Paradoxical somatodendritic decoupling supports cortical plasticity during REM sleep

Abstract

Rapid eye movement (REM) sleep is associated with the consolidation of emotional memories. Yet, the underlying neocortical circuits and synaptic mechanisms remain unclear. We found that REM sleep is associated with a somatodendritic decoupling in pyramidal neurons of the prefrontal cortex. This decoupling reflects a shift of inhibitory balance between parvalbumin neuron–mediated somatic inhibition and vasoactive intestinal peptide–mediated dendritic disinhibition, mostly driven by neurons from the central medial thalamus. REM-specific optogenetic suppression of dendritic activity led to a loss of danger-versus-safety discrimination during associative learning and a lack of synaptic plasticity, whereas optogenetic release of somatic inhibition resulted in enhanced discrimination and synaptic potentiation. Somatodendritic decoupling during REM sleep promotes opposite synaptic plasticity mechanisms that optimize emotional responses to future behavioral stressors.

Large-volume and deep brain imaging in rabbits and monkeys using COMPACT two-photon microscopy

“…Recent imaging studies in rodents have revealed differential neuronal activity in the superficial cortical layer between awake and sleep states, suggesting that activity-dependent processes differ between different behavioral states 22 – 25 . Using the modified COMPACT method, we imaged calcium activity of neurons in layers 5 and 6 of the rabbit motor cortex during quiet awake state and slow wave sleep (Fig.…”

“…The activity of neurons in layers 5 and 6 of the rabbit motor cortex differ during slow wave sleep from that during quiet wakefulness. Different patterns of neuronal calcium activity in the mouse cortex under different behavioral states are suggested to be involved in experience and sleep-dependent cortical plasticity 23 – 25 . It would be of interest to investigate whether and how awake and sleep-related neuronal activity regulates neuronal network plasticity and dynamics under physiological and pathological conditions in large animals.…”

Large-volume and deep brain imaging in rabbits and monkeys using COMPACT two-photon microscopy

“…The activity of neurons in layers 5 and 6 of the rabbit motor cortex differ during slow-wave sleep from that during quiet wakefulness. Different patterns of neuronal calcium activity in the mouse cortex under different behavioral states are suggested to be involved in experience and sleep-dependent cortical plasticity [23][24][25] . It would be of interest to investigate whether and how awake and sleep-related neuronal activity regulates neuronal network plasticity and dynamics under physiological and pathological conditions in large animals.…”

“…Recent imaging studies in rodents have revealed differential neuronal activity in the super cial cortical layer between awake and sleep states, suggesting that activity-dependent processes differ between different behavioral states [22][23][24][25] . Using the modi ed COMPACT method, we imaged calcium activity of neurons in layers 5 and 6 of the rabbit motor cortex during quiet awake state and slow wave sleep (Fig.…”

Alterations in TRN-anterodorsal thalamocortical circuits affect sleep architecture and homeostatic processes in oxidative stress vulnerable Gclm−/− mice

“…However, changes in the phase coupling could contribute to the increase in corticocortical networks activity. In this context, PV + interneurons receive a large proportion of thalamic inputs, preferential from high order thalamus and control feed-forward inhibition of pyramidal neurons that in turn exert top down modulation of thalamic nuclei [110][111][112][113] (Supplementary Fig. 7).…”