Department of Electrical Engineering and Computer Science, University of California, Irvine, United States; Medical Scientist Training Program, University of California, Irvine, United States
Canadian Centre for Behavioral Neuroscience, University of Lethbridge, Lethbridge, Canada
Artur Luczak
Canadian Centre for Behavioral Neuroscience, University of Lethbridge, Lethbridge, Canada
Bruce L McNaughton
Canadian Centre for Behavioral Neuroscience, University of Lethbridge, Lethbridge, Canada; Department of Neurobiology and Behavior, University of California, Irvine, United States
A prevalent model is that sharp-wave ripples (SWR) arise ‘spontaneously’ in CA3 and propagate recent memory traces outward to the neocortex to facilitate memory consolidation there. Using voltage and extracellular glutamate transient recording over widespread regions of mice dorsal neocortex in relation to CA1 multiunit activity (MUA) and SWR, we find that the largest SWR-related modulation occurs in retrosplenial cortex; however, contrary to the unidirectional hypothesis, neocortical activation exhibited a continuum of activation timings relative to SWRs, varying from leading to lagging. Thus, contrary to the model in which SWRs arise ‘spontaneously’ in the hippocampus, neocortical activation often precedes SWRs and may thus constitute a trigger event in which neocortical information seeds associative reactivation of hippocampal ‘indices’. This timing continuum is consistent with a dynamics in which older, more consolidated memories may in fact initiate the hippocampal-neocortical dialog, whereas reactivation of newer memories may be initiated predominantly in the hippocampus.