Functional Magnetic Resonance Imaging Of Sleep Deprivation Affecting Brain Cognitive Function

Sleep deprivation(SD) is defined as a state of multiple deficits of cognitive performance resulting from sleep loss, along with a series of psychological and physiological dysfunction. With the intensified fierce resistance, suddenness, and tension of modern high-tech war, military personnel are often in the state of sleep deprivation. The effect of mental fatigue caused by SD are most prominent for special arms, especially military personnel manipulating sophisticated weapons. In the new era of revolution in military affairs, how to improve the most critical and most vulnerable part – the operator’s ability to maximize the performance of military equipment has become an important subject of military psychology. Therefore, revealing the critical neural mechanism of how SD affects cognitive performance and developing effective intervention strategy against SD have become one of the major issues. The study in this dissertation is sponsored by eleventh and twelfth Five-year Plan in military, aiming to build total sleep deprivation model, reveal the characteristics and mechanisms of cognitive impairment caused by sleep deprivation, provide theoretical evidences for the construction and evaluation of cognitive impairment in military. This work will promote the progress of military protection policies of cognitive function and cognitive disorders treatment, and play an active role to enhance the combat effectiveness of military operations.MethodFifty-one healthy volunteers were recruited in this experiment with self controlled design and divided into two groups. Using functional magnetic resonance imaging(fMRI), we investigated the variable pattern of the brain involved with SD in energy allocation, large-scale interactions between the brain’s intrinsic connectivity networks(ICNs), resting-state emotional network and risky decision making using functional magnetic resonance imaging(fMRI).Results1. Effects of SD on spontaneous activity of brainFunctional connectivity density(FCD), regional homogeneity(ReHo) and fractional amplitude of low-frequency fluctuation(fALFF) were used to study how SD impacted the spontaneous activity of brain. We investigated the variable pattern of FCD, ReHo and fALFF after SD, and analyzed the relationship between different indexes and alertness. We found(1) decreased FCD, ReHo and fALFF were located in dorsolateral prefrontal cortex, medial prefrontal cortex, posterior cingulate cortex, precuneus, and inferior parietal lobule after SD;(2) increased FCD, ReHo and fALFF were found in postcentral gyrus, temporal gyrus, thalamus, and occipital cortex after SD;(3) the changes of FCD, ReHo, and fALFF after SD significantly correlated with each other and(4) the decreased short-term FCD in posterior cingulate cortex was significantly correlated with the performance of psychomotor vigilance test. The results revealed that SD may lead to increased energy metabolism in sensory processing areas and decreased energy metabolism in areas in charge of advanced cognitive function.2. Effects of SD on the interaction of large-scale brain networksBased on the triple network model, we investigated the neural mechanism on which SD impacts the large-scale interactions between the brain’s ICNs—default mode network(DMN), executive control network(ECN), and salience network(SN). Independent component analysis(ICA) was firstly conducted to obtain the network components of DMN, ECN and SN. Dual-regression analysis was then applied to obtain the time course of each component. The results showed(1) the coupling strength between DMN and SN was significantly increased after 36 h of SD;(2) the coupling strength between DMN and SN was positively correlated with both the visual analogue scale score of sleepiness and the reaction time of working memory task, and negatively correlated with the percent correct of working memory task. According to these findings, we suggested the potentiality of SN-DMN coupling strength to be a neuroimaging biomarker for evaluating the mental fatigue.3. Effects of SD on emotional networkSeed-based functional connectivity analysis was used to investigate how SD shaped the emotional network of the resting brain. As amygdala is a structurally and functionally heterogeneous nucleus with three subregions—centromedial amygdala(CMA), basolateral amygdala(BLA), and superficial amygdala(SFA), we took each of these regions as the seed to do functional connectivity analysis. Our results revealed(1) SD had distinct impact on the functional connectivity pattern of each subregion;(2) the functional connectivity between SFA and medial prefrontal cortex was significantly correlated with the mood state and(3) the decreased coupling strength between amygdala and regions in executive control network, and the increased coupling strength between amygdala and regions in default model network may contribute to the emotional disturbance among sleep-deprived participants.4. Effects of SD on the risk-taking propensityBalloon analogue risk task(BART) was used to study the neural mechanism underlying how SD influences risky decision-making behaviors with a changing risk level. First, general linear model(GLM) was used to find the activation involved with risk level, reward and punishment. Then, psychophysiological interaction(PPI) analysis was used to study the functional connectivity pattern of posterior cingulate cortex during risky decision making. Our results showed(1) SD affected the left inferior frontal gyrus(IFG) activity under a continuously changing risk level, with a significant correlation between changes in brain activation and that of risk-taking propensity;(2) ventral striatum and thalamus showed increased activation for the cash out choices after SD;(3) decreased activation were found in the right middle temporal gyrus for explosion regressor in sleep-deprived participants;(4) the changed risktaking propensity in the SD session was related to that of the posterior cingulate cortex(PCC)-ventromedial prefrontal cortex(vmPFC) coupling and(5) the left IFG activity had a mediation effect on the relationship between vmPFC-PCC coupling and risk-taking propensity.ConclusionsIn summary, our study indicated the variable pattern of spontaneous activity in the brain after SD from the perspective of energy allocation and large-scale interactions of the brain’s ICNs using fMRI, providing more neuroimaging evidences for the cognitive resource allocating hypothesis of SD. Furthermore, we found the characterized network pattern of emotion shaped by SD, and this is the first time that the left IFG has come to the forefront in SD-induced alterations of brain activation with a changing risk level. The results are important for understanding of the neural mechanism on which SD impacts the cognitive performance and developing effective intervention strategy against SD.