Dynamic Changes in Phase-Amplitude Coupling Facilitate Spatial Attention Control in Fronto-Parietal Cortex

<div><p>Attention is a core cognitive mechanism that allows the brain to allocate limited resources depending on current task demands. A number of frontal and posterior parietal cortical areas, referred to collectively as the fronto-parietal attentional control network, are engaged during attentional allocation in both humans and non-human primates. Numerous studies have examined this network in the human brain using various neuroimaging and scalp electrophysiological techniques. However, little is known about how these frontal and parietal areas interact dynamically to produce behavior on a fine temporal (sub-second) and spatial (sub-centimeter) scale. We addressed how human fronto-parietal regions control visuospatial attention on a fine spatiotemporal scale by recording electrocorticography (ECoG) signals measured directly from subdural electrode arrays that were implanted in patients undergoing intracranial monitoring for localization of epileptic foci. Subjects (<i>n</i> = 8) performed a spatial-cuing task, in which they allocated visuospatial attention to either the right or left visual field and detected the appearance of a target. We found increases in high gamma (HG) power (70–250 Hz) time-locked to trial onset that remained elevated throughout the attentional allocation period over frontal, parietal, and visual areas. These HG power increases were modulated by the phase of the ongoing delta/theta (2–5 Hz) oscillation during attentional allocation. Critically, we found that the strength of this delta/theta phase-HG amplitude coupling predicted reaction times to detected targets on a trial-by-trial basis. These results highlight the role of delta/theta phase-HG amplitude coupling as a mechanism for sub-second facilitation and coordination within human fronto-parietal cortex that is guided by momentary attentional demands.</p></div

ERPs during attentional allocation.

<p>(<b>a</b>) Single-trial and averaged ERPs time-locked to trial onset (left) or target onset (right) for an example electrode in a single subject (yellow circle on the cortical reconstruction of S8). Top: ERPs averaged across all trials in which the target appeared in the attended/cued hemifield (blue traces) or in the unattended/uncued hemifield (red traces). Blue shaded region represents the time points during which there was a significant difference between conditions (all <i>p</i><0.05, corrected). Bottom: Single trial ERPs for attention/cued conditions only. Black tick marks signify target onset (left) and manual response (right). Trials are stacked according to target or response onset. (<b>b</b>) ERPs averaged across all electrodes that showed an individual ERP (<i>n</i> = 77; top) or averaged across all electrodes with significant delta/theta-HG PAC (<i>n</i> = 123; bottom) time-locked to trial onset (left) or target onset (right). All other conventions are the same as in (a).</p

PAC-behavioral correlations.

<p>Correlations between the strength of delta/theta-HG PAC (measured with PLV) and reaction times (RTs) during SNT performance. Examples of two different electrodes (circled in yellow on each cortical reconstruction) are shown for two different subjects (S3, left panel and S5, right panel) during attention to either the contralateral (top) or ipsilateral (bottom) visual fields. The red circles on each cortical reconstruction indicate all other electrodes in these two subjects that showed significant PAC-RT correlations across trials. The red line on each scatter plot indicates the regression line through each data set.</p

Electrode coverage and Starry Night Test (SNT).

<p>(<b>a</b>) Overlap of implanted electrodes across all subjects (<i>n</i> = 8) on the lateral and medial surfaces (top, bottom, respectively) in the right and left hemispheres (right, left, respectively) overlaid on a cortical reconstruction of the MNI standardized brain. (<b>b</b>) In the SNT, subjects allocated their visual attention to either the RVF or LVF, as indicated by a cue at fixation, and waited for a target (blue square) to appear somewhere in the visual field. Targets appeared on a dynamic background of red circle distracters. Subjects responded with a button press once they detected the target. Example of a single trial is shown during which the RVF was cued.</p

ERPs: Attention to contralateral vs. ipsilateral visual field.

<p>ERPs averaged across all trials where the attended target appeared in either the visual field contralateral (blue traces) or ipsilateral (red traces) to the implanted hemisphere and time-locked to trial onset (left) or target onset (right). ERPs are averaged across all electrodes that showed an individual ERP (<i>n</i> = 77). All other conventions are the same as in <a href="http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1001936#pbio-1001936-g005" target="_blank">Figure 5</a>.</p

ECoG subjects.

<p>F, female; M, male; L, left; R, right; LH, left hemisphere; RH, right hemisphere; LF, lateral frontal; Md, medial; O, occipital; P, parietal; T, temporal.</p><p>ECoG subjects.</p

Delta/theta phase-HG amplitude coupling during attentional allocation.

<p>Examples of electrodes with significant delta/theta phase-HG amplitude coupling during attentional allocation. (<b>a,b</b>) Comodulograms for two example electrodes (circled in yellow on each subject's cortical reconstruction), one over lateral frontal cortex and one surrounding the IPS, are shown underneath the respective brain areas of two subjects, S3 (<b>a</b>) and S5 (<b>b</b>). Each comodulogram illustrates PAC strength (measured with PLV) across a range of frequencies (x-axis = frequency for phase signal, y-axis = frequency for amplitude signal). Contour lines represent <i>p</i>-values (outer to inner: <i>p</i> = 0.50, 0.10, 0.05, 0.01, 0.005). Separate comodulograms were calculated for the contralateral and ipsilateral attention conditions. Additional electrodes with significant delta/theta-HG PAC in these two subjects are circled in red. See <a href="http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1001936#pbio-1001936-g006" target="_blank">Figure 6</a> for the significant electrodes in the remaining subjects. (<b>c</b>) A trough-locked spectrogram from an example electrode over PPC (circled in yellow on the cortical reconstruction of S4). Right, bottom: the trough-locked ERP of the filtered delta/theta signal (2–5 Hz). Right, top: normalized power across a range of frequencies for the corresponding time points of the trough-locked delta/theta signal (below). Additional electrodes with significant delta/theta-HG PAC in S4 are circled in red.</p

HG power changes track attentional allocation.

<p>Event-related spectral perturbations (ERSPs; top) and vertically-stacked single-trial HG traces (bottom) in two example electrodes of two different subjects, S4 (<b>a</b>) and S7 (<b>b</b>). The red circle on each subject's cortical reconstruction indicates the electrode from which each of the ERSPs and single-trial HG traces was taken. ERSPs were averaged across trials when subjects attended to either the visual field contralateral (left) or ipsilateral (right) to the implanted hemisphere. The normalized power from 1–250 Hz is shown time-locked to the beginning of each trial. HG power (70–250 Hz) is shown for each individual trial for contralateral (left) and ipsilateral (right) attentional conditions. Traces are locked to each trial onset and black tick marks signify target onset. Trials are stacked according to target onset.</p