A comparison of hippocampal and retrosplenial cortical spatial and contextual firing patterns

Abstract

The hippocampus (HPC) and retrosplenial cortex (RSC) are key components of the brain's memory and navigation systems. Lesions of either region produce profound deficits in spatial cognition and HPC neurons exhibit well‐known spatial firing patterns (place fields). Recent studies have also identified an array of navigation‐related firing patterns in the RSC. However, there has been little work comparing the response properties and information coding mechanisms of these two brain regions. In the present study, we examined the firing patterns of HPC and RSC neurons in two tasks which are commonly used to study spatial cognition in rodents, open field foraging with an environmental context manipulation and continuous T‐maze alternation. We found striking similarities in the kinds of spatial and contextual information encoded by these two brain regions. Neurons in both regions carried information about the rat's current spatial location, trajectories and goal locations, and both regions reliably differentiated the contexts. However, we also found several key differences. For example, information about head direction was a prominent component of RSC representations but was only weakly encoded in the HPC. The two regions also used different coding schemes, even when they encoded the same kind of information. As expected, the HPC employed a sparse coding scheme characterized by compact, high contrast place fields, and information about spatial location was the dominant component of HPC representations. RSC firing patterns were more consistent with a distributed coding scheme. Instead of compact place fields, RSC neurons exhibited broad, but reliable, spatial and directional tuning, and they typically carried information about multiple navigational variables. The observed similarities highlight the closely related functions of the HPC and RSC, whereas the differences in information types and coding schemes suggest that these two regions likely make somewhat different contributions to spatial cognition.

The Retrosplenial Cortical Role in Delayed Spatial Alternation

“…Previous studies have documented the spatial firing properties of RSC neurons as rats traversed the maze during continuous alternation (Miller et al, 2019; Subramanian et al, 2024) and similar spatial firing patterns were observed here (see examples in Fig. 2A).…”

“…However, the range of lesion placement did not allow systematic examination of the role of individual subregions. Our previous studies of RSC neuronal firing patterns (Subramanian et al, 2024) suggest a distributed coding scheme with little evidence of specialization along the rostro-caudal extent of the RSC (but see Pothuizen et al, 2009; Trask et al, 2021; Van Groen et al, 2004).…”

“…Our previous study using a continuous (non-delayed) version of this T-maze task (Miller et al, 2019, Subramanian et al, 2024) found that RSC neuronal firing patterns differentiate left and right trials as the rats traverse the stem of the maze as well as the left and right reward locations. In the present study, we examined stem- and reward-related firing using the same strategy we employed for the delay period.…”

“…We binned the average firing rate into 200 msec bins for the entire duration of 30 sec delay, and then classified the neurons as having a putative go signal if their maximum firing rate during the final 2 sec of the delay period was at least 3 standard deviations above the mean of the entire delay period. The firing rate of some RSC neurons is strongly correlated with running speed or acceleration (Subramanian et al, 2024), which could cause an increase in firing at the start of the trial solely as a consequence of the rat’s locomotor behavior. After excluding these movement-sensitive neurons (see Methods), we found that 29% (42/144) of RSC neurons met our criteria for having a trial start signal (Fig.…”

“…A growing literature shows that RSC neurons exhibit a wide range of navigation-related firing patterns in rodents (e.g. Subramanian et al, 2024). These firing patterns carry information about the subject’s spatial location (Miller et al, 2019), head direction (Cho & Sharp, 2001; Jacob et al, 2017), routes and trajectories (Alexander & Nitz, 2015, 2017), environmental boundaries (Alexander et al, 2020), navigational cues (Vedder et al, 2017), and goal locations (Miller et al, 2019).…”