Neural correlates of dynamic changes in working memory performance during one night of sleep deprivation

Abstract

Total sleep deprivation (TSD) is common in modern society leading to deterioration of multiple aspects of cognition. Dynamic interaction effect of circadian rhythmicity and homeostatic sleep pressure on sustained attention have been intensively investigated, while how this effect was represented on performance and cerebral responses to working memory, another important element of many neurobehavioral tasks, was not well elucidated. Thirty-six healthy subjects with intermediate chronotype performed the Sternberg working-memory task (SWMT) while undergoing functional magnetic resonance imaging every 2 hr from 10:00 p.m. on the first day to 6:00 a.m. on the second day. Using data from three imaging sessions (10:00 p.m., 04:00 a.m., and 06:00 a.m.), we found that the slowest SWMT reaction time and weakest cerebral responses were not at the end of TSD (06:00 a.m.) but during the early morning (04:00 a.m.) hours of the TSD. In addition, during this worst period of TSD, reaction time for the SWMT were found to be negatively correlated with task-related activation in the angular gyrus and positively correlated with the degree of negative correlation between the control and default networks. Our results revealed a rebound of SWMT reaction time and cerebral responses after the mid-time point of regular biological sleep night and provided more evidence that different cognitive tasks are differentially affected by sleep loss and circadian rhythmicity. K E Y W O R D S dynamic changes, rebound response, sleep deprivation, working memory 1 | INTRODUCTION A single night of total sleep deprivation (TSD) produces a range of fundamental neurocognitive deficits and is associated with serious outcomes (Basner, Rao, Goel, & Dinges, 2013; Lim & Dinges, 2010). To understand the neural underpinnings of TSD-related deterioration within a specific cognitive domain, most imaging studies typically conduct two imaging sessions for each participant, one after TSD and the other after rested wakefulness (RW). The neurocognitive consequences of TSD were largely explained by comparing the differences in brain activity between these two sessions (Durmer & Dinges, 2005; Goel, Rao, Durmer, & Dinges, 2009). However, these types of observations describe modulated cerebral responses rather than the process through which the modulation occurs. A recent study exploring 13 repeated functional magnetic resonance imaging (fMRI) sessions during 42 hr of TSD found differential results for cortical and subcortical responses during a psychomotor vigilance task (PVT) and greatly expanded our understanding of how sustained attention deteriorates during TSD (Muto et al., 2016). Thus, to better understand how sleep deprivation impairs cognitive performance, increasing the numbers of sessions and investigating dynamic changes in behavioral and cerebral responses is critical. Yuanqiang Zhu, Yibin Xi, Jinbo Sun, Fan Guo authors contributed equally to this work.

High-Frequency Repetitive Transcranial Magnetic Stimulation Could Improve Impaired Working Memory Induced by Sleep Deprivation

“…Furthermore, for total SD, the worst negative effects were not at the end of the total SD but during the mid-time point in which data of the working memory test were collected at three time points (10:00 PM, 04:00 AM, and 06:00 AM). The slowest reaction time of the working memory task and the weakest cerebra response were actually detected during the early morning (04:00 AM) [14]. However, at the end of the SD period (6:00 AM), the reaction time was still significantly slower than that before SD which indicates the significant damage on working memory after SD in self-controlled studies.…”

“…Growing evidence has demonstrated the critical impairments of SD on various cognitive abilities, especially on working memory both in younger and older healthy adults, after total SD or partial SD [14,15,[39][40][41][42][43]. Behavioral results of almost all these past studies found that subjects showed a significantly lower response accuracy rate, longer reaction time, and higher lapse rate on the working memory test after SD 4…”

“…These influences on cerebral responses show hyperactivation or lower activation which were most prominent in cognition-related brain areas involving the prefrontal cortex, parietal lobe, cingulate gyrus, thalamus, angular gyrus, hippocampus, and cerebellum [2, 10-12, 14, 15]. In particular, the activation of the angular gyrus and thalamus was reported significantly associated with the deterioration of behavioral performances [12,14].…”

Functional Connectivity Combined With a Machine Learning Algorithm Can Classify High-Risk First-Degree Relatives of Patients With Schizophrenia and Identify Correlates of Cognitive Impairments

“…Preprocessing of the RS-fMRI data and the calculation of FC measures were performed in a similar manner to those described in previous studies (Zhu et al, 2019;Song et al, 2020). The first 10 images were discarded to ensure MRI data stability (Yuan et al, 2016), and then the remaining 230 images were slice timing corrected and realigned to the first image, during which the average frame-wise displacement (FD) was obtained (no differences in this were found across the three groups; see Table 1).…”

Alteration of Brain Gray Matter Density After 24 h of Sleep Deprivation in Healthy Adults

“…Further studies are required to explore the restoration effect of sleep recovery on brain structure. Third, recent studies have reported that behavioral performance and task-related neural responses were dynamically changed during SD ( Muto et al, 2016 ; Zhu et al, 2018 , 2019 ). Further studies should investigate the dynamic changes in GMD during one night of SD.…”