Abstract
Anxiety results in sub-optimal motor learning, but the precise mechanisms through which this effect occurs remain unknown. Using a motor sequence learning paradigm with separate phases for initial exploration and reward-based learning, we show that anxiety states in humans impair learning by attenuating the update of reward estimates. Further, when such estimates are perceived as unstable over time (volatility), anxiety constrains adaptive behavioral changes. Neurally, anxiety during initial exploration increased the amplitude and the rate of long bursts of sensorimotor and prefrontal beta oscillations (13-30 Hz). These changes extended to the subsequent learning phase, where phasic increases in beta power and burst rate following reward feedback were linked to smaller updates in reward estimates, with a higher anxiety-related increase explaining the attenuated belief updating. These data suggest that state anxiety alters the dynamics of beta oscillations during reward processing, thereby impairing proper updating of motor predictions when learning in unstable environments.
Highlights
We explicitly mention that prefrontal electrode regions were one of the regions of interest, together with “sensorimotor” electrode regions
The rationale for including a motor exploration phase in which participants did not receive trial-based feedback or reinforcement was based on findings indicating that initial motor variability can influence the rate at which participants learn in a subsequent motor task (Wu et al, 2014)
In a last post-hoc analysis, we found that the average beta power following the STOP signal in those same significant sensorimotor electrodes was negatively correlated with the across-trials temporal variability, such that participants with a smaller increase in sensorimotor beta power after the STOP signal had a larger expression of taskrelated variability in this initial block (Spearman 1⁄4 À0:4397; P 1⁄4 0:0001; Figure 8—figure supplement 6)
Summary
We explicitly mention that prefrontal electrode regions were one of the regions of interest, together with “sensorimotor” electrode regions. We cite more work that identifies prefrontal regions as central to the neural circuitry of anxiety. “Crucially, in addition to assessing sensorimotor brain regions, we focused our analysis on prefrontal areas on the basis of prior work in clinical and subclinical anxiety linking the prefronal cortex (dmPFC, dlPFC) and the dACC to the maintenance of anxiety states, including worry and threat appraisal (Grube and Nitsche, 2012; Robinson et al 2019). “We assessed both power and burst distribution of beta oscillations to capture dynamic changes in neural activity induced by anxiety and their link to behavioral effects.”. “EEG signals aimed to assess anxiety-related changes in the power and burst distribution in sensorimotor and prefrontal beta oscillations in relation to changes in behavioral variability and rewardbased learning.”
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