Trajectory-modulated hippocampal neurons persist throughout memory-guided navigation

Nathaniel R Kinsky,Samuel J Levy,Michael E Hasselmo,William Mau,David W Sullivan,Evan A Ruesch

doi:10.1038/s41467-020-16226-4

Abstract

Trajectory-dependent splitter neurons in the hippocampus encode information about a rodent’s prior trajectory during performance of a continuous alternation task. As such, they provide valuable information for supporting memory-guided behavior. Here, we employed single-photon calcium imaging in freely moving mice to investigate the emergence and fate of trajectory-dependent activity through learning and mastery of a continuous spatial alternation task. In agreement with others, the quality of trajectory-dependent information in hippocampal neurons correlated with task performance. We thus hypothesized that, due to their utility, splitter neurons would exhibit heightened stability. We find that splitter neurons were more likely to remain active and retained more consistent spatial information across multiple days than other neurons. Furthermore, we find that both splitter neurons and place cells emerged rapidly and maintained stable trajectory-dependent/spatial activity thereafter. Our results suggest that neurons with useful functional coding exhibit heightened stability to support memory guided behavior.

Highlights

Trajectory-dependent splitter neurons in the hippocampus encode information about a rodent’s prior trajectory during performance of a continuous alternation task
How does the level of trajectory-dependent information within the hippocampus correlate with behavioral performance? Second, given the steady evolution of hippocampus activity patterns across days[21,22,23,24], do splitter neurons remain part of the active population longer than other cells, providing a longer lasting memory or planning signal to guide behavior? Third, once a neuron establishes trajectory-dependent activity, is it less prone to remapping than other neurons? These questions are relevant since trajectory-dependent activity has been observed in other tasks[25,26,27] and could be employed more generally by the hippocampus to guide the appropriate behavior based on environmental cues[28]
We first tallied the onset day of splitter neurons and place cells. While both place cells and splitter neurons were present from day 1 and continued to come online throughout the experiment (Fig. 7a, b), the bulk of place cells were recruited on day 1

Summary

Introduction

Trajectory-dependent splitter neurons in the hippocampus encode information about a rodent’s prior trajectory during performance of a continuous alternation task As such, they provide valuable information for supporting memory-guided behavior. The ability of hippocampal neurons to maintain the same firing location in the absence of learning might support long-term memory retrieval In support of this idea, a recent study illustrated that neurons with place fields located near a hidden goal were more stable over time than cells with fields in other locations[19]. Two other experiments found that increasing rodents’ attention to a task selectively heightened stability in neurons that encoded task-relevant features[8,20] These studies, along with the finding that place cells with fields in close proximity to a goal location exhibit heightened activity in post-learning sleep[18], suggest that the utility of a neuron’s information to task performance influences its long-term stability. We found that some attributes of trajectory-dependent coding correlate with task performance

Methods

Results

Conclusion