the underlying neural codes remain poorly understood. Here, we use optogenetic circuit mapping in mice to reveal a double dissociation that allows parallel circuits in superficial RSG to process disparate inputs. The anterior thalamus and dorsal subiculum, sources of spatial information, strongly and selectively recruit small low-rheobase (LR) pyramidal cells in RSG. In contrast, neighboring regular-spiking (RS) cells are preferentially controlled by claustral and anterior cingulate inputs, sources of mostly non-spatial information. Precise sublaminar axonal and dendritic arborization within RSG layer 1, in particular, permits this parallel processing. Observed thalamocortical synaptic dynamics enable computational models of LR neurons to compute the speed of head rotation, despite receiving head direction inputs that do not explicitly encode speed. Thus, parallel input streams identify a distinct principal neuronal subtype ideally positioned to support spatial orientation computations in the RSG.

Automated summary

The granular retrosplenial cortex in mice plays a crucial role in spatial orientation computations, with parallel circuits processing inputs from different sources to support these computations. Small low-rheobase pyramidal cells in the superficial RSG are involved in processing spatial information, while neighboring regular-spiking cells are more responsive to non-spatial information, showing a distinct principal neuronal subtype in the RSG.