Impact of total sleep deprivation and related mood changes on approach-avoidance decisions to threat-related facial displays

Abstract

Study Objectives Total sleep deprivation is known to have significant detrimental effects on cognitive and socio-emotional functioning. Nonetheless, the mechanisms by which total sleep loss disturbs decision-making in social contexts are poorly understood. Here, we investigated the impact of total sleep deprivation on approach/avoidance decisions when faced with threatening individuals, as well as the potential moderating role of sleep-related mood changes. Methods Participants (n = 34) made spontaneous approach/avoidance decisions in the presence of task-irrelevant angry or fearful individuals, while rested or totally sleep deprived (27 hours of continuous wakefulness). Sleep-related changes in mood and sustained attention were assessed using the Positive and Negative Affective Scale and the psychomotor vigilance task, respectively. Results Rested participants avoided both fearful and angry individuals, with stronger avoidance for angry individuals, in line with previous results. On the contrary, totally sleep deprived participants favored neither approach nor avoidance of fearful individuals, while they still comparably avoided angry individuals. Drift-diffusion models showed that this effect was accounted for by the fact that total sleep deprivation reduced value-based evidence accumulation toward avoidance during decision making. Finally, the reduction of positive mood after total sleep deprivation positively correlated with the reduction of fearful display avoidance. Importantly, this correlation was not mediated by a sleep-related reduction in sustained attention. Conclusions All together, these findings support the underestimated role of positive mood-state alterations caused by total sleep loss on approach/avoidance decisions when facing ambiguous socio-emotional displays, such as fear.

Effects of 24-h acute total sleep deprivation on physiological coupling in healthy young adults

“…Findings of a stress test simulating a military march also supported the contention that one-night sleep deprivation presents no obvious effects on physical and physiological responses ( Nieto-Jiménez and Orellana, 2020 ). Moreover, deprivation of sleep has been known to affect brain functions ( Patrick et al, 2017 ; Hudson et al, 2020 ; Garbarino et al, 2021 ; Grèzes et al, 2021 ). In addition, recent studies reported a decrease in respiratory motor output by altering its cortical component with a subsequent reduction of inspiratory endurance while being deprived of one-night sleep ( Westphal et al, 2021 ).…”

Spontaneous instrumental avoidance learning in social contexts

“…We suggested that such an influence was mediated by the fact that threat displays increased the value of the action leading to avoidance (Vilarem et al, 2020). We revealed that avoidance decisions did indeed result from rapid and implicit value-based competition between action alternatives, a mechanism sourced in the ventromedial prefrontal and the orbital cortices (Mennella et al, 2020; for a conceptual replication see Buades-Rotger et al, 2021) and modulated by changes in participants' positive affective state (Grèzes et al, 2021).…”

“…The main task (Fig. 1) was adapted from previous studies (Grèzes et al, 2021;Mennella et al, 2020;Vilarem et al, 2020).…”

“…Therefore, previous experience informs us that angry expressions might function as ready-to-go signals that help us predict and avoid possible future negative consequences. The aversive motivational value of angry expressions is evidenced through their associated perceptual and attentional advantages (e.g., Carretié, 2014;Fox & Damjanovic, 2006;Hansen & Hansen, 1988;Pourtois et al, 2013;Vuilleumier, 2005), induced physiological changes (Noordewier et al, 2020;Roelofs et al, 2010) as well as their influence on the anticipatory processing of action intentions (Kroczek et al, 2021) and action selection (Grèzes et al, 2021;Mennella et al, 2020;Vilarem et al, 2020), even in the absence of awareness (Vetter et al, 2019). To our knowledge, while the influence of social threat displays on specie-specific defensive behaviours, such as freezing (Roelofs, 2017), or on stimulus-driven avoidance tendencies (Hammer & Marsh, 2015;Krypotos et al, 2014;Marsh et al, 2005) has been established, it remains unknown as to whether they can drive instrumental CS-avoidance learning.…”

“…That is, consistently with previous results on humans showing that successful avoidance is intrinsically rewarding (H. Kim et al, 2006), we propose that the outcome "avoiding anger" is preferred to "approaching anger", and, as such, will act as a reinforcer to promote instrumental CS-avoidance learning. To test our hypothesis, we converted our original free choice paradigm (Grèzes et al, 2021;Mennella et al, 2020;Vilarem et al, 2020) into a reinforcement-learning (RL) task. Standard RL tasks require subjects to explicitly maximize their reward, often in terms of maximising points/money gains or minimising points/money losses.…”