Inhibition recruitment in prefrontal cortex during sleep spindles and gating of hippocampal inputs

Abstract

During light slow-wave sleep, the thalamo-cortical network oscillates in waxing-and-waning patterns at about 7 to 14 Hz and lasting for 500 ms to 3 s, called spindles, with the thalamus rhythmically sending strong excitatory volleys to the cortex. Concurrently, the hippocampal activity is characterized by transient and strong excitatory events, Sharp-Waves-Ripples (SPWRs), directly affecting neocortical activity-in particular the medial prefrontal cortex (mPFC)-which receives monosynaptic fibers from the ventral hippocampus and subiculum. Both spindles and SPWRs have been shown to be strongly involved in memory consolidation. However, the dynamics of the cortical network during natural sleep spindles and how prefrontal circuits simultaneously process hippocampal and thalamo-cortical activity remain largely undetermined. Using multisite neuronal recordings in rat mPFC, we show that during sleep spindles, oscillatory responses of cortical cells are different for different cell types and cortical layers. Superficial neurons are more phase-locked and tonically recruited during spindle episodes. Moreover, in a given layer, interneurons were always more modulated than pyramidal cells, both in firing rate and phase, suggesting that the dynamics are dominated by inhibition. In the deep layers, where most of the hippocampal fibers make contacts, pyramidal cells respond phasically to SPWRs, but not during spindles. Similar observations were obtained when analyzing γ-oscillation modulation in the mPFC. These results demonstrate that during sleep spindles, the cortex is functionnaly "deafferented" from its hippocampal inputs, based on processes of cortical origin, and presumably mediated by the strong recruitment of inhibitory interneurons. The interplay between hippocampal and thalamic inputs may underlie a global mechanism involved in the consolidation of recently formed memory traces.cortical deafferentation | fast spiking neurons | regular spiking neurons | memory reprocessing | Up and Down states

Rotating waves during human sleep spindles organize global patterns of activity that repeat precisely through the night

“…Further, HGP is modulated by spindle phase ( Figure 4B), increasing towards the surface-positive (depth-negative) peak, consistent with previous animal (Peyrache et al, 2011) and human recordings. Finally, by studying repeats of rotating waves over 2.5 hr of continuous sleep recording in Subject 1, we observe a preliminary indication of increased reverberation consistent with strengthening of distributed excitatory networks: similarity in the next identified rotating wave is highly predictive of the number of strong reverberations throughout the night (black dots, Figure 4C).…”

“…It is well established that spindles cause pyramidal cells and interneurons in cortex to fire preferentially at the peak of the surface-positive (depth-negative) LFP oscillation, both in intracellular Steriade, 1995, 1996;Kandel and Buzsáki, 1997) and extracellular (Peyrache et al, 2011) recordings. If cortical spindles were perfectly synchronized, spikes emitted during one cycle of the spindle oscillation would arrive at their post-synaptic targets with this temporal delay, leading to a pairing within the window for persistent long-term depression (LTD) that would progressively weaken long-range connections (Figure 2A, right).…”

Theta-associated high-frequency oscillations (110–160Hz) in the hippocampus and neocortex

“…The following observations led us to hypothesize that spiking activity causes SLHFO in the field potential: (1) similar highfrequency activity appears in the spike-triggered average of LFP time-frequency decompositions (Belluscio et al, 2012;Colgin et al, 2009;Peyrache et al, 2011); (2) recent studies have been suggesting that the power of oscillations in the SLHFO range correlates with spiking activity (Jia and Kohn, 2011;Ray et al, 2008;Ray and Maunsell, 2011); (3) the theta phase of maximal SLHFO amplitude coincides with the phase of maximal multiunit activity (Fig. 9b).…”

Sleep spindles are locally modulated by training on a brain–computer interface

“…It has been hypothesized that sleep spindles actually facilitate learning by establishing a cortical state that is conducive to synaptic plasticity, and therefore, to sleep-dependent memory consolidation (11,12). A great deal of emphasis has been placed on the role of sleep spindles in the hippocampal-neocortical dialogue (8,9,13), and thus consolidation of hippocampal-dependent memories. However, there is ample data to suggest that spindles are also important for motor and procedural learning (14)(15)(16)(17).…”