Abstract
Field potential (FP) oscillations are believed to coordinate brain activity over large spatiotemporal scales, with specific features (e.g., phase and power) in discrete frequency bands correlated with motor output. Furthermore, complex correlations between oscillations in distinct frequency bands (phase-amplitude, amplitude-amplitude, and phase-phase coupling) are commonly observed. However, the mechanisms underlying FP-behavior correlations and cross-frequency coupling remain unknown. The thalamus plays a central role in generating many circuit-level neural oscillations, and single-unit activity in motor thalamus (Mthal) is correlated with behavioral output. We, therefore, hypothesized that motor thalamic spiking coordinates motor system FPs and underlies FP-behavior correlations. To investigate this possibility, we recorded wideband motor thalamic (Mthal) electrophysiology as healthy rats performed a two-alternative forced-choice task. Delta (1–4 Hz), beta (13–30 Hz), low gamma (30–70 Hz), and high gamma (70–200 Hz) power were strongly modulated by task performance. As in the cortex, the delta phase was correlated with beta/low gamma power and reaction time. Most interestingly, subpopulations of Mthal neurons defined by their relationship to the behavior exhibited distinct relationships with FP features. Specifically, neurons whose activity was correlated with action selection and movement speed were entrained to delta oscillations. Furthermore, changes in their activity anticipated power fluctuations in beta/low gamma bands. These complex relationships suggest mechanisms for commonly observed FP-FP and spike-FP correlations, as well as subcortical influences on motor output.
Highlights
Field potential (FP) oscillations are rhythmic fluctuations in extracellular potentials that emerge from, and may regulate (Anastassiou et al, 2010), neuronal dynamics over a large spatiotemporal scale (Fries, 2015)
Task-linked motor thalamic (Mthal) FP power modulation was nearly identical to prior observations in the motor cortex and the basal ganglia during a similar task (Figure 2; Leventhal et al, 2012)
The post-Nose Out beta/low gamma increase was more tightly locked to the Nose Out than the Tone event, suggesting that it is related to movement initiation rather than Tone perception (Figure 3)
Summary
Field potential (FP) oscillations are rhythmic fluctuations in extracellular potentials that emerge from, and may regulate (Anastassiou et al, 2010), neuronal dynamics over a large spatiotemporal scale (Fries, 2015). Beta oscillations (∼13–30 Hz) in the cortex and basal ganglia are enhanced under several conditions including pre-movement hold periods (Donoghue et al, 1998; Saleh et al, 2010), isometric contractions (Baker et al, 1997), post-movement ‘‘rebound’’ (Pfurtscheller et al, 1996; Feingold et al, 2015), and parkinsonism (Brown, 2006; Mallet et al, 2008; Ellens and Leventhal, 2013). Movement onset is associated with decreased beta and increased gamma (∼60–100 Hz) power (Feingold et al, 2015; Tan et al, 2019; but see Leventhal et al, 2012). The mechanisms by which FP features and behavior are correlated remain unclear
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