The reuniens nucleus of the thalamus facilitates hippocampo-cortical dialogue during sleep

• Published in: eLife Vol. 12
• Main Authors: Basha, Diellor, Azarmehri, Amirmohammad, Proulx, Elian, Chauvette, Sylvain, Ghorbani, Maryam, Timofeev, Igor
• Format: Journal Article
• Language: English
• Published: England eLife Sciences Publications Ltd 06.03.2025; eLife Sciences Publications, Ltd
• Subjects: Animals; cat; Cats; Electrical stimuli; Electrophysiological recording; Hippocampus; Hippocampus - physiology; interregional synchrony; Intracellular; Male; Memory; Midline Thalamic Nuclei - physiology; Neocortex; Neural networks; Neural Pathways - physiology; Neurons; Neuroscience; NREM sleep; Oscillations; phase amplitude coupling; Prefrontal cortex; Prefrontal Cortex - physiology; REM sleep; sharp wave-ripples; Sleep; Sleep - physiology; slow waves; spindles; Synaptic strength; Thalamus; Topography; slow waves; spindles; neuroscience; phase amplitude coupling; cat; interregional synchrony; sharp wave-ripples
• ISSN: 2050-084X; 2050-084X
• DOI: 10.7554/eLife.90826

Memory consolidation during sleep depends on the interregional coupling of slow waves, spindles, and sharp wave-ripples (SWRs), across the cortex, thalamus, and hippocampus. The reuniens nucleus of the thalamus, linking the medial prefrontal cortex (mPFC) and the hippocampus, may facilitate interregional coupling during sleep. To test this hypothesis, we used intracellular, extracellular unit and local field potential recordings in anesthetized and head restrained non-anesthetized cats as well as computational modelling. Electrical stimulation of the reuniens evoked both antidromic and orthodromic intracellular mPFC responses, consistent with bidirectional functional connectivity between mPFC, reuniens and hippocampus in anesthetized state. The major finding obtained from behaving animals is that at least during NREM sleep hippocampo-reuniens-mPFC form a functional loop. SWRs facilitate the triggering of thalamic spindles, which later reach neocortex. In return, transition to mPFC UP states increase the probability of hippocampal SWRs and later modulate spindle amplitude. During REM sleep hippocampal theta activity provides periodic locking of reuniens neuronal firing and strong crosscorrelation at LFP level, but the values of reuniens-mPFC crosscorrelation was relatively low and theta power at mPFC was low. The neural mass model of this network demonstrates that the strength of bidirectional hippocampo-thalamic connections determines the coupling of oscillations, suggesting a mechanistic link between synaptic weights and the propensity for interregional synchrony. Our results demonstrate the presence of functional connectivity in hippocampo-thalamo-cortical network, but the efficacy of this connectivity is modulated by behavioral state.