A neural pathway for social modulation of spontaneous locomotor activity (SoMo-SLA) in Drosophila.

Social enrichment or social isolation affects a range of innate behaviors, such as sex, aggression, and sleep, but whether there is a shared mechanism is not clear. Here, we report a neural mechanism underlying social modulation of spontaneous locomotor activity (SoMo-SLA), an internal-driven behavior indicative of internal states. We find that social enrichment specifically reduces spontaneous locomotor activity in male flies. We identify neuropeptides Diuretic hormone 44 (DH44) and Tachykinin (TK) to be up- and down-regulated by social enrichment and necessary for SoMo-SLA. We further demonstrate a sexually dimorphic neural circuit, in which the male-specific P1 neurons encoding internal states form positive feedback with interneurons coexpressing doublesex (dsx) and Tk to promote locomotion, while P1 neurons also form negative feedback with interneurons coexpressing dsx and DH44 to inhibit locomotion. These two opposing neuromodulatory recurrent circuits represent a potentially common mechanism that underlies the social regulation of multiple innate behaviors.

The social context of burning mouth syndrome: an exploratory pilot study of stigma, discrimination, and pain.

BACKGROUND: The social context of burning mouth syndrome (BMS) has received little attention in the scientific literature. However, social psychological theory and insights from those with lived experiences suggest that people living with BMS experience compounding effects of stigma related to their pain, diagnosis (or lack thereof), and intersectional identities. OBJECTIVE: Our aim is to provide initial evidence and to motivate new directions for research on BMS. Here, we present the results of an exploratory pilot study (n = 16) of women living with BMS in the United States. METHODS: Participants completed self-report measures of stigma, discrimination, and pain, as well as laboratory assessments of pain through quantitative sensory testing. RESULTS: Results indicate a high prevalence of internalized BMS stigma, experience of BMS-related discrimination from clinicians, and gender stigma consciousness in this population. Moreover, results provide initial evidence that these experiences are related to pain outcomes. The most robust pattern of findings is that internalized BMS stigma was related to greater clinical pain severity, interference, intensity, and unpleasantness. CONCLUSION: Given the prevalence and pain-relevance of intersectional stigma and discrimination identified in this pilot study, lived experience and social context should be incorporated into future research on BMS.

The mere physical presence of another person reduces human autonomic responses to aversive sounds.

Social animals show reduced physiological responses to aversive events if a conspecific is physically present. Although humans are innately social, it is unclear whether the mere physical presence of another person is sufficient to reduce human autonomic responses to aversive events. In our study, participants experienced aversive and neutral sounds alone (alone treatment) or with an unknown person that was physically present without providing active support. The present person was a member of the participants' ethnical group (ingroup treatment) or a different ethnical group (outgroup treatment), inspired by studies that have found an impact of similarity on social modulation effects. We measured skin conductance responses (SCRs) and collected subjective similarity and affect ratings. The mere presence of an ingroup or outgroup person significantly reduced SCRs to the aversive sounds compared with the alone condition, in particular in participants with high situational anxiety. Moreover, the effect was stronger if participants perceived the ingroup or outgroup person as dissimilar to themselves. Our results indicate that the mere presence of another person was sufficient to diminish autonomic responses to aversive events in humans, and thus verify the translational validity of basic social modulation effects across different species.

Collective action reduces androgen responsiveness with implications for shoaling dynamics in stickleback fish.

Androgens, traditionally viewed as hormones that regulate secondary sexual characteristics and reproduction in male vertebrates, are often modulated by social stimuli. High levels of the 'social hormone' testosterone (T) are linked to aggression, dominance, and competition. Low T levels, in contrast, promote sociopositive behaviours such as affiliation, social tolerance, and cooperation, which can be crucial for group-level, collective behaviours. Here, we test the hypothesis that - in a collective context - low T levels should be favourable, using non-reproductive male and female stickleback fish (Gasterosteus aculeatus) and non-invasive waterborne hormone analysis. In line with our predictions, we show that the fishes' T levels were significantly lower during shoaling compared to when alone, with high-T individuals showing the largest decrease. Ruling out stress-induced T suppression and increased T conversion into oestradiol, we find evidence that shoaling directly affects androgen responsiveness. We also show that groups characterized by lower mean T exhibit less hierarchical leader-follower dynamics, suggesting that low T promotes egalitarianism. Overall, we show that collective action results in lower T levels, which may serve to promote coordination and group performance. Our study, together with recent complementary findings in humans, emphasizes the importance of low T for the expression of sociopositive behaviour across vertebrates, suggesting similarities in endocrine mechanisms.

Global and Situational Relationship Satisfaction Moderate the Effect of Threat on Pain in Couples.

OBJECTIVE: The aim of this study was to test the hypothesis that greater global and situational relationship satisfaction would reduce the negative impact of threatening information on acute pain. DESIGN: An experimental design was used to manipulate threat and elicit acute pain via a cold pressor task. SETTING: The study was completed in a research laboratory at a large urban university in the Midwestern USA. SUBJECTS: Participants were 134 couples, in which at least one individual was an undergraduate student. METHODS: After administration of a global relationship satisfaction measure, couples were randomly assigned to either receive high or low threatening information about the painful task. Following the threat manipulation, couples discussed the upcoming task and rated their satisfaction with the interaction (i.e., situational relationship satisfaction). The designated pain participant then completed the painful task alone. RESULTS: The threat manipulation altered couples' perceived threat of pain. Situational relationship satisfaction moderated the effect of threat on pain trajectories such that situational relationship satisfaction predicted less pain intensity at an earlier point in the task for the low threat condition than the high threat condition. Greater global relationship satisfaction predicted greater likelihood of task completion among those in the low threat condition, whereas it was unrelated to task completion in the high threat condition. Greater global relationship satisfaction also predicted lower pain intensity throughout the task. CONCLUSIONS: These findings demonstrate that the interpersonal context is independently related to acute pain and may also alter the effect of threatening information on acute pain.

When is it socially acceptable to feel sick?

Disease is a ubiquitous and powerful evolutionary force. Hosts have evolved behavioural and physiological responses to disease that are associated with increased survival. Behavioural modifications, known as 'sickness behaviours', frequently involve symptoms such as lethargy, somnolence and anorexia. Current research has demonstrated that the social environment is a potent modulator of these behaviours: when conflicting social opportunities arise, animals can decrease or entirely forgo experiencing sickness symptoms. Here, I review how different social contexts, such as the presence of mates, caring for offspring, competing for territories or maintaining social status, affect the expression of sickness behaviours. Exploiting the circumstances that promote this behavioural plasticity will provide new insights into the evolutionary ecology of social behaviours. A deeper understanding of when and how this modulation takes place may lead to better tools to treat symptoms of infection and be relevant for the development of more efficient disease control programmes.

The number of life-history stages does not influence the androgen responsiveness to male-male interactions: sedentary and migratory black redstarts (Phoenicurus ochruros) do not elevate testosterone in response to simulated territorial intrusions.

High plasma levels of testosterone at the beginning of the breeding season adjust male physiology for mating and promote territorial behavior in birds. Conversely intra-sexual competition may elicit a temporary increase in circulating testosterone. Male black redstarts (Phoenicurus ochruros) from migratory populations show the expected increase in baseline testosterone during early breeding, but circulating testosterone levels do not change in response to male-male interactions. Because sedentary populations express fewer life-history stages they may be more flexible in timing of life-history stages and more responsive to environmental modulation of hormone concentrations. Therefore, we tested whether the androgen responsiveness to male-male interactions differs between migratory (6 life-history stages) and sedentary black redstarts (3 life-history stages) during early breeding, predicting that in contrast to migratory birds, sedentary birds would modulate testosterone in response to simulated territorial intrusions (STI). In contrast to our prediction, sedentary males did not modulate post-capture testosterone levels in response to simulated territorial intrusions. Males of both populations increased testosterone after an injection of gonadotropin releasing hormone (GnRH), demonstrating that they were capable of increasing testosterone. Interestingly, in sedentary males the GnRH injection elicited a higher testosterone response in STI males than in control males. The two populations did not differ in their behavioral response to the STIs, except that sedentary males spent less time close to the decoy. In combination with previous data from black redstarts and other socially monogamous and biparental birds our current study adds to the growing evidence that current theory regarding hormone-behavior relationship needs to be refined.

Tuning social modulations of gaze cueing via contextual factors.

Gaze cueing reflects the tendency to shift attention toward a location cued by the averted gaze of others. This effect does not fulfill criteria for strong automaticity because its magnitude is sensitive to the manipulation of different social features. Recent theoretical perspectives suggest that social modulations of gaze cueing could further critically depend on contextual factors. In this study, we tested this idea, relying on previous evidence showing that Chinese participants are more sensitive to gazes on White than on Asian faces, likely as a consequence of differences in perceived social status. We replicated this effect when we made group membership salient by presenting faces belonging to the different ethnicities in the same block. In contrast, when faces belonging to different ethnicities were presented in separate blocks, a similar gaze-cueing effect was noted, likely because no social comparison processes were activated. These findings are consistent with the idea that social modulations are not rigid but are tuned by contextual factors.

Acute Ostracism-Related Pain Sensitization in the Context of Accumulated Lifetime Experiences of Ostracism.

Ostracism (ie, being ignored/excluded) is a form of social adversity that powerfully impacts health and well-being. While laboratory research indicates that experimentally manipulated experiences of ostracism impact pain, findings have been mixed. Prior investigations have not considered moderating or main effects of individual histories of ostracism, and have been limited in the scope of their pain testing. In this study, participants without current pain reported lifetime experiences of ostracism prior to a laboratory visit where they were randomized to experience either a single episode of ostracism (ie, acute ostracism) or control condition that was immediately followed by quantitative sensory testing. Results indicate that the experimental effect of a single episode of ostracism on pain ratings, after-sensations, and temporal summation of pain is moderated by lifetime ostracism; no main effects were found. For individuals with histories of more lifetime ostracism, encountering a single episode of ostracism led to greater pain sensitization relative to the control condition, whereas no experimental effect was observed for individuals with little lifetime exposure to ostracism. These findings indicate that acute experiences of ostracism may be accompanied by periods of hyperalgesia for people who are chronically ostracized, implicating ostracism as a potential social moderator of pain sensitization. People who are stigmatized may therefore experience enhanced pain burden with repeated and accumulating experiences of ostracism. PERSPECTIVE: Results suggest that in the context of accumulated lifetime experiences of ostracism, single experiences of ostracism evoke central sensitization. In this way, ostracism may function to trigger central sensitization and shape socially- and societally-determined patterns of pain burden and disparity.

The skin conductance response indicating pain relief is independent of self or social influence on pain.

Pain relief is defined as the ease of pain and is thus highly relevant for clinical applications and everyday life. Given that pain relief is based on the cessation of an aversive pain experience, it is reasonable to assume that pain relief learning would also be shaped by factors that alter subjective and physiological pain responses, such as social presence or a feeling of control. To date, it remains unclear whether and how factors that shape autonomic pain responses might affect pain relief learning. Here, we investigated how pain relief learning is shaped by two important factors known to modulate pain responses, i.e. social influence and controllability of pain. Skin conductance responses (SCRs) were recorded while participants learned to associate a formerly neutral stimulus with pain relief under three different pain conditions. In the social-influence condition (N = 34), the pain stimulation could be influenced by another person's decisions. In the self-influence condition (N = 31), the participants themselves could influence the pain stimulation. Finally, in the no-influence condition (N = 32), pain stimulation was simply delivered without any influence. According to our results, the SCRs elicited by the stimulus that was associated with pain relief were significantly smaller compared to the SCRs elicited by a neutral control stimulus, indicating pain relief learning. However, there was no significant difference in the pain relief learning effect across the groups. These results suggest that physiological pain relief learning in humans is not significantly influenced by social influence and pain controllability.

"Big girls don't cry": the effect of the experimenter's sex and pain catastrophising on pain.

OBJECTIVES: The expression of pain in males and females involves complex socio-psychological mechanisms. Males may report lower pain to a female experimenter to appear strong, whereas females may report higher pain to a male experimenter to appear weak and to seek protection. However, evidence to support these stereotypes is inconclusive. Individuals who catastrophise about pain rate higher pain than those who do not. How pain catastrophising interacts with the effect of the experimenter's sex on pain reports is yet to be explored. Thus, the aim of this study was to determine whether pain catastrophising moderated the effect of the experimenter's sex on pain reports in healthy males and females. METHODS: Participants (n=60, 30 males) were assigned to one of four experimental conditions: males tested by male experimenters, males tested by female experimenters, females tested by male experimenters, and females tested by female experimenters. Participants completed the Pain Catastrophising Scale, and then sensitivity to heat and to blunt (pressure-pain threshold) and sharp stimuli was assessed on both forearms, and to high frequency electrical stimulation (HFS) administered to one forearm. RESULTS: Females reported lower pressure-pain thresholds than males irrespective of the experimenters' sex. Females reported lower sharpness ratings to male than female experimenters only when the test stimuli were moderately or intensely sharp. Higher pain catastrophising scores were associated with higher sharpness ratings in females but not males. Additionally, higher pain catastrophising scores were associated with greater temporal summation of pain to HFS, and with lower pressure-pain thresholds in females who were tested by male experimenters. CONCLUSIONS: These findings indicate that the experimenters' sex and the participant's pain catastrophising score influence pain reports, particularly in females. Awareness of these psychosocial factors is important in order to interpret pain responses in a meaningful way, especially when females are tested by male experimenters. A greater awareness of sex/gender role biases and their potential interaction with pain catastrophising may help researchers and clinicians to interpret pain reports in meaningful ways. In turn, this may help to improve delivery of treatments for patients with chronic pain.

The Influence of Reward on Facial Mimicry: No Evidence for a Significant Effect of Oxytocin.

Recent findings suggest a role of oxytocin on the tendency to spontaneously mimic the emotional facial expressions of others. Oxytocin-related increases of facial mimicry, however, seem to be dependent on contextual factors. Given previous literature showing that people preferentially mimic emotional expressions of individuals associated with high (vs. low) rewards, we examined whether the reward value of the mimicked agent is one factor influencing the oxytocin effects on facial mimicry. To test this hypothesis, 60 male adults received 24 IU of either intranasal oxytocin or placebo in a double-blind, between-subject experiment. Next, the value of male neutral faces was manipulated using an associative learning task with monetary rewards. After the reward associations were learned, participants watched videos of the same faces displaying happy and angry expressions. Facial reactions to the emotional expressions were measured with electromyography. We found that participants judged as more pleasant the face identities associated with high reward values than with low reward values. However, happy expressions by low rewarding faces were more spontaneously mimicked than high rewarding faces. Contrary to our expectations, we did not find a significant direct effect of intranasal oxytocin on facial mimicry, nor on the reward-driven modulation of mimicry. Our results support the notion that mimicry is a complex process that depends on contextual factors, but failed to provide conclusive evidence of a role of oxytocin on the modulation of facial mimicry.

Evolution of mechanisms and behaviour important for pain.

Our understanding of the biology of pain is limited by our ignorance about its evolution. We know little about how states in other species showing various degrees of apparent similarity to human pain states are related to human pain, or how the mechanisms essential for pain-related states evolved. Nevertheless, insights into the evolution of mechanisms and behaviour important for pain are beginning to emerge from wide-ranging investigations of cellular mechanisms and behavioural responses linked to nociceptor activation, tissue injury, inflammation and the environmental context of these responses in diverse species. In February 2019, an unprecedented meeting on the evolution of pain hosted by the Royal Society brought together scientists from disparate fields who investigate nociception and pain-related behaviour in crustaceans, insects, leeches, gastropod and cephalopod molluscs, fish and mammals (primarily rodents and humans). Here, we identify evolutionary themes that connect these research efforts, including adaptive and maladaptive features of pain-related behavioural and neuronal alterations-some of which are quite general, and some that may apply primarily to humans. We also highlight major questions, including how pain should be defined, that need to be answered as we seek to understand the evolution of pain. This article is part of the Theo Murphy meeting issue 'Evolution of mechanisms and behaviour important for pain'.

Empathy for Pain: Insula Inactivation and Systemic Treatment With Midazolam Reverses the Hyperalgesia Induced by Cohabitation With a Pair in Chronic Pain Condition.

Empathy for pain is the ability to perceive and understand the pain in the other individual. Recent studies suggested that rodents have this social ability. GABAergic system has receptors in the brain structures involved in emotional processes as well as in the insular cortex. This area has been described as an important key in modulation of pain and empathy. The present study has investigated the role of insula and its Benzodiazepine-GABAA system on social modulation of pain induced by cohabiting with a mouse submitted to sciatic nerve constriction, a neuropathic pain model. The insular cortex function was assessed by the structure inactivation (Experiments 1 and 2); the role of GABA system was evaluated by systemic treatment of midazolam (MDZ 0.5, 1, and 2 mg/kg) (Experiment 3); and the role of GABAA receptors of insula were studied by bilateral MDZ (3 and 30 nmol/0.1 µl) microinjections in the structure (Experiment 4). Male Swiss mice were housed in groups or dyads. On dyads, after 14 days of cohabitation they were divided into two groups: cagemate nerve constriction and cagemate sham (CS). After 14 days of familiarity, cagemates were evaluated on the writhing test. For group-housed, insula inactivation did not change nociception. For dyad-housed, cohabiting with a mouse in chronic pain increased the nociceptive response and the insula inactivation has reverted this response. Systemic MDZ attenuated nociception and intra-insula MDZ did not alter it. Our results suggest that cohabitation with a pair in chronic pain induces hypernociception, insula possibly modulates this response and the GABA system is also possibly involved, but not its insular mechanisms.

Impression or expression? The influence of self-monitoring on the social modulation of motor contagion.

Social primes (pro-social, anti-social) can modulate mimicry behaviour. To date, these social modulation effects have been explained by the primed incentive to affiliate with another (Social Top-Down Response Modulation; STORM) and the primed active-self-concept leading to behaviour that is either consistent or inconsistent with the primed-construct (Active-Self account). This study was designed to explore the explanatory power of each of these accounts and thereby gain a greater understanding of how social modulation unfolds. To do this, we assessed social modulation of motor contagion in individuals high or low in self-monitoring. It was reasoned that high self-monitors would modulate mimicry according to the primed social incentive, whereas low self-monitors would modulate according to the primed active-self-concept. Participants were primed with a pro-social and anti-social cue in the first-person and third-person perspective. Next, they completed an interpersonal observation-execution task featuring the simultaneous observation and execution of arm movements that were either congruent or incongruent to each other. Results showed increased incongruent movement deviation (motor contagion) for the anti-social compared to the pro-social prime in the high self-monitors only. Findings support the STORM account of mimicry by showing observers modulate behaviour based on the social incentive underpinning an interpersonal exchange.

The perception of affective touch in anorexia nervosa.

Anorexia nervosa (AN) is a disorder characterized by restricted eating, fears of gaining weight, and body image distortions. The etiology remains unknown; however impairments in social cognition and reward circuits contribute to the onset and maintenance of the disorder. One possibility is that AN is associated with reduced perceived pleasantness during social interactions. We therefore examined the perception of interpersonal, 'affective touch' and its social modulation in AN. We measured the perceived pleasantness of light, dynamic stroking touches applied to the forearm of 25 AN patients and 30 healthy controls using C Tactile (CT) afferents-optimal (3cm/s) and non-optimal (18cm/s) velocities, while simultaneously displaying images of faces showing rejecting, neutral and accepting expressions. CT-optimal touch, but not CT non-optimal touch, elicited significantly lower pleasantness ratings in AN patients compared with healthy controls. Pleasantness ratings were modulated by facial expressions in both groups in a similar fashion; namely, presenting socially accepting faces increased the perception of touch pleasantness more than neutral and rejecting faces. Our findings suggest that individuals with AN have a disordered, CT-based affective touch system. This impairment may be linked to their weakened interoceptive perception and distorted body representation.

The social modulation of pain: others as predictive signals of salience - a systematic review.

Several studies in cognitive neuroscience have investigated the cognitive and affective modulation of pain. By contrast, fewer studies have focused on the social modulation of pain, despite a plethora of relevant clinical findings. Here we present the first review of experimental studies addressing how interpersonal factors, such as the presence, behavior, and spatial proximity of an observer, modulate pain. Based on a systematic literature search, we identified 26 studies on experimentally induced pain that manipulated different interpersonal variables and measured behavioral, physiological, and neural pain-related responses. We observed that the modulation of pain by interpersonal factors depended on (1) the degree to which the social partners were active or were perceived by the participants to possess possibility for action; (2) the degree to which participants could perceive the specific intentions of the social partners; (3) the type of pre-existing relationship between the social partner and the person in pain, and lastly, (4) individual differences in relating to others and coping styles. Based on these findings, we propose that the modulation of pain by social factors can be fruitfully understood in relation to a recent predictive coding model, the free energy framework, particularly as applied to interoception and social cognition. Specifically, we argue that interpersonal interactions during pain may function as social, predictive signals of contextual threat or safety and as such influence the salience of noxious stimuli. The perception of such interpersonal interactions may in turn depend on (a) prior beliefs about interpersonal relating and (b) the certainty or precision by which an interpersonal interaction may predict environmental threat or safety.