Theta oscillations are sensitive to both early and late conflict processing stages: effects of alcohol intoxication

Abstract

Prior neuroimaging evidence indicates that decision conflict activates medial and lateral prefrontal and parietal cortices. Theoretical accounts of cognitive control highlight anterior cingulate cortex (ACC) as a central node in this network. However, a better understanding of the relative primacy and functional contributions of these areas to decision conflict requires insight into the neural dynamics of successive processing stages including conflict detection, response selection and execution. Moderate alcohol intoxication impairs cognitive control as it interferes with the ability to inhibit dominant, prepotent responses when they are no longer correct. To examine the effects of moderate intoxication on successive processing stages during cognitive control, spatio-temporal changes in total event-related theta power were measured during Stroop-induced conflict. Healthy social drinkers served as their own controls by participating in both alcohol (0.6 g/kg ethanol for men, 0.55 g/kg women) and placebo conditions in a counterbalanced design. Anatomically-constrained magnetoencephalography (aMEG) approach was applied to complex power spectra for theta (4-7 Hz) frequencies. The principal generator of event-related theta power to conflict was estimated to ACC, with contributions from fronto-parietal areas. The ACC was uniquely sensitive to conflict during both early conflict detection, and later response selection and execution stages. Alcohol attenuated theta power to conflict across successive processing stages, suggesting that alcohol-induced deficits in cognitive control may result from theta suppression in the executive network. Slower RTs were associated with attenuated theta power estimated to ACC, indicating that alcohol impairs motor preparation and execution subserved by the ACC. In addition to their relevance for the currently prevailing accounts of cognitive control, our results suggest that alcohol-induced impairment of top-down strategic processing underlies poor self-control and inability to refrain from drinking.

Figure 1. Performance measures.

Accuracy, reaction times, and the percentage of trials on which participants corrected their responses immediately after an error (means ± standard errors) are shown for each task and beverage condition. The Stroop interference effect is indicated by lower accuracy and slower reaction times to conflict-inducing incongruous (INC) stimuli overall. Alcohol did not affect RTs, but participants responded less accurately and made more corrective responses on INC trials when intoxicated. Significant alcohol vs. placebo comparisons for each condition are marked, *p<0.05.

Figure 2. Group-average maps of event-related theta source power estimates in 320–470 ms time window.

Event-related theta power is elicited in the fronto-parieto-cingulate network with the ACC as the strongest estimated source, and is attenuated by intoxication (white arrows). The color scale depicts baseline-corrected noise-normalized source power expressed in arbitrary units. The bottom row shows conflict–related theta power (INCONG - CONG contrast) for both beverage conditions. The color scale denotes differential baseline-corrected source power estimates, with red-yellow indicating stronger theta power to INCONG. Conflict-related theta is attenuated by intoxication in the right prefrontal (cyan arrow) and ACC (orange arrow) cortices. CONG stimuli elicited stronger theta in the motor -related medial cortex due to motor preparation at this latency.

Figure 3. Group-average timecourses of event-related theta source power estimates in selected regions of interest.

While alcohol reduces event-related theta power overall, attenuation of the conflict-related theta (INCONG vs. CONG contrast) is particularly prominent in ACC, with contributions from lateral fronto-parietal areas. Direct comparison of the beverage effects on conflict-related theta reached significance as indicated by arrows, *p<0.05, **p<0.01. Horizontal bars indicate the three time windows for which power was averaged and entered into statistical analysis. The y-axis depicts baseline-corrected noise-normalized source power expressed in arbitrary units. ACC: anterior cingulate cortex; IFJ: inferior frontal junction; IFG: inferior frontal gyrus; SFG: superior frontal gyrus; PAR: parietal cortex.

Figure 4. Group-average timecourses of response-locked theta source power estimates in the left ACC and MOT areas.

Time 0 ms corresponds to the button press. The time window immediately preceding motor responses is indicated by a horizontal bar. During this time, only ACC showed sensitivity to conflict with stronger theta on INCONG than CONG trials during placebo (* p<0.02), suggesting the ACC engagement in response selection and execution. Alcohol attenuated pre-response theta overall. The y-axis depicts baseline-corrected noise-normalized source power expressed in arbitrary units.

Figure 5. Grand averages of event-related EEG power at the frontal (Fz) electrode.

a) Time-frequency plots of total event-related power expressed as the relative percentage change from the power in the baseline (−250 to 0 ms) for each frequency. Four task conditions (rows) are shown for placebo and alcohol sessions. Most pronounced beverage and task effects were observed in the theta band. b) Group averaged total event-related power in the theta frequency band at the Fz electrode. Horizontal bars indicate the three time windows for which power was averaged and entered into statistical analysis. Alcohol decreased total event-related theta power overall. Conflict-related increase in theta power was significant in the late time window only under placebo.