Sleep loss and lack of social interaction: a summary interview

Abstract

Sleep loss is popular in modern society, and this health problem may further lead to social dysfunctions. In this article, we present some interesting behavioral and fMRI studies in the field of sleep and social functions. In light of these studies, we provide a dynamic framework for understanding the relationship between sleep loss and social interaction. In this framework, four sequential stages construct a life circle of interaction. The effects of sleep loss have distinct functions in each stage and correspond to different brain networks. These functions include the desire for social interaction, social withdrawal, subjective perceptions of social relationships, and loneliness. More importantly, we identify the core behavioral factors may be sleepiness, social-emotional processing, memory control, and rumination. For the brain networks, default mode network, negative affective network, inhibitory control network, and near-space networks may contribute to the relation between sleep loss and social interaction. In the future, experiments based on ecological sampling, and tracking studies based on the life cycle of interaction may be helpful for our understanding of this framework. The applications of some new technologies such as brain stimulation and neural feedback can be taken at different stages of social interactions.

KEYWORDS::

• Sleep deprivation
• social relationships
• social pain
• loneliness
• brain networks

1. Introduction

Human beings are born to be socially connected. Desires for social interaction and behaviors to initialize and maintain social activities are critical to building up new relationships. High-quality and sufficient social networks are considered to be important contributors to mental and physical well-being [1]. Feeling socially connected predicted less possibility to experience sleep problems [2] and decreased mortality risks [3].

Approximately 30% of healthy adults received less than 6 h of sleep a night [4]. Total sleep deprivation, partial sleep restriction and poor sleep quality consists of sleep loss. And unoccupied night-time hours may result in impaired cognitive and emotional functions during the day [5]. Recently, the literature has tended to focus on the social side of sleep, trying to understand the correlation between sleep and social functions. However, few studies have investigated whether and how sleep loss influence social functions in this field of study.

The current review builds on prior studies to discuss the potential role of sleep on the social side, especially the establishment and maintenance of social relationships, and perspective of their social situations. A dynamic framework is provided for understanding the relationship between sleep loss and social functions. First, relevant studies are organized based on the life cycle of social interaction, which ranges from desires for social interaction, socio-emotional processing during social interaction, and feelings after social interaction to long-term effects caused by social interaction. Then, the brain networks involved in these processes are mentioned.

2. Sleep loss and aversive consequences in the social interaction

The whole cycle of social interaction can be divided into four stages: planning, interacting, memorializing [6], and long-term phases. The planning phase happens before interactions, including social preparation behaviors. The interacting phase refers to some critical elements during social interaction (e.g. who was there, what happened, how it happened, etc.). Memorializing phase after the interaction highlights whether this interaction was remembered. The present theoretical framework builds on the prior one and emphasizes the socioemotional function at each stage (Figure 1).

Figure 1. The framework of sleep loss causes social dysfunctions at different stages of social interaction. The gray words show a reduction or decrease, and the black words show an increase. The black dots show an activation increase, and the gray one refers to an activation decrease. Solid lines indicated exaggerated coupling, and dashed lines indicated weakened functional connectivity. A, B, and C indicate functional changes in the brain network by frontal and sagittal planes (details in Figure 2), and D indicates structural changes by labeling the core region of the default network with a frontal plane.

2.1. Planning phase

It is shown that sleep-deprived individuals are likely to avoid social behaviors and stay alone at the beginning of social interaction. Those who experienced longer sleep onset time, broken sleep continuity, and lower sleep quality were supposed to have fewer connections with others [7]. Subjects were more willing to do more sleep-preparation activities at home rather than social activities after 24 h sleep deprivation [8]. Sleepiness followed by disrupted sleep seems to be a critical factor that motivates people to perform resource conservation activities. As is shown in the 3-week diary research, greater sleepiness predicted less social activities substantially [9]. Another behavioral factor that matters may be intrusive thoughts. Sleep deprivation leads to failure in suppressing unwanted information [10]. Unwanted memories of negative social events previously experienced may uncontrollably come to their mind. As a result, they will hold negative expectations at the beginning of social interaction. In addition to avoiding social activities, sleep-deprived individuals were less appealing to others in social situations [11]. The opportunities and behaviors to build social connections were decreased as a consequence of sleep loss.

2.2. Interacting phase

During the interacting phase, the lack of sleep leads to hypervigilance toward social threats and causes feelings of vulnerability in social contexts.

People were more likely to move away from high-threat stimuli toward low-threat stimuli, as the self-protective implication of interpersonal distance [12]. Comfort interpersonal distance paradigm (CID) is the most popular measure for personal space [13], and this is also known as the stop-distance paradigm [14]. In the task, participants stand 3 m away from the experimenters, then walk towards or be passively approached by the experimenter until they report discomfort (Figure 2(A)). However, the sleep-deprived has a lower threshold for threatening stimulus during social interaction. Subjects who experienced sleep deprivation classified most neutral faces as threatening in the threat discrimination task [15]. And they preferred larger social distance in CID [14]. They also showed difficulties in recognizing happy and sad faces in a face impression classification task [16]. These emotions are highly related to involvement in prosocial interpersonal interactions.

Figure 2. Experimental design in the interacting phase. (A) Comfortable interpersonal distance; (B) cyberball task; (C) first impression task (photo presented here is virtual character from http://seeprettyface.com/mydataset_page2.html#mulu).

Besides, individuals were shown to have more negative affective behaviors during social activities after sleep restrictions [17]. Social pain is one of the negative consequences of sleep loss. It is a neuropsychological response induced by negative social events that impair the perception of social relationships, such as social rejection, social exclusion, and negative social evaluation [18]. Rejections by a partner were associated with stronger feelings of hurt in those with lower sleep quality and shorter sleep duration [19]. And self-reported poor sleep quality predicted stronger negative emotions during negative social feedback in an experimental study of 2338 participants [20]. Whereas, subjects experiencing sleep deprivation did not report more negative affect during cyberball [21,22], but had shorter heartbeat intervals [20].

Cyberball is an online ball-tossing game in the field of social pain. In this game, participants play with two or three others, and the other players are virtual and controlled by the programmers (Figure 2(B)). The possibility of receiving the ball is controlled by the experimenter to regulate the extent of social inclusion/exclusion [23]. The first impression paradigm is another method to induce social pain [24]. Participants are told that they will join in a multi-university task and go to make a judgment for others. They are taken photos at first arrival and give and receive judgment during the task (Figure 2(C)).

In summary, the sleep-deprived has impaired negative emotional processing, thus leading to social withdrawal and increased social pain.

2.3. Memorizing phase

When interaction is completed, the sleep-deprived are likely to experience emotional distress. They were supposed to suffer from depressive symptoms [25], reported a higher level of negative affect [21], and showed a reduction in a positive mood [26]. The aversive emotional responses may be the consequence of impaired memory suppression.

Sleep-deprived individuals show deficits in memory control [27]. They cannot successfully suppress unwanted thoughts about unpleasant events and reduce psychological arousal of those events [10]. Moreover, the aversive emotional tone will last as a result of increased rumination. The sleep-deprived are vulnerable to negative emotions, repetitively and uncontrollably thinking about negative events [28]. A longitudinal study of 445 participants found that sleep disturbance at baseline predicted rumination over 6 months [29]. Another study of 73 healthy adults showed increased repetitive negative thinking after one night of sleep restrictions [30].

Uncontrollable and constant thoughts of negative social events will lead to emotional distress after socialization.

2.4. Long-term effect

When social interactions are completed, sleep-deprived individuals are more likely to experience loneliness [14]. Loneliness, which is also known as perceived social isolation, is an unpleasant feeling when there exists a discrepancy between actual and desired interpersonal relationships [31]. Weiss (1973) suggested social isolation and emotional isolation were two forms of loneliness. Social loneliness originated from a lack of social integration, whereas emotional loneliness originated from an absence of an intimate attachment to another person. Loneliness is usually measured by scales like UCLA [32]. What’s more, the one-item survey asking participants whether or how much they feel lonely is also a common method [14,33]. Social and emotional loneliness is measured by de Jong Gierveld Loneliness Scale [34].

The strong relationship between sleep and loneliness exists regardless of the measurements and samples. In a longitudinal study, a higher level of sleep disturbances at baseline predicted a higher level of loneliness [35]. Adolescents with sleep disturbances reported spending enjoyable time with fewer people, even controlling for anxiety, depressive symptoms, and socioeconomic characteristics [7]. Those with sleep disorders experienced emotional, social, and general loneliness after controlling for demographic and socioeconomic factors [36]. Even a day-to-day decrease in sleep efficiency predicted an increase in self-reported loneliness measured by a question [14].

At the beginning of social interaction, sleepiness and negative expectations for interacting consequences will lead to decreased desires about social activities and less involvement in social activities [8,9]. As a result of these impairments, the sleep-deprived will have small social networks and few people to interact with. This is a symptom of social loneliness [33]. During the interacting and memorizing phase, the consequences of sleep loss include a lack of pleasure in communicating with others and feelings of being rejected [16,20]. Those with disrupted sleep were more likely to give attention to social threats, and feel rejected [15,19]. Moreover, they find it difficult to successfully suppress memory for these unpleasant interacting experiences [10]. And constantly go through negative emotions [28]. These dysfunctions contribute to the psychological barrier to connecting with others [37]. They may hinder the building of intimate relationships, thus leading to emotional loneliness [33].

Without interventions, sleep loss will thoroughly cause social and emotional loneliness, as the consequence of dysfunctions in the planning, interacting, and memorizing phases.

3. Changes of activity and functional connectivity in brain networks

It is supposed by a large body of resting-state and task-fMRI studies that the default mode network (DMN), the Negative Affective network (AN), the Inhibitory Control network, and the Near-spatial network are important neural bases for the correlation between sleep loss and social interaction (Figure 3). For one thing, sleep deprivation has a direct functional impairment on the posterior cingulate cortex, prefrontal cortex, anterior cingulate cortex, amygdala, insula, and temporoparietal joint brain areas [5]; for another thing, these brain areas are also core brain areas which are directly involved in social cognitive processing [38,39].

Figure 3. Brian networks involved in the framework. Default mode network (A), affective network (B), inhibitory control network (C), and near-space network (D). mPFC: media prefrontal cortex; Pcu: precuneus; PCC: posterior cingulate cortex; TPJ: temporal–parietal junction; ACC: anterior cingulate cortex; AI: anterior insula; Amg: amygdala; dlPFC: dorsolateral prefrontal cortex; HC: hippocampus; DIPS: dorsal intraparietal sulcus; PMv: ventral premotor cortex.

3.1. Default mode network

There are regions of the brain experiencing negative activation during cognitive tasks of external stimuli and increased activity during resting states and self-relevant tasks. The ventral medial prefrontal cortex (vmPFC), dorsal medial prefrontal cortex (dmPFC), posterior cingulate cortex (PCC), precuneus, and lateral parietal lobe are its core brain regions [40,41]. They constitute the default mode network (DMN), which plays an important role in emotion processing, self-referential processing, and rumination [42].

Acute sleep deprivation will result in decreased activation in the frontal and parietal cortex, which helps combine present information with a prior belief to generate new predictions [14,43,44]. Deficits in predicting the future eliminate social motivations in the planning phase. What’s more, decreases in the activity of the precuneus and temporal–parietal joint junction are likely to cause impairments in speculating on the behavior and intentions of others during the interacting phase [14]. Besides, decreases in the functional connectivity between the anterior and posterior parts of DMN accompanied by 24 h sleep deprivation will lead to emotional distress after social interaction [41,45]. In addition to acute sleep deprivation, daily sleep disturbances can also lead to decreased connectivity within DMN [46]. Apart from decreased resting-state connectivity of the mPFC with the PCC and precuneus, the sleep-deprived have lower whole-brain FC in the precuneus and PCC compared with normal sleepers [47]. These areas of DMN are supposed to be core regions linked with rumination [42,48]. If the functional impairments caused by acute sleep deprivation are left untreated, it may gradually lead to alterations in brain structures including white matter fiber connections and cortical thickness, which eventually shape a lonely person [2,49].

3.2. Negative affective network

The negative emotion network, which consists of brain regions such as the amygdala, insula, dorsal anterior cingulate gyrus, dorsomedial, and ventral medial prefrontal lobes, is sensitive to negative emotion responses [50]. Dorsal regions are responsible for processing emotional stimuli and ventral regions are responsible for the regulation of negative emotions [39,51]. The impairments in NA are mostly related to social dysfunctions in the interacting phase.

Sleep-deprived individuals had abnormal activity within the negative emotion network, as evidenced by exaggerated amygdala responses, abnormally low and high activity in the anterior insula and dorsal anterior cingulate gyrus, showed hypervigilance to emotional stimuli [15,52]. In addition, activation of the right amygdala is enhanced in the sleep-deprived compared to normal sleepers when experiencing social rejection [21]. Discomfort during self-space intrusion is also associated with amygdala activity [53].

Sleep-deprived individuals also have altered functional connectivity within negative emotional networks. Killgore classified subjects into short sleep (≤6.5 h), moderate sleep (6.6–7.9 h), and long sleep groups (≥8 h) based on their self-report of sleep duration the previous night [54]. A lessening of negative coupling between the ventral medial prefrontal cortex and amygdala was found in short sleepers during a 5-min open-eye resting-state MRI scan, which showed weaker up-down regulation of the amygdala. Moreover, subjects with restricted sleep experience enhanced anterior cingulate to amygdala connectivity during social rejection [21].

Not only is there an abnormal connection within the negative emotion network, but weakened connectivity between the amygdala and the dorsolateral prefrontal cortex is also responsible for the impaired emotion process and reduced emotion regulation in the sleep-deprived [52].

3.3. Other networks

The inhibitory control network takes responsibility for the social dysfunction during the planning and memorizing phase. This network consists of the dorsolateral prefrontal cortex (dlPFC), hippocampus, and amygdala [27]. The top-down regulation of dlPFC to retrieval-related activity in the hippocampus and arousal-related activity in the amygdala were disrupted after sleep deprivation [10], showing impairments in controlling unwanted memories.

The intraparietal sulcus (DIPS) and the medial premotor cortex (PMv) in the frontoparietal region together form a near-spatial network as key brain areas sensitive to social stimuli around the body. The stronger the connectivity between the two brain regions, the smaller the individual’s preferred interpersonal distance and the greater the social comfort level [55]. Individuals experiencing all-night sleep deprivation have reduced social comfort and prefer greater interpersonal distance during the interaction. Invasion of personal space is accompanied by abnormal positive activity in the near-space network [14].

4. Discussion

This review highlights the social consequences of sleep loss at different stages of social interaction. The life cycle of social interaction can be divided into planning, interaction, and memorizing phases [6], and sleep loss may ruin our social functions at every stage. Socioemotional dysfunctions in the planning, interacting, and memorizing phases may thoroughly lead to long-term loneliness without interventions.

The emotional and cognitive consequences of sleep loss differ among individuals, and such differences are stable and trait-like [56]. Some individuals are vulnerable to sleep loss while others are not [58]. Individual tolerance to sleep deprivation can be explained by the microstructure of the brain. Higher fractional anisotropy of the superior longitudinal fasciculus, which connected frontal and parietal regions, predicted less vulnerability to sleep deprivation [59]. Other environmental factors may also help relieve from negative state caused by sleep loss. For example, perceived social support significantly moderated anxious and depressed feelings caused by uncertainty [60].

Another interesting question is which phase of the whole cycle of social interaction is most important. The contribution of a specific phase to long-term loneliness may differ. Tracking studies based on the life cycle of interaction may be helpful for our understanding of this question. During the longitudinal study, ecological sampling may be more suitable than experimental studies. Participants are required to record their daily social events and sleep status for a long period [9]. Besides, we can focus on changes in social functions at a particular stage and emotional state follow-up after experimental sleep deprivation.

In addition to that, we suggest that sleep loss will finally lead to loneliness. First, sleep and loneliness are closely related. Even a day-to-day decrease in sleep efficiency induces an increase in loneliness [14]. Loneliness will increase with more baseline sleep disturbances [35]. Then, we proposed the idea that this aversive health problem may not only be the consequence of repetitive sleep disturbances but also social dysfunctions accompanied by acute sleep deprivation. For example, short sleepers are supposed to have more repetitive negative thoughts after social interaction, which is the reason for emotional loneliness, as well as the cause of shorter sleep duration and longer sleep latency [61].

Several intervention techniques can be taken to alleviate sleep disturbances and the aversive consequence of sleep loss. Transcranial direct current stimulation (tDCS), as well as transcranial magnetic stimulation (TMS), is a non-invasive stimulation technique used to treat several symptoms. Depending on specific methodologies, they can be used to increase or decrease neuronal activities in order to alleviate sleep and emotional disturbances [62–64]. Using intensities ranging between 1.5 and 2 mA, anodal tDCS one DLPFC would produce a significant increase of sleep quality [63]. Active stimulation on the lateral PFC resulted in reductions in negative emotional response, and this effect lasted at least one hour [48]. In addition to brain stimulations, neurofeedback (NFB) is considered an efficient tool to improve emotional regulation abilities [57]. Four-week training resulted in decreased reactivation in the amygdala as well as increased coupling with the prefrontal area [65].

We come to a broad conclusion that sleep loss ruins social relationships through the life cycle of social interaction. Future studies are needed to investigate the contributions of social functions at different stages to loneliness. The combination of experimental and ecological studies is critical. For interventions, we should focus on interindividual variability. Brain stimulation and neurofeedback for emotional regulation training may be an important way to reduce the aversive consequences of sleep loss.

5. Conclusion

In all, the current review provided a dynamic framework for understanding the relationship between sleep and social interaction. This framework suggests that sleep loss impairs social relationships at different stages of social interaction. And we try to explain the behavioral and neural mechanisms through several experimental researches. At the beginning of social interaction, individuals who have less sleep are more likely to be involved in fewer social activities as a consequence of high sleepiness and low social appeal, such social dysfunctions are accompanied by low reactivations within DMN. During social interaction, the vulnerability to social threat and feelings of being rejected or excluded exaggerated due to alterations in emotional perception, and impaired emotional processing with AN and near-space networks. After social interaction, social loneliness occurred and is maintained with the help of rumination. Without interventions, sleep loss will shape a lonely person mentally and physically. Future interventions can be taken at different stages of social interaction to alleviate the social burden of sleep loss.

Author contributions

Yiqi Mi: Conceptualization, Writing – Original Draft.

Xu Lei: Writing – Conceptualization, Review & Editing, Funding acquisition

Disclosure statement

No potential conflict of interest was reported by the author(s).

Additional information

Funding

This research is supported by National Key Research and Development Program of China [2021YFC2501500] and National Natural Science Foundation of China [31971028].