The retrosplenial cortex (RSC) is a cortical area that connects various brain regions and relays diverse neural information. Based on its unique connectivity, the RSC has been reported to be involved in a range of cognitive functions, including spatial navigation, episodic memory, sensory information processing and imagination of future events (Vann et al., 2003; Vann et al., 2009; Czajkowski et al., 2014). Recent studies suggested that the RSC communicates hippocampal information to the neocortex during sharp-wave ripples (SWRs), highly synchronous oscillatory events associated with memory consolidation during behavioral immobility and non-REM sleep (Nitzan et al., 2020; Opalka et al., 2020). However, the basic electrophysiological nature of RSC neurons remains to be elucidated.
Here, we report a unique form of short-term intrinsic plasticity in mouse granular RSC (gRSC) layer 2/3 (L2/3) pyramidal cells. These cells exhibited a late-spiking firing feature, i.e. slowly ramping depolarization and considerably delayed spikes, in response to step current injections into the soma, but the spike timing became earlier when a preceding brief depolarizing current (priming) was injected. According to our experiments, this self-sensitizing priming effect could last for more than 3 s, which possibly provides a time window for increased sensitivity to gRSC inputs. This facilitatory effect induced by the priming was uniquely detected in gRSC L2/3; in the four other types of pyramidal cells we have tested, the priming effect was in contrast to that observed in gRSC L2/3 neurons. By performing in vitro and in vivo patch-clamp recordings following optogenetic activation of axonal fibers on gRSC L2/3, we found that the preceding stimulation of subicular but not gRSC L5 afferents replicated the facilitatory priming effect. These results indicate that subicular inputs to gRSC layer 2/3 neurons may play a role in the modulation of subsequent information integration in the RSC circuit.