Differential Impact of Sleep Deprivation and Circadian Timing on Reflexive Versus Inhibitory Control of Attention

Jinny Collet,Sean W Cain,Meaghan Clough,Joanne Fielding,Suzanne Ftouni,Clare Anderson

doi:10.1038/s41598-020-63144-y

Abstract

In a visually stimulating environment with competing stimuli, we continually choose where to allocate attention, and what to ignore. Wake and circadian-dependent modulation of attentional control and resolution of conflict is poorly understood. Twenty-two participants (17males; 25.6 ± 5.6 years) completed ocular motor tasks throughout 40 hours of sleep deprivation under constant routine conditions. A prosaccade task required a reflexive saccade toward a stimulus (no conflict), while an antisaccade task required inhibiting a reflexive saccade to the peripheral stimulus, and looking in the mirror opposite instead (conflict resolution). Antisaccade inhibitory errors showed circadian modulation, being highest in the morning, progressively decreasing until melatonin onset, before returning to the prior morning’s peak throughout the biological night. This diurnal rhythm was blunted by sleep loss (>24 hours), with inhibitory control remaining impaired across the second biological day. For prosaccade, responses slowed down during the biological night. Taken together, we provide evidence for a circadian modulation of attentional bias: the morning being biased toward reflexive responding, and the evening toward higher inhibitory control. Our data show that sleep loss and circadian timing differentially impact attention, depending on whether a response conflict is present (antisaccade) or absent (prosaccade).

Highlights

The capacity to remain vigilant to the environment, and able to quickly respond to relevant stimuli, is critically important to many modern-day activities, such as driving and surveillance of safety-critical systems
Symbols indicate the timing of tests: Crossed circle (⊗) represents the ocular motor battery practice; black circles () represent ocular motor batteries completed during the constant routine; white circles (○) represent additional ocular motor batteries conducted on the baseline and recovery days that are not reported here
Data were collected from 22 participants across 40 h of total sleep deprivation under constant routine[24] conditions; see Fig. 1 for in-laboratory study protocol

Summary

Introduction

The capacity to remain vigilant to the environment, and able to quickly respond to relevant stimuli, is critically important to many modern-day activities, such as driving and surveillance of safety-critical systems. Well-rested individuals performance on this task remains stable across the waking day, followed by a sharp reduction in sustained attention when wakefulness extends beyond 16 hours awake[5,6] This is due to a combination of both wake (e.g., extended time awake without sleep) and circadian factors (e.g., the drive for sleep during the biological night). The STROOP task is non-specific in that it involves multiple cognitive domains, such as attention, processing speed, cognitive flexibility, and working memory[13], which is reflected by the recruitment of a vast array of neural circuitry beyond those networks involved in inhibition[14] Despite these shortcomings, the available literature provides evidence that attentional inhibitory control may be by modulated by the circadian clock. While this provides key evidence of our hypothesis, the measure of inhibition used by Burke and colleagues was speed-based [( the difference between congruent (facilitation) and incongruent (interference) median reaction times for correct trials] which represents the cost of inhibition, rather than response inhibition accuracy; this is best captured in terms of the number of inhibition failures, such as error rate for incongruent trials[13]

Methods

Results

Conclusion