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Abstract

retention of previously acquired awake experience. Although hippocampal ripples have been studied in detail using neurophysiological methods, the global effects of ripples on the entire brain remain elusive, primarily owing to a lack of methodologies permitting concurrent hippocampal recordings and whole-brain activity mapping. By combining electrophysiological recordings in hippocampus with ripple-triggered functional magnetic resonance imaging, here we show that most of the cerebral cortex is selectively activated during the ripples, whereas most diencephalic, midbrain and brainstem regions are strongly and consistently inhibited. Analysis of regional temporal response patterns indicates that thalamic activity suppression precedes the hippocampal population burst, which itself is temporally bounded by massive activations of association and primary cortical areas. These findings suggest that during off-line memory consolidation, synergistic thalamocortical activity may be orchestrating a privileged interaction state between hippocampus and cortex by silencing the output of subcortical centers involved in sensory processing or potentially mediating procedural learning. Several clinical studies, have demonstrated the phase-dependent synergistic or antagonistic relationship between the neural structures related to declarative and non-declarative (e.g. procedural) memory; Yet our observation demonstrates for the first time that such antagonistic relationship may exist during the “consolidation phase of long-term memory. The down regulation evidently generates conditions of minimal interference between subsystems, enabling consolidation of hippocampus-dependent memory. Importantly, neither the activation maps nor the sequences of up and down-regulation should be thought of indicating a causal relationship between the trigger event and the network activity changes. The state of widespread networks probably depends on a large number of variables (for example, activity changes in individual structures, or changes in inter-structure correlations), a subset of which may be eventually characterized following intensive future experimentation. The outcome of each experimental session may be conceived