Hyperexcitable Neurons Enable Precise and Persistent Information Encoding in the Superficial Retrosplenial Cortex

The retrosplenial cortex (RSC) is essential for memory and navigation, but the neural codes underlying these functions remain largely unknown. Here, we show that the most prominent cell type in layers 2/3 (L2/3) of the mouse granular RSC is a hyperexcitable, small pyramidal cell. These cells have a low rheobase (LR), high input resistance, lack of spike frequency adaptation, and spike widths intermediate to those of neighboring fast-spiking (FS) inhibitory neurons and regular-spiking (RS) excitatory neurons. LR cells are excitatory but rarely synapse onto neighboring neurons. Instead, L2/3 is a feedforward, not feedback, inhibition-dominated network with dense connectivity between FS cells and from FS to LR neurons. Biophysical models of LR but not RS cells precisely and continuously encode sustained input from afferent postsubicular head-direction cells. Thus, the distinct intrinsic properties of LR neurons can support both the precision and persistence necessary to encode information over multiple timescales in the RSC. [Display omitted] •Two distinct subtypes of excitatory neurons in superficial retrosplenial cortex (RSC)•Most common neuron in layer 2/3 of RSC is excitatory low-rheobase (LR) neuron•LR intrinsic properties enable precise, sustained encoding of information•Layer 2/3 of RSC is dominated by feedforward, not feedback, inhibition The retrosplenial cortex is critical for navigation and memory, but the underlying neural codes remain unclear. Here, Brennan et al. identify a distinct, prominent excitatory neuron whose intrinsic properties enable sustained encoding of head direction inputs. Their neuronal connectivity map reveals a retrosplenial circuit dominated by feedforward, not feedback, inhibition.