Awake reactivation of emotional memory traces through hippocampal-neocortical interactions.
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.
Donders Institute for Brain, Cognition and Behaviour, Radboud university medical center, 6500 HB, Nijmegen, The Netherlands; Department for Cognitive Neuroscience, Radboud university medical center, 6500 HB, Nijmegen, The Netherlands. Electronic address: l.devoogd@donders.ru.nl.
Lycia D
LD
de Voogd
Donders Institute for Brain, Cognition and Behaviour, Radboud university medical center, 6500 HB, Nijmegen, The Netherlands; Department for Cognitive Neuroscience, Radboud university medical center, 6500 HB, Nijmegen, The Netherlands.
Guillén
G
Fernández
Donders Institute for Brain, Cognition and Behaviour, Radboud university medical center, 6500 HB, Nijmegen, The Netherlands; Department for Cognitive Neuroscience, Radboud university medical center, 6500 HB, Nijmegen, The Netherlands.
Erno J
EJ
Hermans
D000328:Adult; D001931:Brain Mapping; D003214:Conditioning, Classical; D004597:Electroshock; D004644:Emotions; D005239:Fear; D005260:Female; D006624:Hippocampus / Q000502:physiology*; D006801:Humans; D008279:Magnetic Resonance Imaging; D008297:Male; D011939:Mental Recall / Q000502:physiology*; D019579:Neocortex / Q000502:physiology*; D009434:Neural Pathways / Q000502:physiology; D012146:Rest; D055815:Young Adult
Amygdala; Arousal; Fear conditioning; Hippocampus; Representational similarity analysis; Resting-state functional connectivity