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.