Sleep duration and resting fMRI functional connectivity: examination of short sleepers with and without perceived daytime dysfunction

Abstract

Background: Approximately 30% of the U.S. population reports recurrent short sleep; however, perceived sleep need varies widely among individuals. Some "habitual short sleepers" routinely sleep 4-6 hr/night without self-reported adverse consequences. Identifying neural mechanisms underlying individual differences in perceived sleep-related dysfunction has important implications for understanding associations between sleep duration and health.

Method: This study utilized data from 839 subjects of the Human Connectome Project to examine resting functional connectivity associations with self-reported short sleep duration, as well as differences between short sleepers with versus without reported dysfunction. Functional connectivity was analyzed using a parcellation covering the cortical, subcortical, and cerebellar gray matter at 5 mm resolution.

Results: Self-reported sleep duration predicts one of the primary patterns of intersubject variance in resting functional connectivity. Compared to conventional sleepers, both short sleeper subtypes exhibited resting fMRI (R-fMRI) signatures consistent with diminished wakefulness, potentially indicating inaccurate perception of functionality among those denying dysfunction. Short sleepers denying dysfunction exhibited increased connectivity between sensory cortices and bilateral amygdala and hippocampus, suggesting that efficient sleep-related memory consolidation may partly explain individual differences in perceived daytime dysfunction.

Conclusions: Overall, current findings indicate that R-fMRI investigations should include assessment of average sleep duration during the prior month. Furthermore, short sleeper subtype findings provide a candidate neural mechanism underlying differences in perceived daytime impairment associated with short sleep duration.

Keywords: environmental stimulation; fatigue; resting functional connectivity; sleep duration.

Figure 1

Regions for which functional connectivity significantly covaried with reported sleep duration. Color scale shows for each ROI how many of the 6,922 connections to other ROIs were correlated with sleep duration. The top 50% of ROIs are colored

Figure 2

Correlation of functional connectivity to sensory/motor cortex and sleep duration. Left: Seeds used for auditory, motor, somatosensory, and visual cortex. Middle: Correlation of functional connectivity to the seed and other regions in the brain. Right: Slices showing significant covariation between functional connectivity to the seed and sleep duration. Slices are in neurological format with subject left on image left. Slice locations: MNI z = −25, z = 20, z = 65

Figure 3

Correlation of sleep duration and functional connectivity between sensory/motor cortex, subcortical, and cerebellar regions. (A) Asterisk (*) denotes connections that were significant for false discovery rate q < .05 over all region pairs. Color scale shows Pearson correlation coefficient between functional connectivity and sleep duration across subjects. (B) Correlation values were obtained from two subject cohorts: n = 475 subjects from the S500 Release, and n = 364 additional subjects from the S900 Release. Scatter plots show comparison of results for the same 4 × 32 ROIs for both subject samples. (C) Relationship between sleep duration and head motion for all 839 subjects is shown. (D) Comparison of correlation with sleep duration for the same 4 × 32 ROIs using two different postprocessing strategies to account for head motion

Figure 4

Principal components of intersubject variance in functional connectivity. (A) The first three principal components are shown representing subject by connection singular vectors. (B) Matrix of 839 subjects × 118 connections used to obtain principal components. (C) Singular values of first five components. (D) Comparison of principal component 2 with relationship of sleep duration and functional connectivity for the same connections

Figure 5

Differences in functional connectivity in self‐reported short sleepers versus conventional sleepers reporting and denying daytime dysfunction. Colored squares satisfied p < .05, uncorrected. Asterisk (*) denotes connections that were significant for false discovery rate q < .05 over all region pairs. Color scale represents t‐statistic for a two‐tailed t‐test of functional connectivity between short and conventional sleepers

Figure 6

Model for effects of sleep duration on functional connectivity in self‐reported short sleepers reporting and denying daytime dysfunction