Specific hippocampal representations are linked to generalized cortical representations in memory

Abstract

SummaryMemories link information about specific experiences to more general knowledge that is abstracted from and contextualizes those experiences, but how neuronal activity patterns support this link is not known. Here we show that during memory reactivation in a foraging task with multiple spatial paths, specific hippocampal place representations are concurrently and preferentially reactivated with a subset of prefrontal cortical task representations that generalize across different paths. This link between specific and general representations may serve as a neural substrate for abstraction and task guidance in mammals.

Canonical goal-selective representations are absent from prefrontal cortex in a spatial working memory task requiring behavioral flexibility

“…Finally, our results suggest a role for mPFC in working memory tasks by representing task structure in terms of groups of behaviorally related elements (Jung et al, 1998;Yu et al, 2018;Kaefer et al, 2020), consistent with findings that the PFC forms long-term memories of learned stimulus categories (Freedman et al, 2001). Each trial consisted of the following steps: (1) the current goal is randomly assigned and cued with lights; a single, randomly assigned route (bridge) is available; rat gets small reward upon arrival at cued goal; (2) animal returns to center via any route; all routes are blocked upon arrival at center;…”

The hippocampal sharp wave–ripple in memory retrieval for immediate use and consolidation

“…Early in learning, hippocampal-PFC co-activity patterns during SWRs are correlated with co-activity during behaviour, suggesting a simple Hebbian association mechanism 159 . Later, once the environment and task are familiar, this relationship becomes much weaker 129 , with a subset of PFC neurons that encode general features of the environment and task showing more specific engagement during SWRs 171 . The resulting hippocampal-PFC co-activity preferentially links hippocampal activity patterns representing specific locations with cortical activity patterns that generalize across a set of locations.…”

Prefrontal cortical activity predicts the extra-place field spiking of hippocampal place cells

“…In order to understand the extent of isolated spiking during active behavior and to identify a potential function of this activity, we took an unbiased approach where we surveyed CA1 place cell spiking across all movement periods (animal speed >2cm/s) as animals performed a spatial navigation task (Yu, Kay et al 2017, Yu, Liu et al 2018) (Figure 1A-B, Figure S1). In the hippocampus the temporal structure of spiking during locomotion is strongly influenced by the endogenous ~8Hz theta rhythm (O’Keefe and Recce 1993), and bouts of higher rate spiking corresponding to place field traversals spanned multiple, adjacent cycles of theta (Fig.…”

“…Given the anatomical and functional connectivity between these regions, evidence of coordination between hippocampus and PFC would argue that these events are not the result of local noise in the hippocampus but instead reflect coherent and structured activity across brain regions. An example of such hippocampal-cortical engagement occurs during SWRs, where hippocampal reactivation is accompanied by the coordinated reactivation of cortical representations (Remondes and Wilson 2015, Jadhav, Rothschild et al 2016, Wang and Ikemoto 2016, Rothschild, Eban et al 2017, Yu, Kay et al 2017, Yu, Liu et al 2018). If such coordination is seen around the times of isolated spikes, we should be able to identify PFC neurons that spike differently around times of isolated activity in the hippocampus than at comparable periods where isolated spiking was not observed.…”