Abstract: 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.

Abstract: The retrosplenial cortex is essential for spatial memory and navigation. We sought to learn about how the retrosplenial cortex encodes information through oscillations. Our experiment results reveal an oscillation pattern we call “splines”, resembling the similarly-named interlocking teeth on mechanical gears. Splines are 110-160 Hz, precisely coupled to the peaks of local theta rhythms, and observed during both REM sleep and active awake behaviors. We found that splines are distinct from gamma rhythms. While gamma rhythms are in-phase across the two retrosplenial hemispheres, splines are anti-phase across the hemispheres. By sorting theta cycles by either spline or gamma power, we show that retrosplenial splines and gamma oscillations occur independently of each other within any given theta cycle. Splines are also distinct from sharp wave ripples and alternate with sharp wave ripples across REM and NREM sleep, respectively. At higher running speeds, splines become more powerful, more strongly phase-amplitude coupled to theta, and have greater cross-hemispheric coherence. The retrosplenial cortex’s ability to rapidly switch between splines and gamma as distinct modes of rapid interhemispheric communication may allow this region to more effectively integrate information using two mechanistically distinct rhythms.