Chenhao Wang1, Ju Lynn Ong1, Amiya Patanaik1, Juan Zhou1,2, and Michael W. L. Chee1
1Neuroscience and Behavioral Disorders Program, Duke-NUS Graduate Medical School Singapore, Singapore, Singapore, 2Clinical Imaging Research Center, Agency for Science, Technology and Research, Singapore, Singapore
Synopsis
To
elucidate relationship between fluctuation in functional connectivity and behavior
we estimated dynamic connectivity states (DCS) from task-free fMRI obtained
from sleep-deprived healthy young adults. Using spontaneous eye closures as a
proxy for vigilance, we identified two DCS that were associated with high and low
arousal respectively. DCS exhibiting similar connectivity patterns
were also observed when individuals were performing an auditory vigilance task.
Dwell time in high or low arousal DCS predicted task performance. Additionally,
fluctuations in DCS and task response time were correlated. Fluctuations in
functional connectivity appear to be related to spontaneous changes in arousal that
affect vigilance.Purpose
Time varying functional connectivity detected using task-free fMRI exhibits recurring patterns that constitute distinct dynamic connectivity states (DCS)
1. Although the range of functional connectivity states is reduced with lowered levels of consciousness
2,3, few studies have directly correlated DCS with behavior. Here we used spontaneous eyelid-closures (SEC) on sleep deprived persons as a proxy for vigilance to identify DCSs that correlate with greater and lesser levels of arousal
4,5. We then sought to test if spontaneous shifts into high or low arousal DCS would correspond to behavior during a vigilance task.
Methods
Young
adults underwent task-free fMRI scans as well as scans performed during an
auditory vigilance task after being kept awake for ~24 hours. Video recordings
of the eyes during task-free scans were assigned scores ranging from 1-closed to
9-open. Whole-brain dynamic functional connectivity between
126 predefined regions
6 in task-free fMRI were
estimated using 40s wide, sliding-window correlation, shifted in steps of 1 TR
(2 sec). This was followed by K-means
clustering to estimate centroids of DCSs. We then correlated the
occurrence probability of each DCS with the concurrent SEC ratings to identify
if any of them were associated with SEC changes. DCSs derived from task fMRI
were estimated using an identical approach and were matched to their task-free
fMRI counterparts. Matched DCSs were used to predict task performance.
Results
From the 9
DCSs estimated from task-free fMRI, we identified 2 extreme DCS (Figure 1). At
one extreme was a DCS corresponding to a state of low arousal with high
likelihood of behavioral lapses (associated with closed eyelids). At the other extreme
was a DCS corresponding to a state of high arousal (associated with wide open
eyelids) characterized by increased intra-network connectivity involving
default mode, control, attention and salience networks, and increased
anti-correlations between default mode and attention networks. The high and low
arousal task-related DCSs were highly similar in configuration to their task-free
counterparts. Participants who spent more time in the high
arousal DCS had fewer behavioral lapses (rho = -0.548, p = 0.003), whereas more time in the low arousal DCS
predicted a higher lapse rate (rho = 0.465, p = 0.022). The fluctuation between
high and low arousal DCSs correlated with fluctuation in response times.
Discussion and Conclusion
Functional
connectivity during periods of high arousal (proxied by way of eyelid opening)
is characterized by elevated levels of intra- and inter-network connectivity
and anti-correlation between networks that have been shown to be crucial in
management of attentional resources, detection of salient stimuli and
coordination of externally and internally oriented cognitive processes
7-9. The distinct patterns between high and low arousal
DCSs resemble functional connectivity changes reported in sleep deprived
subjects
10-12. We
demonstrate that a significant behavioral accompaniment of fluctuating
functional connectivity is fluctuation in arousal that is in turn accompanied
by eyelid closure and slower responding.
Acknowledgements
The study was supported by grants from National Medical Research Council, Singapore (NMRC/STaR/0004/2008 and NMRC/STaR/0015/2013) awarded to Micheal W. L. Chee and the Duke-NUS Graduate Medical School, Singapore (block grant) awarded to Juan Zhou.References
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