Transient suppression of broadband gamma power in the default-mode network is correlated with task complexity and subject performance

Abstract

Task performance is associated with increased brain metabolism but also with prominent deactivation in specific brain structures known as the default-mode network (DMN). The role of DMN deactivation remains enigmatic in part because its electrophysiological correlates, temporal dynamics, and link to behavior are poorly understood. Using extensive depth electrode recordings in humans, we provide first electrophysiological evidence for a direct correlation between the dynamics of power decreases in the DMN and individual subject behavior. We found that all DMN areas displayed transient suppressions of broadband gamma (60-140 Hz) power during performance of a visual search task and, critically, we show for the first time that the millisecond range duration and extent of the transient gamma suppressions are correlated with task complexity and subject performance. In addition, trial-by-trial correlations revealed that spatially distributed gamma power increases and decreases formed distinct anticorrelated large-scale networks. Beyond unraveling the electrophysiological basis of DMN dynamics, our results suggest that, rather than indicating a mere switch to a global exteroceptive mode, DMN deactivation encodes the extent and efficiency of our engagement with the external world. Furthermore, our findings reveal a pivotal role for broadband gamma modulations in the interplay between task-positive and task-negative networks mediating efficient goal-directed behavior and facilitate our understanding of the relationship between electrophysiology and neuroimaging studies of intrinsic brain networks.

Figures

Figure 1.

High-density depth electrode recordings during visual search. A, Left, Top and right side views of implanted electrode locations represented on a 3-D reconstruction of a standard (MNI) brain. Blue dots represent the Talairach coordinates for all contacts on all SEEG electrodes for all 14 subjects (total = 1730 recording sites). B, Example of visual search arrays for easy (blue) and difficult (red) conditions (subjects were asked to find the T among the Ls). C, Strong power suppression in broad-band gamma (60–140 Hz) in right VLPFC during visual search. High gamma suppression also coincides with power increases in lower (<30 Hz) frequency range. The illustrative time–frequency map represent increases and decreases in spectral power compared to a prestimulus baseline level (baseline, [from −400 to −100] ms, Wilcoxon Z value).

Figure 2.

Brain-wide dynamics of gamma-band power decrease, GBD, during visual search. A, Anatomical distribution of statistically significant broad-band gamma (60–140 Hz) suppression obtained by mapping depth electrode data in all subjects (n = 14) to a standard brain. The spatial properties of GBD bear a striking resemblance to DMN maps previously reported with fMRI. Data snapshot at t = 640 ms following search array presentation (only power decreases are shown here; see Fig. 5 for power increases and decreases and Materials and Methods for details) B, GBD temporal profile during easy (blue) and difficult (red) search for four illustrative clusters: PCC, MPFC, LTC, and VLPFC left (L). Time t = 0 ms indicates onset of search array display. C, Mean GBD onset for each cluster. Values represent mean onset latency, i.e., time sample at which deactivation reached statistical significance (group effect F(4,98) = 6.817, p < 0.0001; Tukey's HSD Test (*) indicates p < 0.05). D, Duration of GBD for easy (blue) and difficult (red) visual search conditions. Values represent mean duration of significant deactivation across all electrodes of each cluster (t test (*) indicates t > 2.76, p < 0.01). See Table 2 for the details of task-related GBD duration and associated p values and Table 3 for GBD cluster details.

Figure 3.

Single electrode data show suppression of gamma-band activity varies with task difficulty. Temporal profile of gamma band (60–140 Hz) power modulations are displayed for the two conditions: easy search (blue) and difficult search (red) for representative sites in the task-negative (i.e., power suppression) network. The displayed data correspond to electrodes located in (from top to bottom): VLPFC left (L), PCC, VLPFC right (R), MPFC, and LTC. Horizontal red and blue lines, beneath the waveforms, indicate statistically significant gamma-band suppressions relative to baseline period ([from −400 to −100] ms). We used signed rank Wilcoxon test and FDR correction (p < 0.05). Line upper/lower bounds indicate ± 1 SEM. Note that the anatomical ROI name above each MRI panel is followed by subject number and electrode name.

Figure 4.

Relationship between gamma-band power decreases and behavioral performance. A, Mean gamma power suppression computed separately for 50% fastest response trials (magenta) and 50% slowest response trials (turquoise). Gamma power suppressions in MPFC and right VLPFC (VLPC R) clusters were stronger for fast target detection than for the slower detections (both t > 3.11, p < 0.01). Differences were not statistically significant for other GBD clusters (data not shown). Mean power was computed over a [200–700] ms time window following stimulus presentation. B, Profile of mean gamma power (± SE) in a VLPFC R recording site (Talairach coordinates: x = 55, y = 33, z = 0) for 50% fastest (magenta) versus 50% slowest (turquoise) response trials. C, Profile of correlation coefficient between single-trial gamma power at this site and the individual reaction times. A peak correlation occurred at tmax = 736 ms after stimulus onset. D, Trial-by-trial plot of reaction time (RT) versus gamma power at tmax depicts the significant correlation between single-trial gamma suppression and behavioral performance (Spearman's correlation test, rho = 0.34968, p = 0.0000969). E, Single-trial gamma power plot for same electrode as in B–D with trials sorted according to RTs (fastest to slowest target detection). White line depicts RT (i.e., latency of button press indicating target detection for each trial. Time t = 0 corresponds to visual search array onset.

Figure 5.

Spatial distribution of task-related power decreases (blue) and increases (red) during visual search in multiple frequency bands. A, Theta (4–7 Hz). B, Alpha band (8–12 Hz). C, Beta band (13–30 Hz). D, Low gamma band (30–60 Hz). E, High gamma band (60–140 Hz). The distribution of task-related gamma power suppressions is the one that most closely matches typical DMN deactivation patterns. Power patterns in theta and alpha bands did not show comparable suppressions in DMN areas. Beta power suppressions were observed in some DMN areas but also in visual and dorsal attention network areas. Unlike gamma suppressions, beta suppressions in the DMN clusters were not significantly correlated with behavior (data not shown).

Figure 6.

Correlated and anticorrelated gamma-band task networks. A, Spatial distribution of task-related gamma decreases (blue) and increases (red) during visual search, representing a task negative network and a task positive network, respectively. While TNN closely matches DMN and ventral attention network areas, TPN depicts concurrent activations in visual and dorsal attention network areas (data represent a snapshot of gamma power modulation at t = 640 ms as compared to baseline level). B, Anticorrelated gamma networks. These measure correlation among TPN-TNN by assessing correlation between single-trial data from all electrodes of TPN ROIs and TNN ROIs. C, Correlated gamma networks. These are the same as in B, but electrode pairs for the correlation analysis were always from the same type of network i.e., TPN-TPN and TNN-TNN correlations (TPN and TNN anatomical regions and electrode details are provided in Table 3).