Sleep deprivation alters task-related changes in functional connectivity of the frontal cortex: A near-infrared spectroscopy study.

Peter Mukli,György Purebl,Orestis Stylianou,Jeremy M Kellawan,Cameron D Owens,Farzaneh A Sorond,Agnes Lipecz,Zoltan I Ungvari,Andriy Yabluchanskiy,Jonathan W Perry,Anna Csiszar,Tamas Csipo,Stefano Tarantini,William E Sonntag,Yuan Yang,Frigyes Samuel Racz

doi:10.1002/brb3.2135

Abstract

Sleep deprivation (SD) is known to be associated with decreased cognitive performance; however, the underlying mechanisms are poorly understood. As interactions between distinct brain regions depend on mental state, functional brain networks established by these connections typically show a reorganization during task. Hence, analysis of functional connectivity (FC) could reveal the task‐related change in the examined frontal brain networks. Our objective was to assess the impact of SD on static FC in the prefrontal and motor cortices and find whether changes in FC correlate with changes in neuropsychological scores. Healthy young male individuals (n = 10, 27.6 ± 3.7 years of age) participated in the study. A battery of tests from the Cambridge Neuropsychological Test Automated Battery (CANTAB) and 48 channel functional near‐infrared spectroscopy (fNIRS) measurements were performed before and after 24 hr of SD. Network metrics were obtained by graph theoretical analysis using the fNIRS records in resting state and during finger‐tapping sessions. During task, SD resulted in a significantly smaller decrease in the number and strength of functional connections (characterizing FC) in the frontal cortex. Changes in the global connection strengths correlated with decreased performance in the paired association learning test. These results indicate a global impact of SD on functional brain networks in the frontal lobes.

Highlights

Sleep is a vital homeostatic function (Tononi, 2012) for the central nervous system (CNS), and poor quality of sleep has been a growing health problem in Western countries (Chattu et al, 2018)
To test the hypothesis that after sleep deprivation, task-related changes of static functional connectivity (FC) are different compared to the nonsleep-deprived state, we examined the FC by applying a finger- tapping paradigm that is considered to activate specific regions of the motor cortex
Our results demonstrated the impact of 24-hr sleep deprivation on the global properties of frontal lobe networks when investigating resting-state functional connectivity and its alteration in response to a finger-tapping paradigm assessed by functional near-infrared spectroscopy (fNIRS)

Summary

Introduction

Sleep is a vital homeostatic function (Tononi, 2012) for the central nervous system (CNS), and poor quality of sleep has been a growing health problem in Western countries (Chattu et al, 2018). Besides the direct effect on the CNS, abundant studies demonstrate that SD is associated with an increased risk of obesity, type 2 diabetes mellitus, and other cardiovascular conditions through, possibly, a profound effect of SD on metabolic processes (Reutrakul & Van Cauter, 2018). Impaired CNS functioning negatively affects general health, which leads to sleep disturbances (Muscogiuri et al, 2019) and increases the risk of SD. These interactions create a vicious circle, which may escalate the negative consequences of SD. Despite its prevalence and clinical importance, the mechanisms underlying sleep deprivation-induced decline in cognitive performance are poorly understood

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