The Degree of Nesting between Spindles and Slow Oscillations Modulates Neural Synchrony

Abstract

Spindles and slow oscillations (SOs) both appear to play an important role in memory consolidation. Spindle and SO "nesting," or the temporal overlap between the two events, is believed to modulate consolidation. However, the neurophysiological processes modified by nesting remain poorly understood. We thus recorded activity from the primary motor cortex of 4 male sleeping rats to investigate how SO and spindles interact to modulate the correlation structure of neural firing. During spindles, primary motor cortex neurons fired at a preferred phase, with neural pairs demonstrating greater neural synchrony, or correlated firing, during spindle peaks. We found a direct relationship between the temporal proximity between SO and spindles, and changes to the distribution of neural correlations; nesting was associated with narrowing of the distribution, with a reduction in low-and high-correlation pairs. Such narrowing may be consistent with greater exploration of neural states. Interestingly, after animals practiced a novel motor task, pairwise correlations increased during nested spindles, consistent with targeted strengthening of functional interactions. These findings may be key mechanisms through which spindle nesting supports memory consolidation.

Twitches emerge postnatally during quiet sleep in human infants and are synchronized with sleep spindles

“…If so, then the temporal association between twitches and sleep spindles (Figure 4) could reflect emerging communication among brainstem and cortical motor structures, including primary motor cortex (M1). In fact, in adult rats, sleep spindles increase the likelihood that neurons in M1 fire synchronously 22 and contribute to M1 activity associated with the learning of a skilled motor task. 23 In mammals, M1 develops much later than is commonly realized.…”

Twitches emerge postnatally during quiet sleep in human infants and are synchronized with sleep spindles

“…If so, then the temporal association between twitches and sleep spindles (Figure 4) could reflect emerging communication among brainstem and cortical motor structures, including primary motor cortex (M1). In fact, in adult rats, sleep spindles increase the likelihood that neurons in M1 fire synchronously [20] and contribute to M1 activity associated with the learning of a skilled motor task [21].…”

“…Topoplots were then averaged (mean) across sleep sessions within each age group. To produce a single value for sleep-spindle and delta power for each sleep session, we calculated the median value over electrode sites within regions of interest (sleep spindles: electrodes 5,6,7,12,13,20,29,30,31,36,37,42,55,80,87,93,104,105,106,111,112,118; delta: anterior electrodes 3, 4, 5,6,7,10,11,12,13,16,18,19,20,23,24,28,29,30,31,36,37,55,80,87,93,104,105,106,111,112,117,118,124; posterior electrodes 70, 74, 75, 81, 82, 83).…”

Local coupling between sleep spindles and slow oscillations supports the stabilization of motor memories

“…There is growing evidence sustaining that both SO, spindle activity and their coupling develop locally during sleep rather than globally (Massimini et al, 2004;Andrillon et al, 2011;Nir et al, 2011;Cox et al, 2018). In motor skill learning, for example, local modulation has been observed in humans for sleep spindles (Nishida & Walker, 2007;Johnson et al, 2012) and more recently in rats for spindle-SO coupling (Silversmith et al, 2020). This focal effect suggests that sleep may promote the consolidation of memory representations in local networks that may be active during learning (Klinzing et al, 2019).…”

“…Recent work carried out in rats using the grasp-and-reach learning paradigm described the occurrence of task-related neural replay over the motor cortex during NREM sleep, often phase locked to spindle oscillations (Ramanathan et al, 2015). A more recent study from the same lab reported a modulation of motor learning over the density of spindle-SO couplings (Silversmith et al, 2020). Yet, whether the two phenomena are linked to one another and relate to offline gains in performance remains to be established.…”