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Abstract

Hippocampal ripples, brief high-frequency oscillations, occur during behavioral states that are not associated with active sensory processing. The ripple event represents a simultaneous burst of a large neuronal population that is synchronized across the entire hippocampus. Reactivation of neuronal ensembles that were active during learning predominantly occurs during ripples. The number of ripples is increased after learning and this increase is predictive for memory recall. Ripple suppression is unfavorable for memory consolidation. Ripples have been suggested to provide a neurophysiological substrate for ‘off-line’ memory consolidation by facilitating synaptic plasticity within the learning-associated neuronal ensembles. The neuronal activity in other brain regions that is time-locked to hippocampal ripples may underlie a cross-regional information transfer. We exploited the methodology allowing simultaneous extracellular recording combined with fMRI. An anesthetized rat was fixed in the MRI scanner and MRI-compatible linear electrode array was placed with electrode contacts in cortex, hippocampus, and thalamus using a custom-made movable drive. Spontaneous whole-brain BOLD activity was acquired along with multi-site electrophysiological recording. The ripple events were detected and classified off-line using a custom software. The time series of BOLD responses were extracted for each voxel according to the event-triggered design, where the ripple onset was used as an event, and the statistical maps were generated indicating the voxels with positive and negative BOLD responses. The voxels were subsequently grouped according to the anatomical brain regions by co-registration of the functional images with the digital rat brain atlas. The positive BOLD response was detected within the direct proximity to the ripple recording site in the CA1 region of hippocampus. The most of the hippocampal volume was also co-activated. In addition, a number of cortical regions including sensory and associative cortices contained a substantial proportion of voxels showing positive BOLD responses. Several brain regions consistently showed negative BOLD responses. These included many of the thalamic nuclei, neuromodulatory nuclei of the midbrain and brain stem and cerebellum. The fMRI findings were further confirmed by electrophysiological recordings in multiple brain areas. Our results identify a brain network that possibly supports hippocampal-dependent memory consolidation. Besides, hippocampal ripples may cause a transient inhibition within competing functional networks to enable more efficient intra brain region communication.