Oscillatory dynamics coordinating human frontal networks in support of goal maintenance

Abstract

Humans have a capacity for hierarchical cognitive control-the ability to simultaneously control immediate actions while holding more abstract goals in mind. Neuropsychological and neuroimaging evidence suggests that hierarchical cognitive control emerges from a frontal architecture whereby prefrontal cortex coordinates neural activity in the motor cortices when abstract rules are needed to govern motor outcomes. We utilized the improved temporal resolution of human intracranial electrocorticography to investigate the mechanisms by which frontal cortical oscillatory networks communicate in support of hierarchical cognitive control. Responding according to progressively more abstract rules resulted in greater frontal network theta phase encoding (4-8 Hz) and increased prefrontal local neuronal population activity (high gamma amplitude, 80-150 Hz), which predicts trial-by-trial response times. Theta phase encoding coupled with high gamma amplitude during inter-regional information encoding, suggesting that inter-regional phase encoding is a mechanism for the dynamic instantiation of complex cognitive functions by frontal cortical subnetworks.

Figure 1

Task, subjects, and behavior. (A) Example trial events in the Response (R2 block) and Dimension (D2 block) sub-tasks. For the Response task, subjects responded according to 1st order mappings of colored squares to different button press responses; for the Dimension task subjects were cued by the colored square to make a 3rd order mapping – specifically, an object comparison based upon one of two object dimensions (texture or shape). Matching and non-matching examples are shown. (B) Example rule set mapping colors to key press responses across R1 (all colors map to the same response) and R2 (colors map to distinct responses) conditions of the Response task (left). Example mappings from colors to target dimensions across D1 (all colors map to the same dimension) and D2 (colors map to distinct dimensions) conditions of the Dimension task (right). (C) All artifact-free frontal electrodes were included in the analyses. All anterior electrodes are colored in blue and all posterior electrodes are colored in orange. Electrodes outlined in white showed significant task-dependent changes in high gamma amplitude. Of the 31 electrodes demonstrating a main effect of task on amplitude, 15 were located over M1/PMC and the remaining 16 were located over PFC. (D) Each subject showed a main effect of task on RTs such that RTs slowed as abstraction, and the corresponding cognitive control demands, increased. Subjects were fastest for zero-order stimulus-response mappings (R1, no conflict). RTs then increased parametrically for 1st order (R2), 2nd order (D1), and 3rd order response rules (D2). Error bars indicate SEM. (*) Significant regression of task condition on RT, p < 10^-20.

Figure 2

High gamma amplitude differentiates frontal responses. (A,B) Time-courses for the average event-related high gamma response across trials at the (A) 15 posterior (M1/PMC) and (B) 16 anterior (PFC) sites. (C) High gamma activity time to peak becomes increasingly delayed with increasing task abstraction in both M1/PMC (orange, p < 10^-5) and PFC (blue, p = 0.026) (* Significant interaction, p = 0.033; main effect of region, p = 0.00010; and main effect of task abstraction, p < 10^-4) (D) In contrast, peak high gamma amplitude decreases in M1/PMC (orange, p = 0.0023) as task abstraction increases, with no change in PFC amplitude (blue) (** Significant task-by-region interaction, p = 0.008; and main effect of region, p < 10^-9). Shaded regions and error bars indicate SEM.

Figure 3

Frontal phase/amplitude communication model. (A) Example instantaneous theta phase encoding between PFC (blue) and M1/PMC (orange) (rose plots). Note that these plots are illustrative of significant, instantaneous phase-encoding at a single time point, but that these encoding values are dynamic and the encoding phases for each condition can change within a trial, across trials, and across channel pairs. (B) The onset of significant phase encoding relative to the stimulus onset (Δt) differs for each encoding electrode pair (see Methods). This relationship is shown for an example pair of M1/PMC and PFC electrodes, along with the corresponding gamma amplitudes in M1/PMC, across multiple trial events. (C) Following the onset of significant phase encoding, event-related theta phase/high gamma amplitude phase/amplitude coupling (PAC) can be evaluated. As seen in this example, PAC is statistically assessed as a non-uniformity in the distribution of high gamma amplitude relative to the theta phase difference between PFC and M1/PMC sites such that for an illustrative case, (D), interregional encoding-triggered PAC provides an index of frontal communication via temporally-specific high gamma increases during interregional theta phase encoding.

Figure 4

Task- and region-dependent frontal theta phase encoding. (A) Time course of event-related interregional theta phase encoding between electrode pairs within M1/PMC (black), between M1/PMC and PFC (blue), and within PFC (red) for electrode pairs showing theta phase information transfer (phase encoding of the task). (B) Time-to-peak interregional theta phase encoding is earliest for electrode pairs within M1/PMC, peaks later for pairs between M1/PMC and PFC, and peaks latest for pairs within PFC (color scheme same as A). (C) Maximum event-related theta phase encoding is only different for pairs between M1/PMC and PFC compared to pairs within PFC. Note that the peak encoding and encoding times as inferred from the plots in A may differ from those found by averaging the trial-by-trial peaks shown in B and C due to the differences in findings peaks of averages (A) versus averaging peaks (B and C) (see Fig. S5 for an illustrative example). Shaded regions and error bars indicate SEM. (*) Significant t-test; p < 0.05. Horizontal bars indicate significant regression; p < 0.05 (uncorrected).

Figure 5

Encoding-triggered PAC. (A) For electrode pairs showing theta phase encoding of the task, theta/gamma PAC around the encoding peak increases as a function of task demands (main effect of task abstraction, p < 10^-18). There was also a task-by-coupling region interaction (*** Significant task-by-region interaction, p = 0.0058) such that encoding-triggered PAC increases as a function of task between encoding PFC electrode pairs (p < 10^-49) and for encoding pairs between M1/PMC and PFC (p < 10^-17), but less so for encoding pairs within M1/PMC (p = 0.084). (B) There was also an effect of directionality on PAC between M1/PMC and PFC such that PFC theta phase was a stronger predictor of M1/PMC high gamma than M1/PFC theta phase was of PFC high gamma (*** Significant main effect of direction, p = 0.0021; main effect of load: p < 10^-23). (C) Time course of time-resolved PAC (averaged across task conditions, colors same as in B); and, (D) effect size of directional PAC relative to encoding onset, showing that the peak directional effect is near the theta phase encoding onset (dashed line shows maximum directional PAC effect size observed in stimulus-locked case). (E) At no point during the trial period does this directionality effect for stimulus-locked PAC reach the magnitude of the directional PAC effect observed in the encoding-triggered case. (*) Significant main effect of task, p < 10^-4. Error bars and shaded regions indicate SEM. (ns: not significant)