Neuron
Volume 107, Issue 2, 22 July 2020, Pages 283-291.e6
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Hippocampal Network Reorganization Underlies the Formation of a Temporal Association Memory

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Highlights

  • Population activity in hippocampal CA1 was studied during trace fear conditioning

  • CA1 does not generate persistent activity to bridge the “trace” delay period

  • Neurons encoding the CS during cue and trace periods emerge with learning

  • Neural activity is temporally variable but predicts CS identity over longer periods

Summary

Episodic memory requires linking events in time, a function dependent on the hippocampus. In “trace” fear conditioning, animals learn to associate a neutral cue with an aversive stimulus despite their separation in time by a delay period on the order of tens of seconds. But how this temporal association forms remains unclear. Here we use two-photon calcium imaging of neural population dynamics throughout the course of learning and show that, in contrast to previous theories, hippocampal CA1 does not generate persistent activity to bridge the delay. Instead, learning is concomitant with broad changes in the active neural population. Although neural responses were stochastic in time, cue identity could be read out from population activity over longer timescales after learning. These results question the ubiquity of seconds-long neural sequences during temporal association learning and suggest that trace fear conditioning relies on mechanisms that differ from persistent activity accounts of working memory.

Keywords

hippocampus
memory
learning
trace fear conditioning
calcium imaging
population coding

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