Sleep spindles mediate hippocampal-neocortical coupling during long-duration ripples

Sleep is pivotal for memory consolidation. According to two-stage accounts, memory traces are gradually translocated from hippocampus to neocortex during non-rapid-eye-movement (NREM) sleep. Mechanistically, this information transfer is thought to rely on interactions between thalamocortical spindles and hippocampal ripples. To test this hypothesis, we analyzed intracranial and scalp Electroencephalography sleep recordings from pre-surgical epilepsy patients. We first observed a concurrent spindle power increase in hippocampus (HIPP) and neocortex (NC) time-locked to individual hippocampal ripple events. Coherence analysis confirmed elevated levels of hippocampal-neocortical spindle coupling around ripples, with directionality analyses indicating an influence from NC to HIPP. Importantly, these hippocampal-neocortical dynamics were particularly pronounced during long-duration compared to short-duration ripples. Together, our findings reveal a potential mechanism underlying active consolidation, comprising a neocortical-hippocampal-neocortical reactivation loop initiated by the neocortex. This hippocampal-cortical dialogue is mediated by sleep spindles and is enhanced during long-duration hippocampal ripples.

A distributed neocortical action map associated with reach-to-grasp

ABSTRACTReach-to-Grasp (RtG) is known to be dependent upon neocortical circuits and extensive research has provided insights into how selected neocortical areas contribute to control dexterous movements. Surprisingly, little infor-mation is available on the global neocortical computations underlying RtG in the mouse. Here, we characterized, employing fluorescence wide-field cal-cium imaging, the neocortex-wide dynamics from mice engaging in a RtG task. We demonstrate that, beyond canonical motor regions, several areas, such as the visual and the retrosplenial cortices, also increase their activ-ity levels during successful RtGs. Intriguingly, homologous regions across the ipsilateral hemisphere are also involved. Functional connectivity among areas increases transiently from rest to planning, and decreases during move-ment. Two anti-correlated neocortical networks emerged during movement. At variance, neural activity levels scale linearly with kinematics measures of successful RtGs in secondary motor areas. Our findings establish the coex-istence of distributed and localized neocortical dynamics for efficient control of complex movements.SIGNIFICANCE STATEMENTIn mammals, including humans, the cerebral cortex is known to be critical for the correct execution of dexterous movements. Despite the importance of the mouse for elucidating the neural circuitry for motor control, its neocortex-wide dynamics during RtG are largely unexplored. We used in-vivo fluores-cence microscopy to characterize the neural activity across the neocortex as mice performed a reach-to-grasp task. We show that for such complex movements, a large network of neocortical areas gets involved, while movement kinematics correlates with neural activity in secondary motor areas. These findings indicate the coexistence, at the mesoscale level, of distributed and localized neocortical dynamics for the execution of fine movements. This study offers a novel view on the neocortical correlates of motor control, with potential implications for neural repair.