Awake reactivation of emotional memory traces through hippocampal-neocortical interactions

Neuroimage. 2016 Jul 1;134:563-572. doi: 10.1016/j.neuroimage.2016.04.026. Epub 2016 Apr 16.


Emotionally arousing experiences are typically well remembered not only due to immediate effects at encoding, but also through further strengthening of subsequent consolidation processes. A large body of research shows how neuromodulatory systems promote synaptic consolidation. However, how emotionally arousing experiences alter systems-level interactions, presumably a consequence of modifications at a synaptic level, remains unclear. Animal models predict that memory traces are maintained by spontaneous reactivations across hippocampal-neocortical circuits during "offline" periods such as post-learning rest, and suggest this might be stronger for emotional memories. The present study was designed to test this hypothesis in humans using functional Magnetic Resonance Imaging. Participants underwent a two-category localizer paradigm followed by a categorical differential delay fear conditioning paradigm interleaved with blocks of awake rest. Counterbalanced across participants, exemplars of one category (CS+), but not the other (CS-), were paired with mild electrical shocks. Fear recall (differential conditioned pupil dilation) was tested 24h later. Analyses of the localizer paradigm replicate earlier work showing category-specific response patterns in neocortical higher-order visual regions. Critically, we show that during post-learning rest, spontaneous reactivation of these neocortical patterns was stronger for the CS+ than the CS- category. Furthermore, hippocampal connectivity with the regions exhibiting these reactivations predicted strength of fear recall 24h later. We conclude that emotional arousal during learning promotes spontaneous post-learning reactivation of neocortical representations of recent experiences, which leads to better memory when coinciding with hippocampal connectivity. Our findings reveal a systems-level mechanism that may explain the persistence of long-term memory for emotional experiences.

Keywords: Amygdala; Arousal; Fear conditioning; Hippocampus; Representational similarity analysis; Resting-state functional connectivity.

MeSH terms

  • Adult
  • Brain Mapping
  • Conditioning, Classical
  • Electroshock
  • Emotions*
  • Fear
  • Female
  • Hippocampus / physiology*
  • Humans
  • Magnetic Resonance Imaging
  • Male
  • Mental Recall / physiology*
  • Neocortex / physiology*
  • Neural Pathways / physiology
  • Rest
  • Young Adult