Enhanced amygdala-cingulate connectivity associates with better mood in both healthy and depressive individuals after sleep deprivation.

Sleep loss robustly disrupts mood and emotion regulation in healthy individuals but can have a transient antidepressant effect in a subset of patients with depression. The neural mechanisms underlying this paradoxical effect remain unclear. Previous studies suggest that the amygdala and dorsal nexus (DN) play key roles in depressive mood regulation. Here, we used functional MRI to examine associations between amygdala- and DN-related resting-state connectivity alterations and mood changes after one night of total sleep deprivation (TSD) in both healthy adults and patients with major depressive disorder using strictly controlled in-laboratory studies. Behavioral data showed that TSD increased negative mood in healthy participants but reduced depressive symptoms in 43% of patients. Imaging data showed that TSD enhanced both amygdala- and DN-related connectivity in healthy participants. Moreover, enhanced amygdala connectivity to the anterior cingulate cortex (ACC) after TSD associated with better mood in healthy participants and antidepressant effects in depressed patients. These findings support the key role of the amygdala-cingulate circuit in mood regulation in both healthy and depressed populations and suggest that rapid antidepressant treatment may target the enhancement of amygdala-ACC connectivity.

Test-retest reliability and time-of-day variations of perfusion imaging at rest and during a vigilance task.

Arterial spin-labeled perfusion and blood oxygenation level-dependent functional MRI are indispensable tools for noninvasive human brain imaging in clinical and cognitive neuroscience, yet concerns persist regarding the reliability and reproducibility of functional MRI findings. The circadian rhythm is known to play a significant role in physiological and psychological responses, leading to variability in brain function at different times of the day. Despite this, test-retest reliability of brain function across different times of the day remains poorly understood. This study examined the test-retest reliability of six repeated cerebral blood flow measurements using arterial spin-labeled perfusion imaging both at resting-state and during the psychomotor vigilance test, as well as task-induced cerebral blood flow changes in a cohort of 38 healthy participants over a full day. The results demonstrated excellent test-retest reliability for absolute cerebral blood flow measurements at rest and during the psychomotor vigilance test throughout the day. However, task-induced cerebral blood flow changes exhibited poor reliability across various brain regions and networks. Furthermore, reliability declined over longer time intervals within the day, particularly during nighttime scans compared to daytime scans. These findings highlight the superior reliability of absolute cerebral blood flow compared to task-induced cerebral blood flow changes and emphasize the importance of controlling time-of-day effects to enhance the reliability and reproducibility of future brain imaging studies.

Morning resting hypothalamus-dorsal striatum connectivity predicts individual differences in diurnal sleepiness accumulation.

While the significance of obtaining restful sleep at night and maintaining daytime alertness is well recognized for human performance and overall well-being, substantial variations exist in the development of sleepiness during diurnal waking periods. Despite the established roles of the hypothalamus and striatum in sleep-wake regulation, the specific contributions of this neural circuit in regulating individual sleep homeostasis remain elusive. This study utilized resting-state functional magnetic resonance imaging (fMRI) and mathematical modeling to investigate the role of hypothalamus-striatum connectivity in subjective sleepiness variation in a cohort of 71 healthy adults under strictly controlled in-laboratory conditions. Mathematical modeling results revealed remarkable individual differences in subjective sleepiness accumulation patterns measured by the Karolinska Sleepiness Scale (KSS). Brain imaging data demonstrated that morning hypothalamic connectivity to the dorsal striatum significantly predicts the individual accumulation of subjective sleepiness from morning to evening, while no such correlation was observed for the hypothalamus-ventral striatum connectivity. These findings underscore the distinct roles of hypothalamic connectivity to the dorsal and ventral striatum in individual sleep homeostasis, suggesting that hypothalamus-dorsal striatum circuit may be a promising target for interventions mitigating excessive sleepiness and promoting alertness.

Locus coeruleus microstructural integrity is associated with vigilance vulnerability to sleep deprivation.

Insufficient sleep compromises cognitive performance, diminishes vigilance, and disrupts daily functioning in hundreds of millions of people worldwide. Despite extensive research revealing significant variability in vigilance vulnerability to sleep deprivation, the underlying mechanisms of these individual differences remain elusive. Locus coeruleus (LC) plays a crucial role in the regulation of sleep-wake cycles and has emerged as a potential marker for vigilance vulnerability to sleep deprivation. In this study, we investigate whether LC microstructural integrity, assessed by fractional anisotropy (FA) through diffusion tensor imaging (DTI) at baseline before sleep deprivation, can predict impaired psychomotor vigilance test (PVT) performance during sleep deprivation in a cohort of 60 healthy individuals subjected to a rigorously controlled in-laboratory sleep study. The findings indicate that individuals with high LC FA experience less vigilance impairment from sleep deprivation compared with those with low LC FA. LC FA accounts for 10.8% of the variance in sleep-deprived PVT lapses. Importantly, the relationship between LC FA and impaired PVT performance during sleep deprivation is anatomically specific, suggesting that LC microstructural integrity may serve as a biomarker for vigilance vulnerability to sleep loss.

Sleep deprivation attenuates neural responses to outcomes from risky decision-making.

Sleep loss impacts a broad range of brain and cognitive functions. However, how sleep deprivation affects risky decision-making remains inconclusive. This study used functional MRI to examine the impact of one night of total sleep deprivation (TSD) on risky decision-making behavior and the underlying brain responses in healthy adults. In this study, we analyzed data from N = 56 participants in a strictly controlled 5-day and 4-night in-laboratory study using a modified Balloon Analogue Risk Task. Participants completed two scan sessions in counter-balanced order, including one scan during rested wakefulness (RW) and another scan after one night of TSD. Results showed no differences in participants' risk-taking propensity and risk-induced activation between RW and TSD. However, participants showed significantly reduced neural activity in the anterior cingulate cortex and bilateral insula for loss outcomes, and in bilateral putamen for win outcomes during TSD compared with RW. Moreover, risk-induced activation in the insula negatively correlated with participants' risk-taking propensity during RW, while no such correlations were observed after TSD. These findings suggest that sleep loss may impact risky decision-making by attenuating neural responses to decision outcomes and impairing brain-behavior associations.

Vigilant attention mediates the association between resting EEG alpha oscillations and word learning ability.

Individuals exhibit considerable variability in their capacity to learn and retain new information, including novel vocabulary. Prior research has established the importance of vigilance and electroencephalogram (EEG) alpha rhythm in the learning process. However, the interplay between vigilant attention, EEG alpha oscillations, and an individual's word learning ability (WLA) remains elusive. To address this knowledge gap, here we conducted two experiments with a total of 140 young and middle-aged adults who underwent resting EEG recordings prior to completing a paired-associate word learning task and a psychomotor vigilance test (PVT). The results of both experiments consistently revealed significant positive correlations between WLA and resting EEG alpha oscillations in the occipital and frontal regions. Furthermore, the association between resting EEG alpha oscillations and WLA was mediated by vigilant attention, as measured by the PVT. These findings provide compelling evidence supporting the crucial role of vigilant attention in linking EEG alpha oscillations to an individual's learning ability.

Cerebellum anatomy predicts individual risk-taking behavior and risk tolerance.

Human risk tolerance is highly idiosyncratic and individuals often show distinctive preferences when faced with similar risky situations. However, the neural underpinnings of individual differences in risk-taking remain unclear. Here we combined structural and perfusion MRI and examined the associations between brain anatomy and individual risk-taking behavior/risk tolerance in a sample of 115 healthy participants during the Balloon Analogue Risk Task, a well-established sequential risky decision paradigm. Both whole brain and region-of-interest analyses showed that the left cerebellum gray matter volume (GMV) has a strong association with individual risk-taking behavior and risk tolerance, outperforming the previously reported associations with the amygdala and right posterior parietal cortex (PPC) GMV. Left cerebellum GMV also accounted for risk tolerance and risk-taking behavior changes with aging. However, regional cerebral blood flow (CBF) provided no additional predictive power. These findings suggest a novel cerebellar anatomical contribution to individual differences in risk tolerance. Further studies are necessary to elucidate the underestimated important role of cerebellum in risk-taking.

Risk-taking in the human brain: An activation likelihood estimation meta-analysis of the balloon analog risk task (BART).

The Balloon Analog Risk Task (BART) is increasingly used to assess risk-taking behavior and brain function. However, the brain networks underlying risk-taking during the BART and its reliability remain controversial. Here, we combined the activation likelihood estimation (ALE) meta-analysis with both task-based and task-free functional connectivity (FC) analysis to quantitatively synthesize brain networks involved in risk-taking during the BART, and compared the differences between adults and adolescents studies. Based on 22 pooled publications, the ALE meta-analysis revealed multiple brain regions in the reward network, salience network, and executive control network underlying risk-taking during the BART. Compared with adult risk-taking, adolescent risk-taking showed greater activation in the insula, putamen, and prefrontal regions. The combination of meta-analytic connectivity modeling with task-free FC analysis further confirmed the involvement of the reward, salience, and cognitive control networks in the BART. These findings demonstrate the core brain networks for risk-taking during the BART and support the utility of the BART for future neuroimaging and developmental research.

Sleep Architecture and Sleep EEG Alterations are Associated with Impaired Cognition Under Sleep Restriction.

Purpose: Many studies have investigated the cognitive, emotional, and other impairments caused by sleep restriction. However, few studies have explored the relationship between cognitive performance and changes in sleep structure and electroencephalography (EEG) during sleep. The present study aimed to examine whether changes in sleep structure and EEG can account for cognitive impairment caused by sleep restriction. Patients and Methods: Sixteen young adults spent five consecutive nights (adaptation 9h, baseline 8h, 1st restriction 6h, 2nd restriction 6h, and recovery 10h) in a sleep laboratory, with polysomnography recordings taken during sleep. Throughout waking periods in each condition, participants completed the psychomotor vigilance test (PVT), which measures vigilant attention, and the Go/No-Go task, which measures inhibition control. Results: The results showed that sleep restriction significantly decreased the proportion of N1 and N2 sleep, increased the proportion of N3 sleep, and reduced the time spent awake after sleep onset (WASO) and sleep onset latency. Poorer performance on the PVT and Go/No Go task was associated with longer WASO, a larger proportion of N3 sleep, and a smaller proportion of N2 sleep. Additionally, the power spectral density of delta waves significantly increased after sleep restriction, and this increase predicted a decrease in vigilance and inhibition control the next day. Conclusion: These findings suggest that sleep architecture and EEG signatures may partially explain cognitive impairment caused by sleep restriction.

Test-Retest Reliability of Resting Brain Small-World Network Properties across Different Data Processing and Modeling Strategies.

Resting-state functional magnetic resonance imaging (fMRI) with graph theoretical modeling has been increasingly applied for assessing whole brain network topological organization, yet its reproducibility remains controversial. In this study, we acquired three repeated resting-state fMRI scans from 16 healthy controls during a strictly controlled in-laboratory study and examined the test-retest reliability of seven global and three nodal brain network metrics using different data processing and modeling strategies. Among the global network metrics, the characteristic path length exhibited the highest reliability, whereas the network small-worldness performed the poorest. Nodal efficiency was the most reliable nodal metric, whereas betweenness centrality showed the lowest reliability. Weighted global network metrics provided better reliability than binary metrics, and reliability from the AAL90 atlas outweighed those from the Power264 parcellation. Although global signal regression had no consistent effects on the reliability of global network metrics, it slightly impaired the reliability of nodal metrics. These findings provide important implications for the future utility of graph theoretical modeling in brain network analyses.

State Boredom Partially Accounts for Gender Differences in Novel Lexicon Learning.

Gender plays an important role in various aspects of second language acquisition, including lexicon learning. Many studies have suggested that compared to males, females are less likely to experience boredom, one of the frequently experienced deactivating negative emotions that may impair language learning. However, the contribution of boredom to gender-related differences in lexicon learning remains unclear. To address this question, here we conducted two experiments with a large sample of over 1,000 college students to explore the relationships between gender differences in boredom and lexicon learning. In Experiment 1, a cohort of 527 participants (238 males) completed the trait and state boredom scales as well as a novel lexicon learning task without awareness of the testing process. In Experiment 2, an independent cohort of 506 participants (228 males) completed the same novel lexicon learning task with prior knowledge of the testing procedure. Results from both experiments consistently showed significant differences between female and male participants in the rate of forgetting words and the state boredom scores, with female participants performing better than male participants. Furthermore, differences in state boredom scores partially explained differences in the rate of forgetting words between female and male participants. These findings demonstrate a novel contribution of state boredom to gender differences in lexicon learning, which provides new insights into better language-learning ability in females.

Resting-state occipito-frontal alpha connectome is linked to differential word learning ability in adult learners.

Adult language learners show distinct abilities in acquiring a new language, yet the underlying neural mechanisms remain elusive. Previous studies suggested that resting-state brain connectome may contribute to individual differences in learning ability. Here, we recorded electroencephalography (EEG) in a large cohort of 106 healthy young adults (50 males) and examined the associations between resting-state alpha band (8-12 Hz) connectome and individual learning ability during novel word learning, a key component of new language acquisition. Behavioral data revealed robust individual differences in the performance of the novel word learning task, which correlated with their performance in the language aptitude test. EEG data showed that individual resting-state alpha band coherence between occipital and frontal regions positively correlated with differential word learning performance (p = 0.001). The significant positive correlations between resting-state occipito-frontal alpha connectome and differential world learning ability were replicated in an independent cohort of 35 healthy adults. These findings support the key role of occipito-frontal network in novel word learning and suggest that resting-state EEG connectome may be a reliable marker for individual ability during new language learning.

Perfusion Imaging of Fatigue and Time-on-Task Effects in Patients With Parkinson's Disease.

Fatigue is a highly prevalent and debilitating non-motor symptom in Parkinson's disease (PD), yet its' neural mechanisms remain poorly understood. Here we combined arterial spin labeling (ASL) perfusion functional magnetic resonance imaging (fMRI) with a sustained mental workload paradigm to examine the neural correlates of fatigue and time-on-task effects in PD patients. Twenty-one PD patients were scanned at rest and during continuous performance of a 20-min psychomotor vigilance test (PVT). Time-on-task effects were measured by the reaction time changes during the PVT and by self-reported fatigue ratings before and after the PVT. PD subjects demonstrated significant time-on-task effects, including progressively slower reaction time on the PVT and increased post-PVT fatigue ratings compared to pre-PVT. Higher levels of general fatigue were associated with larger increases in mental fatigue ratings after the PVT. ASL imaging data showed increased CBF in the right middle frontal gyrus (MFG), bilateral occipital cortex, and right cerebellum during the PVT compared to rest, and decreased CBF in the right MFG at post-task rest compared to pre-task rest. The magnitude of regional CBF changes in the right MFG and right inferior parietal lobe correlated with subjective fatigue rating increases after the PVT task. These results demonstrate the utility of continuous PVT paradigm for future studies of fatigue and cognitive fatigability in patients, and support the key role of the fronto-parietal attention network in mediating fatigue in PD.

Impaired Vigilant Attention Partly Accounts for Inhibition Control Deficits After Total Sleep Deprivation and Partial Sleep Restriction.

PURPOSE: Sleep loss impairs a range of neurobehavioral functions, particularly vigilant attention and arousal. However, the detrimental effects of sleep deprivation on inhibition control and its relationship to vigilant attention impairments remain unclear. This study examined the extent to which vigilant attention deficits contribute to inhibition control performance after one night of total sleep deprivation (TSD) and two nights of partial sleep restriction (PSR). PARTICIPANTS AND METHODS: We analyzed data from N = 49 participants in a one-night of TSD experiment, N=16 participants in a control experiment without sleep loss, and N = 16 participants in a two-nights of PSR experiment (time in bed, TIB = 6 h for each night). Throughout waking periods in each condition, participants completed the psychomotor vigilance test (PVT), which measures vigilant attention, and the Go/No-Go task, which measures inhibition control. RESULTS: After TSD and PSR, participants displayed significantly slower reaction times (RT) and more lapses in PVT performance, as well as slower Go RT and more errors of omission during the Go/No-Go task. PVT deficits accounted for 18.0% of the change in Go RT and 12.4% of the change in errors of omission in the TSD study, and 23.7% of the change in Go RT and 20.3% of the change in errors of omission in the PSR study. CONCLUSION: Both TSD and PSR impaired inhibition control during the Go/No-Go task, which can be partly accounted for by vigilant attention deficits during the PVT. These findings support the key role of vigilant attention in maintaining overall neurobehavioral function after sleep loss.