ABSTRACT
The retrosplenial cortex (RSC) is essential for successful memory formation and spatial navigation. However, the rate and temporal coding schemes employed by the RSC to achieve these functions remain a mystery, and no biophysically realistic computational models of RSC cells yet exist. To understand the computational principles underlying RSC function, here we systematically characterize the intrinsic physiology and local connectivity of neurons in the superficial layers of the retrosplenial granular cortex (RSG). We show that the most prominent cell type in layers 2/3 of the RSG is a hyperexcitable, small pyramidal cell. These cells have a low rheobase (LR), high input resistance, lack of spike-frequency adaptation, and spike widths that are intermediate to those of neighboring fast-spiking (FS) inhibitory neurons and regular-spiking (RS) excitatory neurons. Using paired whole-cell recordings, we show, for the first time, that these LR cells are excitatory. However, they rarely synapse onto neighboring L2/3 neurons, exciting only 17% of FS cells and 0% of other L2/3 LR or RS cells. Instead, their axons head to deeper layers and towards the corpus callosum, likely targeting contralateral RSC. LR cells receive dominant inhibition from neighboring FS cells, with FS cells inhibiting over 52% of LR cells. Given the sparsity of reciprocal LR to FS connections, this inhibition is more likely to serve a feedforward, rather than feedback, role. In terms of rhythmic computations, this also means that the superficial RSG circuit may not employ the standard rules of pyramidal-interneuron gamma (PING) generation. Our results suggest that the retrosplenial cortex uses unique coding schemes that balance hyperexcitable excitatory neurons capable of sustained long-duration firing with dominant feedforward inhibitory control.