Long-Term Effects of Attentional Performance on Functional Brain Network Topology

<div><p>Individuals differ in their cognitive resilience. Less resilient people demonstrate a greater tendency to vigilance decrements within sustained attention tasks. We hypothesized that a period of sustained attention is followed by prolonged changes in the organization of “resting state” brain networks and that individual differences in cognitive resilience are related to differences in post-task network reorganization. We compared the topological and spatial properties of brain networks as derived from functional MRI data (N = 20) recorded for 6 mins before and 12 mins after the performance of an attentional task. Furthermore we analysed changes in brain topology during task performance and during the switches between rest and task conditions. The cognitive resilience of each individual was quantified as the rate of increase in response latencies over the 32-minute time course of the attentional paradigm. On average, functional networks measured immediately post-task demonstrated significant and prolonged changes in network organization compared to pre-task networks with higher connectivity strength, more clustering, less efficiency, and shorter distance connections. Individual differences in cognitive resilience were significantly correlated with differences in the degree of recovery of some network parameters. Changes in network measures were still present in less resilient individuals in the second half of the post-task period (i.e. 6–12 mins after task completion), while resilient individuals already demonstrated significant reductions of functional connectivity and clustering towards pre-task levels. During task performance brain topology became more integrated with less clustering and higher global efficiency, but linearly decreased with ongoing time-on-task. We conclude that sustained attentional task performance has prolonged, “hang-over” effects on the organization of post-task resting-state brain networks; and that more cognitively resilient individuals demonstrate faster rates of network recovery following a period of attentional effort.</p></div

Changes in nodal network clustering over resting state fMRI periods.

<p><b>Top:</b> Clustering changed over the three resting state fMRI periods. Following task performance all brain regions show higher clustering or cliquishness. <b>Bottom left:</b> Significantly different changes in clustering at nodal level (yellow) were evident among others in visual cortex and basal forebrain; brain areas involved in the processing of visual sustained attention tasks. <b>Bottom right:</b> Significant changes in clustering in the post-task phase that were related to vigilance decline were found among others in the thalamus (red).</p

Experiment design.

<p><b>Top:</b> Order of the resting state (RS) and task periods (T) with the number of acquired whole brain scans. The task was separated from the resting state periods by brief instructions. Task periods (T1 to T5) were continuously measured and later split up into five scan periods with the same length. The post-task resting state period (RS2 and RS3) was also measured continuously and split up later for the analyses. The changes from the first resting state period (RS1) to the first task period (T1) as well as from the last task period (T5) to the first post-task resting state period (RS2) are referred to as ‘task switch’. <b>Bottom:</b> Scheme of the vigilance task during the task period. Participants were instructed to detect a red fixation cross (here depicted in bold).</p

Pairwise comparisons of resting state data: Effects on (i) mean connectivity strength, (ii) network topology, (iii) physical distances and (iv) its correlations with performance.

(a)<p>Change between resting states, paired t-tests, df = 19.</p>(b)<p>Differences between resting states correlated with individual vigilance decrements.</p>(c)<p>Group comparison between attentionally impaired and resilient subjects (see text), two-sample t-tests, df = 18.</p

Illustration of parcellation routine for seed region/node definition.

<p>Cortical and subcortical brain regions were parcellated into 442 brain nodes. (<b>A</b>) The parcellation routine was based on an anatomically parcellated and labeled T1 volume provided by the AAL toolbox (Tzourio-Mazoyer et al., 2002). (<b>B</b>) The parcellation routine randomly and homogenously split the larger AAL regions into 442 smaller subparcels while preserving the macro-anatomical borders as defined in the AAL-template. (<b>C</b>) This parcellation approach creates more homogenous seed region sizes as compared to the original AAL-template so that possible biasing effects of parcel sizes on functional connectivity (Salvador et al., 2008; Fornito et al., 2010) were prevented. The main statistical analyses were repeated with alternative templates in order to assure that the reported effects of the RS data analysis were not driven by a singular parcellation template (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0074125#pone.0074125.s001" target="_blank">File S1</a>).</p

Pairwise comparisons of resting state and task data before and following task switches (R1, T1, T5 and R2): Effects on (i) mean connectivity strength, (ii) network topology, (iii) physical distances.

(a)<p>Paired t-tests, df = 19.</p>(b)<p>T-tests based on averaged values for RS1/T1, respectively T5/RS2.</p

Vigilance decrements in the attentional task.

<p>(<b>A</b>) Median reaction times averaged across subjects for each of the 96 target presentations during the task are shown. Solid line: The robust fit regression showed a significant RT increase/vigilance decrement. (<b>B</b>) On the individual level, participants showed a large variability in their change in RTs during task performance. For each subject, the individual robust fits for the RTs were used to estimate the RT change at the end of the task. For illustration we divided the participants into a group with significant RT increase (red, referred to as ‘attentional impaired’ subjects) and without a significant RT increase (blue, referred to as ‘attentional resilient’ subjects). However, to test the correlation between network parameters and behavioural performance without loss of information, the individual RTs increases were used and tested for a linear relationship.</p

Mixed-effects analysis of task data: Effects of time-on-task on (i) mean connectivity strength, (ii) functional network and (iii) physical distance metrics.

(a)<p>corrected for unequal variances.</p

Changes in connectivity strength and network topology during the post-task resting state period (RS2 vs. RS3) and relation with behavioural performance; Changes in the histogram of physical distances.

<p>(<b>A–C</b>) Correlation between post-task changes (RS3-RS2) and individual performance. (<b>A</b>) Connectivity strength: More attentional resilient subjects (blue, subjects with low vigilance decrements) show a reduction in connectivity strength from RS2 to RS3, whereas impaired subjects (red) show a further increase. (<b>B</b>) Changes in global efficiency from RS2 to RS3 did not correlate with performance. (<b>C</b>) <b>Changes in</b> clustering during the post-task phase significantly correlated with individual performance. Resilient subjects (blue) show decreases in clustering from RS2 to RS3, impaired subjects (red) further increase in clustering. (<b>D</b>) Change in histogram of mean distances between nodes following task performance (RS1 vs. RS2): The number of connections were counted in 32 distance bins of 5 mm (ΔN: differences in the number of connections). <b>Top:</b> Following task performance the number of short distances significantly increased and the number of longer distance connections significantly decreased at all cost levels. Significance is indicated by the grey patches at the top of the figure (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0074125#pone.0074125.s002" target="_blank">File S2</a> for a 2D version of this plot). Note that graphs at higher cost levels comprise the edges from graphs at lower cost levels which lead to larger differences in the number of connections at higher cost levels (ΔN). <b>Bottom:</b> Distance changes at 50% cost level: impaired subjects (red) showed a more pronounced (but not significant) shift towards shorter connections following the task as compared to more resilient subjects (blue).</p

Demographic and clinical characteristics of the participants.

<p>IQ, intelligence quotient; YIAS, Young Internet Addiction Scale</p