Understanding the cognitive and neuroimaging bases underlying the detrimental impact of sleep deprivation on reciprocity

Abstract

Although the impact of sleep loss on social behaviors has been widely observed in recent years, the mechanisms underpinning these impacts remain unclear. In this study, we explored the detrimental effects of sleep deprivation on reciprocity behavior as well as its underlying psychological and neuroimaging mechanisms by combining sleep manipulation, an interpersonal interactive game, computational modeling and neuroimaging. Our results suggested that after sleep deprivation, individuals showed reduced reciprocity behavior, mainly due to their reduced weights on communal concern when making social decisions. At neural level, we demonstrated that sleep deprivation's effects were observed in the precuneus (hyperactivity) and temporoparietal junction, dorsal lateral prefrontal cortex (DLPFC) (both hypoactivity), and reduced reciprocity was also accounted for by increased precuneus-thalamus connectivity and DLPFC-thalamus connectivity. Our findings contributed to the understanding of the psychological and neuroimaging bases underlying the deleterious impact of sleep deprivation on social behaviors.

Keywords: Cognitive neuroscience; Techniques in neuroscience.

Graphical abstract

Figure 1

Experimental design The present study was a repeated-measure counterbalanced design with 40 participants. After either of two sleep sessions, levels of vigilance, subjective sleepiness and affective state were measured, followed by a computerized task within the scanner and other computerized tasks outside scanner. PVT, psychomotor vigilance test.

Figure 2

Detailed procedure of the interactive task In each trial, the benefactor decided how much of their endowment to spend (i.e., benefactor’s cost) to reduce the participant’s noise duration. The more the benefactor spent, the shorter the duration of noise stimulus. Participants indicated how much they thought the benefactor expected them to reciprocate (i.e., second-order belief of the benefactor’s expectation for repayment). Participants accepted their help and could reciprocate by allocating monetary points to the benefactor. Unbeknownst to participants, benefactors’ decisions were pre-determined by the computer program. We manipulated the perception of the benefactor’s intentions by providing extra information about whether the benefactor knew that the participant could (i.e., Repayment possible condition) or could not (i.e., Repayment impossible condition) reciprocate after receiving help.

Figure 3

Effects of total sleep deprivation on reciprocity behavior and emotional responses after receiving help (A) Effects of total sleep deprivation on the participant’s reciprocity behavior (i.e., amount of reciprocate) (Two-way repeated measures ANOVA). (B) Effect of total sleep deprivation on different concerns underlying reciprocity behavior using computational model (two-tailed paired t-test/Wilcoxon test). (C) Mediation analysis to assess the relationship between Sleep manipulation and reciprocity behavior, using parameter φ as the mediator (Mediation analysis). (D) Effect of total sleep deprivation on the contributions of self-reported sense of obligation, gratitude and guilt to reciprocity behavior, respectively (Linear mixed model). (E) Mediation analysis to assess the relationship between Sleep manipulation and reciprocity behavior, using gratitude (regression beta) as the mediator (Mediation analysis). (F) Mediation analysis to assess the relationship between Sleep manipulation and reciprocity behavior, using guilt (regression beta) as the mediator (mediation analysis). Error bars indicate standard error of the mean. ∗∗p < 0.01, ∗∗∗p < 0.001, n.s. = p > 0.05. SR, sleep-rested; TSD, total sleep deprivation.

Figure 4

Effects of total sleep deprivation on the brain activation related to reciprocity in Repayment possible and Repayment impossible conditions (A) Whole-brain contrast of total sleep deprivation vs. sleep rested in the Repayment impossible condition. (B) Parameter estimates (beta values) corresponding to the two conditions in two sleep sessions were extracted from precuneus (MNI coordinate: −9, −64, 35) for illustrative purposes (Two-way repeated measures ANOVA). (C) Correlation analysis between activation in left precuneus and parameter φ (Pearson’s correlation analyses). Error bars indicate standard error of the mean. PCC, posterior cingulate cortex; SR, sleep-rested; TSD, total sleep deprivation.

Figure 5

Effects of total sleep deprivation on the TPJ and DLPFC activations related to reciprocity behavior (A and C) Regions of interest of total sleep deprivation vs. sleep rested in the Repayment possible and Repayment impossible conditions. Parameter estimates (beta values) corresponding to the two conditions in two sleep manipulation sessions were extracted from TPJ (MNI coordinate: 48, −52, 31) and DLPFC (MNI coordinate: 39, 8, 38) for illustrative purposes (Two-way repeated measures ANOVA in right). (B and D) Correlation analysis between activation in right TPJ, DLPFC and parameter φ, respectively (Pearson’s correlation analyses). Error bars indicate standard error of the mean. DLPFC, dorsal lateral prefrontal cortex; SR, sleep-rested; TPJ, temporoparietal junction; TSD, total sleep deprivation.

Figure 6

Effects of total sleep deprivation on the reciprocity-related coupling of precuneus-thalamus and DLPFC-thalamus (A and C) Higher functional connectivity between precuneus and thalamus, DLPFC and thalamus were found after receiving help following total sleep deprivation relative to the sleep rested session (Two-way repeated measures ANOVA in right). (B and D) Correlation analysis between precuneus-thalamus connectivity, DLPFC-thalamus connectivity and parameter φ, respectively (Pearson’s correlation analyses). Error bars indicate standard error of the mean. ∗p < 0.05 indicates a significant main effect of Condition. DLPFC, dorsal lateral prefrontal cortex; SR, sleep-rested; TSD, total sleep deprivation.