Abstract
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.
Highlights
Beginning with the theoretical work of Marr (1971), the idea that hippocampal-neocortical interactions during slow-wave sleep (SWS) play an important role in the process of systems memory consolidation has become a dominant paradigm in memory research (Buzsaki, 1989; McClelland et al, 1995; Wilson and McNaughton, 1994)
Having observed that neocortical regions are strongly modulated around sharp-wave ripples (SWR), we investigated whether the reverse is the case, that is Does ripple power increase when strong activations take place in a given neocortical region? To address this question, the ripple power traces centered on peak activations in each neocortical pixel were averaged and compared across neocortical subnetworks (Figure 1E)
It is important to have a functional map of peri-SWR neocortical activity during sleep, which could inform our search for neocortical regions engaged in memory consolidation
Summary
Beginning with the theoretical work of Marr (1971), the idea that hippocampal-neocortical interactions during slow-wave sleep (SWS) play an important role in the process of systems memory consolidation has become a dominant paradigm in memory research (Buzsaki, 1989; McClelland et al, 1995; Wilson and McNaughton, 1994) This idea is supported by observations of replay of recently active neural ensemble patterns in hippocampus (Kudrimoti et al, 1999; Nadasdy et al, 1999; Pavlides and Winson, 1989; Skaggs and McNaughton, 1996; Wilson and McNaughton, 1994) and neocortex (Euston et al, 2007; Hoffman and McNaughton, 2002; Ji and Wilson, 2007; Jiang et al, 2017; Qin et al, 1997), a key role of SWS in enabling structural rearrangements of neocortical synaptic connections (Yang et al, 2014), and effects of interruptions of SWS on memory (Gais et al, 2007).
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