Ongoing Activity in Temporally Coherent Networks Predicts Intra-Subject Fluctuation of Response Time to Sporadic Executive Control Demands

<div><p>Can ongoing fMRI BOLD signals predict fluctuations in swiftness of a person’s response to sporadic cognitive demands? This is an important issue because it clarifies whether intrinsic brain dynamics, for which spatio-temporal patterns are expressed as temporally coherent networks (TCNs), have effects not only on sensory or motor processes, but also on cognitive processes. Predictivity has been affirmed, although to a limited extent. Expecting a predictive effect on executive performance for a wider range of TCNs constituting the cingulo-opercular, fronto-parietal, and default mode networks, we conducted an fMRI study using a version of the color–word Stroop task that was specifically designed to put a higher load on executive control, with the aim of making its fluctuations more detectable. We explored the relationships between the fluctuations in ongoing pre-trial activity in TCNs and the task response time (RT). The results revealed the existence of TCNs in which fluctuations in activity several seconds before the onset of the trial predicted RT fluctuations for the subsequent trial. These TCNs were distributed in the cingulo-opercular and fronto-parietal networks, as well as in perceptual and motor networks. Our results suggest that intrinsic brain dynamics in these networks constitute “cognitive readiness,” which plays an active role especially in situations where information for anticipatory attention control is unavailable. Fluctuations in these networks lead to fluctuations in executive control performance.</p></div

Distribution of response time (RT) for the Stroop task (A) and simple response task (B).

<p>Data of all subjects were concatenated.</p

Statistics for the response time (RT) predictivity of the nine temporally coherent networks (TCNs) at pre-trial time points (<i>t</i> = −6.0 to 0.0 s).

<p>Each cell shows the <i>t</i>-value (df = 47) of the two-tailed one sample <i>t</i>-test of the mean coefficient of RT-predictive ANCOVA model over subjects, with a braced false discovery rate (FDR)-corrected <i>p</i>-value.</p

All the independent components (ICs) extracted by the group ICA.

<p><i>I_q</i>: cluster quality index; MNI peak: Montreal Neurological Institute (MNI) coordinates of the highest peak position; DR: dynamic range; LH: low to high power ratio.</p><p>ICs were classified into TCNs or artifacts, and TCNs were labeled with anatomical names based on their spatial maps. AG: angular gyrus; AI: anterior insula; Amyg: amygdala; dACC: dorsal anterior cingulate cortex; dlPFC: dorsolateral prefrontal cortex; FEF: frontal eye field; FO: frontal operculum; IFG: inferior frontal gyrus; IPL: inferior parietal lobule; MFG: middle frontal gyrus; mPFC: medial prefrontal cortex; MTG: middle temporal gyrus; PCC: posterior cingulate cortex; SFG: superior frontal gyrus; SMA: supplementary motor area; SMG: supramarginal gyrus; SOG: superior occipital gyrus; SPL: superior parietal lobule; Op: operculum;</p><p>TCNs were divided into the following groups based on their spatial organization and their activation/deactivation to the task: cingulo-opercular network (CON), fronto-parietal network (FPN), default mode network (DMN), visual (VIS), auditory (AUD), sensorimotor (MOT), and subcortical (SC) networks.</p

Description of the RT-predictive temporally coherent networks (TCNs).

<p>Spatial maps, BOLD activity around the trial onsets, and the relationship between their activity and the response time (RT) for the nine RT-predictive TCNs. (A) dorsal anterior cingulate cortex TCN (IC53); (B) anterior insula TCN (IC38); (C) frontal operculum TCN (IC41); (D) right middle frontal gyrus TCN (IC50); (E) left fusiform gyrus TCN (IC23); (F) right fusiform gyrus TCN (IC24); (G) sensorimotor TCN (IC13); (H) left sensorimotor TCN (IC05); (I) right sensorimotor TCN (IC04). For each TCN, a spatial map (converted to <i>z</i>-score and thresholded with <i>z</i> >3.0) shows its average distribution over all subjects and sessions, sectioned at the highest peak position [with its Montreal Neurological Institute (MNI) coordinates given], and superimposed on the MNI 152 standard space T1 template image. Dots in the BOLD activity represent pre-trial activity (time ≤ 0.0 s) and task response (time > 0.0 s) averaged over the trials in four task sessions for each subject, with the black line showing the grand average over all subjects. The time course for the relationship between activity and RT is shown as the group-averaged time course of estimated coefficients of an analysis of covariance (ANCOVA) model explaining the variance of RT. Error bars in the graphs show standard error of the mean (SEM) over subjects.</p

Description of temporally coherent networks (TCNs) that were partially RT-predictive.

<p>Ten TCNs for which the activity at 0.0< <i>t</i> ≤ 3.0 s from the trial onset significantly explained response time (RT) variability. The format for composite visualization of each TCN is the same as in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0099166#pone-0099166-g004" target="_blank">Figure 4</a>.</p

Functional network connectivity (FNC) between all temporally coherent networks (TCNs) for the ongoing activity time courses in the task sessions.

<p>The residual time course in each TCN of each subject was obtained by regressing out the average response from the back-reconstructed and preprocessed time course, leaving trial-to-trial fluctuation of the ongoing activity in the TCN. For each pair of TCNs, the correlation coefficient was calculated for each subject over sessions, subjected to Fisher’s <i>r</i>-to-<i>z</i> transformation, and averaged over subjects. The asterisks indicate significant connectivity over subjects (two-tailed one sample <i>t</i>-test, <i>p</i><0.001 with control of the false discovery rate [FDR] for all TCN pairs). The solid lines indicate the division of TCNs into network groups. The FNC matrices (see also <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0099166#pone.0099166.s002" target="_blank">Figure S2</a>) also support the division of the FPN into dorsal and ventral parts <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0099166#pone.0099166-Kerns1" target="_blank">[64]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0099166#pone.0099166-Logan1" target="_blank">[29]</a>, as indicated by the dashed lines. See the note below <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0099166#pone-0099166-t001" target="_blank">Table 1</a> for the abbreviations.</p

Experimental paradigm.

<p>(A) The Stroop task for fMRI sessions. In each trial, subjects were required to indicate the position of a surrounding word that names the font color of the central word. All the words used were color–word incongruent. (B) Control task outside the scanner. Subjects were required to simply replicate the directions indicated by the arrows. (C) Distribution of inter-stimulus intervals (ISIs) across trials for both tasks.</p