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Abstract

Hippocampal sharp wave-ripple complexes (SPW-Rs) have been postulated to be involved in hippocampal-cortical information transfer underlying declarative memory consolidation. Our recent neural event-triggered fMRI study showed that occurrence of SPW-Rs was associated with activity suppression in a number of subcortical regions, including thalamus. Description of such specific activation/deactivation pattern of the whole-brain activity associated with SPW-Rs extended the predominant view on the SPW-Rs as indicators of hippocampal-cortical functional connectivity, and SPW-R has been suggested to indicate a global network state supporting declarative memory. The midline thalamic nuclei have been implicated to play a role for learning and memory. However, it remains unexplored how thalamic neural activity contributes to hippocampal-cortical dialogue. The medial dorsal nucleus of thalamus (MD) receives input from the entorhinal cortex and is reciprocally connected with the prefrontal cortex (PFC). The MD anatomical connectivity combined with the results of MD lesion studies suggested a critical role of MD for associative and mnemonic functions. In the present study, we characterized MD neural activity associated with hippocampal SPW-Rs. We performed simultaneous extracellular electrophysiological recordings in MD and hippocampus in urethane-anesthetized and behaving rats. We then examined the firing rate modulation of the MD single units (n = 151) around SPW-Rs. Nearly half of MD single units (46.4) showed the firing rate inhibition at times of SPW-R occurrence. Moreover, about 37 (26 of 70) of this MD population decreased their firing at least ~1s prior the SPW-R onset. Similar dynamics was observed for MD multiunit activity and gamma-power during rat spontaneous behavior. Our results suggest that MD inhibition plays a permissive role for initiating SPW-R-associated information transfer underlying ‘off-line’ memory consolidation.