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Abstract

Learning and memory are system properties emerging from the concerted operations of micro- and macro networks at multiple levels of the brain. The consolidation of declarative memory – that entirely depends on hippocampus - is long thought to occur during the slow wave sleep (SWS) by means of the reactivation of neural representations that were temporally stored in hippocampus during the awake state. A large number of studies have suggested that the
behavior-dependent electrical changes in the hippocampus may travel back to the cortex by means of the so-called sharp-wave ripple (SPW-R) events. Until recently we had no information related to the effects of SPW-R bursts on different structures of the brain. We developed a new methodology, a neural event triggered BOLD fMRI NET-fMRI), allowing to relate the local brain activity at a recording site to activity in other brain regions, and applied it for mapping brain activity associated with SPW-Rs in non-human primates and rats. We showed that SPW-Rs were tightly associated with robust cortical activations that occur concurrently with extensive activity suppression in subcortical thalamic, associational (e.g. basal ganglia, cerebellum), and midbrain-brainstem neuromodulatory centers. Suppression of thalamic activity might be a strategy that could increase the signal-to-noise ratio of hippocampal-cortical communication. Strong inhibition of the associational subcortical brain structures that are closely involved in the mechanisms of associative learning, such as the basal ganglia and the cerebellar cortex may indicate competition between the fundamentally distinct memory systems. A competition between the hippocampal and pontine regions may similarly reflect antagonistic interactions between procedures related to the
redistribution of hippocampal memory traces during SWS (network plasticity), and those occurring during REM (rapid eye movement) sleep phase and involving local increases in plasticity related immediate early gene activity favoring the subsequent synaptic consolidation (local plasticity) in the cortex. The latter procedure, taking place during high cholinergic and theta activity, is associated with the Pontine-Geniculate-Occipital (PGO) waves that are characteristic markers of REM sleep. Thus, NET-fMRI methodology may ultimately reveal the network states
that possibly underlie various behaviors and cognitive functions.