Experience‐dependent recruitment of Arc expression in multiple systems during rest

Abstract

The patterns of ensemble activity in the hippocampal formation during wakeful, attentive behavior are recapitulated during subsequent resting states. This replay of activity has also been found in several brain regions across many species, indicating a very general biological phenomenon. Concomitantly, transcription of immediate-early genes (IEGs) such as Arc also reoccurs in the same hippocampal neurons, suggesting that IEGs contribute to "off-line" consolidation. If continued IEG expression during rest reflects a correlate of ensemble replay, then the same generality should be observed in IEG transcription patterns. This hypothesis was tested by examining Arc in F344 rats engaging in spatial exploration alongside a rest episode. The probability that an individual neuron participates in "constitutive" Arc expression during rest is increased by recent experience in multiple cortical regions as well as across the septal and temporal poles of the hippocampus, consistent with memory trace reactivation. That is, neurons that were recently active during spatial exploration are preferentially recruited into further Arc expression during subsequent rest. The continued Arc expression, however, occurs in only a small fraction of the cells that were engaged in transcription during previous behavior. This fraction is greatest in CA3 and progressively decreases in CA1, superficial, and deep cortical layers and is consistent with the idea that consolidation occurs rapidly in the hippocampus (centering on the CA3 recurrent network) while changes are much more gradual in neocortical synaptic networks.