Abstract
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.
Highlights
The retrosplenial cortex (RSC) plays a critical role in learning and memory
There is prevalent local inhibition from fast-spiking (FS) layers 2/3 (L2/3) neurons onto these highly excitable neurons and between pairs of FS cells, highlighting a network dominated by feedforward, not feedback, inhibition. We use this information to construct biophysically realistic computational models of RSC cell types and investigate how they process realistic, in vivo spike trains of incoming information. We find that these hyperexcitable principal neurons in the RSG are optimally suited to precisely and persistently encode the sustained head direction (HD) input they receive from the postsubiculum
For reasons investigated and explained below, we refer to these distinct neurons as low-rheobase (LR) cells
Summary
The retrosplenial cortex (RSC) plays a critical role in learning and memory. In humans, damage to the RSC results in both anterograde and retrograde amnesia, often purging several years of recent memories (Ironside and Guttmacher, 1929; Heilman and Sypert, 1977; Valenstein et al, 1987; Todd and Bucci, 2015; Chrastil, 2018). Human case studies show that RSC damage leads to disorientation in space in addition to memory impairments (Bottini et al, 1990; Takahashi et al, 1997; Ino et al, 2007; Osawa et al, 2007) Such patients can identify known scenes or locations but are unable to extract any orientation information from them and, experience difficulties navigating even familiar environments (Bottini et al, 1990; Takahashi et al, 1997; Ino et al, 2007). Similar to excitatory background inputs, inhibitory inputs were simulated at a frequency of 5 Hz and reversal potential of À80 mV ðEGABAÞ
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