Differential Relation between Neuronal and Behavioral Discrimination during Hippocampal Memory Encoding

Abstract

Summary How are distinct memories formed and used for behavior? To relate neuronal and behavioral discrimination during memory formation, we use in vivo 2-photon Ca 2+ imaging and whole-cell recordings from hippocampal subregions in head-fixed mice performing a spatial virtual reality task. We find that subthreshold activity as well as population codes of dentate gyrus neurons robustly discriminate across different spatial environments, whereas neuronal remapping in CA1 depends on the degree of difference between visual cues. Moreover, neuronal discrimination in CA1, but not in the dentate gyrus, reflects behavioral performance. Our results suggest that CA1 weights the decorrelated information from the dentate gyrus according to its relevance, producing a map of memory representations that can be used by downstream circuits to guide learning and behavior.

Distinct place cell dynamics in CA1 and CA3 encode experience in new environments

“…Rather than a deterioration in the memory representation of the environment, such remapping may serve a function and has been proposed to encode distinct episodes that occur in the same environment separated by time or small changes in environment 10,37,39,41,59-63 . This remapping might therefore allow the animal to create independent representations of different episodes associated with the same environment and favor mnemonic discrimination of those episodes 64,65 . Our data support this idea as the average PF correlation in CA1 across days in a novel environment was 0.49 ± 0.02 (see methods) revealing considerable remapping across days (Fig.…”

A synaptic novelty signal to switch hippocampal attractor networks from generalization to discrimination

“…Animals were ‘teleported’ back to the beginning of the track upon crossing of a defined threshold near the end of the virtual corridor. As the virtual environments, training protocol and reward contingencies used in this study are different from the ones used in previous work 12 , the hit rate results are not directly comparable. After having completed the five-day training protocol in the familiar environment, a behavioral recording session was conducted in which laps in the familiar environment (F) were alternated with laps in the novel environment 1 (N1).…”

“…Electrodes were arranged to penetrate the brain tissue perpendicularly to the cortical surface at the center of the craniotomy and the depth of the recorded cell was estimated from the distance advanced with the micromanipulator (Luigs & Neuman), taking as a reference the point where the recording electrode made contact with the cortical surface. Whole-cell patch-clamp recordings were obtained using a standard blind-patch approach, as previously described 12,26,84 . Only recordings with a seal resistance > 1 GΩ were included in the analysis.…”

“…Some of the recordings included in the present study have also been used for previous work 12 , where the specificity of subthreshold responses for the familiar and novel environments was analyzed.…”

“…To address this question, we obtained in vivo whole-cell patch-clamp recordings from granule cells of the dentate gyrus in head-fixed mice navigating in familiar and novel virtual environments 12,26 . We report that dentate gyrus granule cells consistently show a task-dependent small and transient depolarization of their membrane potential when an animal encounters a novel environment.…”