Theta oscillatory dynamics of inhibitory control, error processing, and post-error adjustments: Neural underpinnings and alcohol-induced dysregulation in social drinkers

Abstract

Background: Alcohol intoxication impairs inhibitory control, resulting in disinhibited, impulsive behavior. The anterior cingulate cortex (ACC) plays an essential role in a range of executive functions and is sensitive to the effects of alcohol, which contributes to the top-down cognitive dysregulation. This study used a multimodal approach to examine the acute effects of alcohol on the neural underpinnings of inhibitory control, inhibition failures, and neurobehavioral optimization as reflected in trial-to-trial dynamics of post-error adjustments.

Methods: Adult social drinkers served as their own controls by participating in the Go/NoGo task during acute alcohol and placebo conditions in a multi-session, counterbalanced design. Distributed source modeling of the magnetoencephalographic signal was combined with structural magnetic resonance imaging to characterize the spatio-temporal dynamics of inhibitory control in the time-frequency domain.

Results: Successful response inhibition (NoGo) elicited right-lateralized event-related theta power (4 to 7 Hz). Errors elicited a short-latency increase in theta power in the dorsal (dACC), followed by activity in the rostral (rACC), which may underlie an affective "oh, no!" orienting response to errors. Error-related theta in the dACC was associated with subsequent activity of the motor areas on the first post-error trial, suggesting the occurrence of post-error output adjustments. Importantly, a gradual increase of the dACC theta across post-error trials closely tracked improvements in accuracy under placebo, which may reflect cognitive control engagement to optimize response accuracy. In contrast, alcohol increased NoGo commission errors, dysregulated theta during correct NoGo withholding, and abolished the post-error theta enhancement of cognitive control.

Conclusions: Confirming the sensitivity of frontal theta to inhibitory control and error monitoring, the results support functional and temporal dissociation along the dorso-rostral axis of the ACC and the deleterious effects of alcohol on the frontal circuitry subserving top-down regulation. Over time, alcohol-induced disinhibition may give rise to compulsive drinking and contribute to alcohol misuse.

Keywords: alcohol intoxication; anterior cingulate cortex; errors; event-related theta; response inhibition.

FIGURE 1

Inhibitory Go/NoGo task. A sequence of “X” and “Y” letters, 600 in total, was presented in rapid succession every 1200 ± 100 ms. Each letter was presented for 230 ms and was replaced by a centrally located fixation dot for the remainder of the trial. Participants were instructed to respond with their right index finger to each alternation (Go, 80%) and to inhibit responding to each letter repetition (NoGo, 20%). In this task, all NoGo errors are errors of commission, and all Go errors are errors of omission

FIGURE 2

Performance measures (means ± standard errors) for: (A) Go and NoGo accuracy, (B) reaction times to correct Go and erroneous NoGo responses for both beverage conditions. Alcohol increased the number of NoGo errors (*p < 0.05), but did not affect RTs

FIGURE 3

Group‐average maps of event‐related theta source power estimates for successful response execution (Go) and inhibition (NoGo) are shown on an inflated template cortex for both hemispheres laterally (top two rows) and medially (bottom two rows), for both alcohol and placebo sessions. Time‐courses of estimated activity are shown for the most prominent loci. (A) Successful response execution on Go trials elicited a much larger event‐related theta power increase in the left sensorimotor (sMOT) cortex and the SMA than response withholding on NoGo trials. Alcohol attenuated Go theta in the left sMOT and the left IFC, *p < 0.05. (B) Successful response inhibition on NoGo trials elicited event‐related theta power predominantly in the right frontal and temporal cortices. Alcohol reduced theta power selectively on NoGo trials in the right IFC, LTC, SMA, and the ACC, *p < 0.05, **p < 0.01

FIGURE 4

Group‐average maps of response‐locked event‐related theta source power estimates in the right hemisphere in the 50 to 200 ms (a) and 300 to 400 ms (b) time windows following erroneous button presses on NoGo Err trials and correct Go responses. Time‐courses of the activity estimated to the insula (INS), dorsal ACC (dACC) and rostral ACC (rACC) are shown in the lower panel. Under placebo, NoGo errors elicit greater theta immediately after an error, followed by another theta peak in the rACC ~250 ms later. Alcohol attenuated error‐related theta in the INS and rACC. ^& p = 0.08, *p < 0.05, **p < 0.01

FIGURE 5

(A) Accuracy and RTs on the first Go trial following NoGo errors and correct NoGo trials. Reduced accuracy and RT slowing was observed on the first post‐error Go trials, *p < 0.05. (B) Theta elicited by NoGo errors in the right dorsal ACC predicts theta power on the subsequent Go trial in the left lateral (sMOT) and medial (SMA) motor cortices. (C) On Go trials following NoGo errors, theta increase in the right dorsal ACC (200 to 450 ms) tracks trial‐to‐trial improvement in accuracy under placebo. In contrast, the post‐error adjustments of accuracy and theta power were dysregulated by alcohol. Time‐courses of theta estimated to the dACC on post‐error Go trials are shown in the right panel