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

Autor: Daniel Egert, Daniel B. Silversmith, Karunesh Ganguly, Joshua D. Berke, Stefan M. Lemke
Rok vydání: 2020
Předmět:
Male
0301 basic medicine
1.1 Normal biological development and functioning
Population
Local field potential
Biology
spiking
Basic Behavioral and Social Science
Medical and Health Sciences
03 medical and health sciences
slow waves
0302 clinical medicine
Clinical Research
Underpinning research
Behavioral and Social Science
Neuroplasticity
Animals
sleep
education
Research Articles
Memory Consolidation
Neurons
education.field_of_study
Neurology & Neurosurgery
General Neuroscience
Psychology and Cognitive Sciences
Motor Cortex
slow oscillations
Neurosciences
Electroencephalography
spindle
Neurophysiology
Brain Waves
Degree (music)
Rats
030104 developmental biology
correlation
Neurological
Nesting (computing)
Memory consolidation
Sleep Stages
Primary motor cortex
Sleep
Neuroscience
030217 neurology & neurosurgery
Zdroj: The Journal of neuroscience : the official journal of the Society for Neuroscience, vol 40, iss 24
J Neurosci
ISSN: 1529-2401
0270-6474
DOI: 10.1523/jneurosci.2682-19.2020
Popis: 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. SIGNIFICANCE STATEMENT 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 local field potential, and synchrony across units peaked during spindles. Moreover, we showed that the degree of nesting between spindles and slow oscillations 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 slow oscillations 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.
Databáze: OpenAIRE