Spatial Learning Drives Rapid Goal Representation in Hippocampal Ripples without Place Field Accumulation or Goal-Oriented Theta Sequences

Abstract

The hippocampus is critical for rapid acquisition of many forms of memory, although the circuit-level mechanisms through which the hippocampus rapidly consolidates novel information are unknown. Here, the activity of large ensembles of hippocampal neurons in adult male Long-Evans rats was monitored across a period of rapid spatial learning to assess how the network changes during the initial phases of memory formation and retrieval. In contrast to several reports, the hippocampal network did not display enhanced representation of the goal location via accumulation of place fields or elevated firing rates at the goal. Rather, population activity rates increased globally as a function of experience. These alterations in activity were mirrored in the power of the theta oscillation and in the quality of theta sequences, without preferential encoding of paths to the learned goal location. In contrast, during brief "offline" pauses in movement, representation of a novel goal location emerged rapidly in ripples, preceding other changes in network activity. These data demonstrate that the hippocampal network can facilitate active navigation without enhanced goal representation during periods of active movement, and further indicate that goal representation in hippocampal ripples before movement onset supports subsequent navigation, possibly through activation of downstream cortical networks.

Neuronal signature of spatial decision-making during navigation by freely moving rats by using calcium imaging

“…Spatial recency within a well-learned context can be encoded and accessed remarkably fast. These observations complement those in another report, which was published while this manuscript was in preparation, to the effect that hippocampal representations can emerge after only a limited number of trials ( 48 ).…”

“…These observations of spatially predictive activity collectively support findings that suggest that prospective coding could be used to guide future behavior ( 48 , 49 ). While some authors have proposed this, other reports have argued that replay may rather reflect past memory, as past trajectories seem to be overrepresented in reward-switch tasks ( 19 ).…”

Bidirectional synaptic changes in deep and superficial hippocampal neurons followingin vivoactivity

“…When we quantified the rates of participation of deep and superficial cells in pre-experience SWRs, we observed no significant difference between the two populations (Figure 4 D). However, following exploration of the linear track, participation rates were elevated for both deep and superficial neurons, consistent with an experience-driven increase in overall hippocampal network activity 58–60 (Figure 4 D). Importantly, the experience-dependent increase in participation was significantly stronger for superficial neurons than for deep neurons (Figure 4 D).…”

Hippocampal representations of foraging trajectories depend upon spatial context

“…Neuronal ensembles active in SPEs tended to be recruited during execution of navigational and non-navigational forelimb trajectories (Extended Data Fig. 6 ); however, there was substantial variance in this relationship, and SPE ensembles could also contain additional information about the trajectory critical for learning (such as in ‘non-replay’ events 52 ). Moreover, in the NTF task, ensembles recruited during the trajectory were insufficient to decode kinematics, suggesting that additional information in SPE ensembles might be critical.…”