Single-trial regression elucidates the role of prefrontal theta oscillations in response conflict

Abstract

In most cognitive neuroscience experiments there are many behavioral and experimental dynamics, and many indices of brain activity, that vary from trial to trial. For example, in studies of response conflict, conflict is usually treated as a binary variable (i.e., response conflict exists or does not in any given trial), whereas some evidence and intuition suggests that conflict may vary in intensity from trial to trial. Here we demonstrate that single-trial multiple regression of time-frequency electrophysiological activity reveals neural mechanisms of cognitive control that are not apparent in cross-trial averages. We also introduce a novel extension to oscillation phase coherence and synchronization analyses, based on "weighted" phase modulation, that has advantages over standard coherence measures in terms of linking electrophysiological dynamics to trial-varying behavior and experimental variables. After replicating previous response conflict findings using trial-averaged data, we extend these findings using single-trial analytic methods to provide novel evidence for the role of medial frontal-lateral prefrontal theta-band synchronization in conflict-induced response time dynamics, including a role for lateral prefrontal theta-band activity in biasing response times according to perceptual conflict. Given that these methods shed new light on the prefrontal mechanisms of response conflict, they are also likely to be useful for investigating other neurocognitive processes.

Keywords: EEG; cognitive control; medial frontal cortex; oscillations; regression; response conflict; single trial; theta.

Figures

Figure 1

Conditions (x-axis) are labeled according to previous (first, lowercase letter) and current trial (second, uppercase letter) conflict: C = congruent, I = incongruent. (A) Reaction times in ms. (B) Spearman's rank correlation coefficients. Error bars denote SEM.

Figure 2

Trial-averaged results, separated according to condition. (A,B) Condition-averaged topographical maps of power and phase coherence, which are the average of 150 ms surrounding the time point indicated below the maps. (C,D) Time–frequency plots of peri-response power and inter-trial phase coherence. Black areas enclose regions in which contiguous pixels were significantly different from inter-trial-interval baseline at p < 0.01 (two-tailed) for at least 300 ms and at least three consecutive frequencies.

Figure 3

Time–frequency plots of peri-response (time = 0) single-trial multiple regression coefficients, separated by condition (rows) and regression term (A–C). Black lines enclose significant regions, as in Figure 2. Time–frequency (TF) regression coefficient plots are taken from electrodes indicated by fuchsia circles.

Figure 4

Individual subject single-trial data illustrating the relationship between theta power (x-axis) and RT (y-axis). Axes differ per subject and are unlabeled. Each point is a single trial; lines reflect the best linear fit. Red pluses and lines are taken from cI trials, blue circles and lines from cC trials. These data correspond to the regression from a single time–frequency point for each subject. To select this subject-specific time–frequency point, we averaged the RT regression coefficients from all conditions and selected the point with the largest coefficient within the range of 1–12 Hz, −400 to 200 ms (the average across subjects was −233 ms and 5.1 Hz). Note that this selection procedure is not based on maximizing differences between cI and cC trials.

Figure 5

Time–frequency plots of peri-response single-trial phase modulation, separated by condition. Black lines enclose significant regions, as in Figure 2. Note the differences between these phase modulation plots – where the dominant effects occur in the theta band over frontal regions – and the trial-averaged phase coherence in Figure 2, which shows a dominant delta-band effect without a medial frontal focus.

Figure 6

Phase synchronization between electrode FCz (over MFC) and lateral prefrontal sites including F6 is present generally prior to the response, and, during high conflict situations, increases in strength with increasing reaction time. (A) Time–frequency plots of FCz–F6 “standard” (no modulation) phase synchronization (left column) and synchronization modulated by reaction time, luminance, and their interaction (right three columns). (B) Topographical maps of reaction time-modulated synchronization with FCz over time (columns) and condition (rows). Statistical thresholding is the same as in previous figures.

Figure 7

Selection of independent components for all subjects. Components were selected based on spatial correlation with a priori specified templates (left column). The average component across subjects was similar to the templates (middle column). Individual maps from all 15 subjects are shown in the right-most column.

Figure 8

Trial-averaged power results from the independent components (same as Figure 2C but using components instead of electrode-specific data).

Figure 9

Single-trial multiple regression analyses from independent components. The analysis was identical to that presented in Figure 3 but using components time courses instead of electrode-specific data.

Figure 10

Comparison of theta-band effects (trial-averaged power, power regression with reaction time, phase modulation by reaction time). Gray shading indicates that the regression coefficients are significantly greater than trial-averaged power at p < 0.01, minimum 300 ms continuous cluster threshold. Red and blue circles indicate subject-specific waveform peak times.