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

• Published in: The Journal of neuroscience 2020-06, Vol.40 (24), p.4673-4684
• Main Authors: Silversmith, Daniel B, Lemke, Stefan M, Egert, Daniel, Berke, Joshua D, Ganguly, Karunesh
• Format: Article
• Language: English
• Subjects: Consolidation; Correlation; Cortex (motor); Cortex (temporal); Nesting; Oscillations
• ISSN: 0270-6474; 1529-2401
• DOI: 10.1523/JNEUROSCI.2682-19.2020

Spindles and slow oscillations (SO) 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 (M1) of four male sleeping rats to investigate how SO and spindles interact to modulate the correlation structure of neural firing. During spindles, M1 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. Our analysis revealed changes in cortical spiking structure that followed the waxing and waning of spindles; firing rates increased, spikes were more phase-locked to spindle-band LFP, and synchrony across units peaked during spindles. Moreover, we showed that the degree of nesting between spindles and SO modified the correlation structure across units by narrowing the distribution of pairwise correlations. Finally, we demonstrated that engaging in a novel motor task increased pairwise correlations during nested spindles. These phenomena suggest key mechanisms through which the interaction of spindles and SO may support sensorimotor learning. More broadly, this work helps link large-scale measures of population activity to changes in spiking structure, a critical step in understanding neuroplasticity across multiple scales.