Socio-affective Behavior Research Articles

Impact of the gut microbiome composition on social decision-making.

There is increasing evidence for the role of the gut microbiome in the regulation of socio-affective behavior in animals and clinical conditions. However, whether and how the composition of the gut microbiome may influence social decision-making in health remains unknown. Here, we tested the causal effects of a 7-week synbiotic (vs. placebo) dietary intervention on altruistic social punishment behavior in an ultimatum game. Results showed that the intervention increased participants' willingness to forgo a monetary payoff when treated unfairly. This change in social decision-making was related to changes in fasting-state serum levels of the dopamine-precursor tyrosine proposing a potential mechanistic link along the gut-microbiota-brain-behavior axis. These results improve our understanding of the bidirectional role body-brain interactions play in social decision-making and why humans at times act "irrationally" according to standard economic theory.

Lower affective empathy in oral contraceptive users: a cross-sectional fMRI study.

Evidence accumulates that oral contraceptive (OC) use modulates various socio-affective behaviors, including empathic abilities. Endogenous and synthetic sex hormones, such as estrogens and progestogens, bind to receptor sites in brain regions (i.e. frontal, limbic, and cerebellar) involved in socio-affective processing. Therefore, the aim of this study was to investigate the role of OC use in empathy. In a cross-sectional functional magnetic resonance imaging study, women in different hormonal states, including OC use (n = 46) or being naturally cycling in the early follicular (fNC: n = 37) or peri-ovulatory phase (oNC: n = 28), performed a visual, sentence-based empathy task. Behaviorally, OC users had lower empathy ratings than oNC women. Congruently, whole-brain analysis revealed significantly larger task-related activation of several brain regions, including the left dorsomedial prefrontal gyrus (dmPFG), left precentral gyrus, and left temporoparietal junction in oNC compared to OC women. In OC users, the activity of the left dmPFG and precentral gyrus was negatively associated with behavioral and self-reported affective empathy. Furthermore, empathy-related region-of-interest analysis indicated negative associations of brain activation with synthetic hormone levels in OC women. Overall, this multimodal, cross-sectional investigation of empathy suggests a role of OC intake in especially affective empathy and highlights the importance of including synthetic hormone levels in OC-related analyses.

Capturing Between- and Within-Person Variability of Borderline Traits in Youth from a Developmentally Sensitive Situational Judgment Perspective

The significance of early maladaptive traits for understanding the roots of borderline personality disorder (BPD) is increasingly endorsed. Given the interpersonal nature of BPD and fluctuations in phenotypic symptomatology, this study aims to test the assumption that a situation-contingent contextualized assessment of borderline traits is a viable avenue to more fully capture the way underlying traits are reflected in socioaffective behavior that occurs in age-relevant situations. We aimed to explore the extent to which the variability on these responses represents a meaningful construct for understanding the clinical richness of BPD. Toward this end, a contextualized measure of DSM–5 BPD traits was developed along a situational judgment test (SJT) format, allowing us to explore both between-person and within-person variability in a more economic format than repeated measurement does. Examination of the psychometric properties of the SJT revealed distinctive correlational patterns of the situation-based traits with symptom scales of a youth BPD measure, but also indicated that for certain traits consistency in trait level across different situations is more maladaptive, whereas for other traits a greater degree of variability in trait expression is more maladaptive. Overall, this work could set the stage for further research on the potential of SJTs for understanding personality vulnerabilities both at the dispositional and the dynamic level.

The Impact of Virtual Nature Therapy on Stress Responses: A Systematic Qualitative Review

This study aims to review the key findings of past studies that assessed the impact of virtual environments, such as nature and forests for stress therapy. Previous research has found that virtual reality (VR) experiences affect socio-affective behavior, indicating the potential of using VR for cognitive and psychological stress therapy. However, evidence for the impacts of virtual forest therapy as a stress-reduction technique is lacking, and the usefulness of these techniques has yet to be determined. This review was carried out following the preferred reporting items for meta-analyses and systematic reviews. It summarized the literature and provided evidence on virtual forest therapy (VFT) effectiveness in stress relief. We conducted a literature search considering VR-related studies published from 2013 until June 2021 for different databases, including Embase, Medline/PubMed, Hindawi, ScienceDirect, Scopus, Web of Science, Taylor & Francis, and the Cochrane Library, to see how effective VFT reduces stress levels and improves mental well-being. According to the set inclusion criteria, eighteen relevant papers detailing original research were eligible for inclusion. This overview suggests that VR provides benefits for assessing and reducing stress levels. While real natural environments effectively promote recovery from stress, virtual exposure to nature also positively affects stress. Thus, VR could be an effective technique for promoting relaxation, particularly during the COVID-19 pandemic, where stress levels rise globally. However, more in-depth studies are required to substantiate this potential field of VR relaxation.

Neonatal anesthesia and dysregulation of the epigenome†.

Each year, millions of infants and children are anesthetized for medical and surgical procedures. Yet, a substantial body of preclinical evidence suggests that anesthetics are neurotoxins that cause rapid and widespread apoptotic cell death in the brains of infant rodents and nonhuman primates. These animals have persistent impairments in cognition and behavior many weeks or months after anesthesia exposure, leading us to hypothesize that anesthetics do more than simply kill brain cells. Indeed, anesthetics cause chronic neuropathology in neurons that survive the insult, which then interferes with major aspects of brain development, synaptic plasticity, and neuronal function. Understanding the phenomenon of anesthesia-induced developmental neurotoxicity is of critical public health importance because clinical studies now report that anesthesia in human infancy is associated with cognitive and behavioral deficits. In our search for mechanistic explanations for why a young and pliable brain cannot fully recover from a relatively brief period of anesthesia, we have accumulated evidence that neonatal anesthesia can dysregulate epigenetic tags that influence gene transcription such as histone acetylation and DNA methylation. In this review, we briefly summarize the phenomenon of anesthesia-induced developmental neurotoxicity. We then discuss chronic neuropathology caused by neonatal anesthesia, including disturbances in cognition, socio-affective behavior, neuronal morphology, and synaptic plasticity. Finally, we present evidence of anesthesia-induced genetic and epigenetic dysregulation within the developing brain that may be transmitted intergenerationally to anesthesia-naïve offspring.

Atrophy in Distinct Corticolimbic Networks Subserving Socioaffective Behavior in Semantic Variant Primary Progressive Aphasia

Background: Although traditionally conceptualized as a language disorder, semantic variant primary progressive aphasia (svPPA) is often accompanied by significant behavioral and affective symptoms which considerably increase disease morbidity. Specifically, these neuropsychiatric symptoms are characterized by breaches in normative socioaffective function, for example, an inability to read social cues, excessive trusting of others, and decreased empathy. Our prior neuroimaging work identified 3 corticolimbic networks anchored in the amygdala, temporal pole, and frontoinsular cortex: an affiliation network, theorized to mediate social approach behavior; an aversion network, theorized to subserve the appraisal of social threat; and a perception network, theorized to mediate the detection of social cues. We hy­pothesized that degeneration of these networks could provide neuroanatomical substrates for socioaffective deficits in svPPA. Methods: We examined hypothesized relationships between subscores on the Social Impairment Rating Scale (SIRS) and atrophy in each of these 3 networks in a group of 16 svPPA patients (using matched cognitively normal controls as a reference). Results: Consistent with our predictions, the magnitude of atrophy in the affiliation network in svPPA patients correlated with the SIRS subscore of socioemotional detachment, while the magnitude of atrophy in the aversion network in svPPA patients correlated with the SIRS subscore of inappropriate trusting. We did not find the predicted association between perception network atrophy and the SIRS subscore of lack of attention to social cues. Conclusion: These findings highlight specific socioaffective deficits in svPPA and provide a neuroanatomical basis for these impairments by linking them to networks commonly targeted in this disorder.

In Touch with the Heartbeat: Newborns' Cardiac Sensitivity to Affective and Non-Affective Touch.

The sense of touch is the first manner of contact with the external world, providing a foundation for the development of sensorimotor skills and socio-affective behaviors. In particular, affective touch is at the core of early interpersonal interactions and the developing bodily self, promoting the balance between internal physiological state and responsiveness to external environment. The aim of the present study is to investigate whether newborns are able to discriminate between affective touch and non-affective somatosensory stimulations and whether affective touch promotes a positive physiological state. We recorded full-term newborns’ (N = 30) heart rate variability (HRV)—which reflects oscillations of heart rate associated with autonomic cardio-respiratory regulation—while newborns were presented with two minutes of affective (stroking) and non-affective (tapping) touch alternated with two minutes of resting in a within-subject design. The results revealed that non-affective touch elicits a decrease in HRV, whereas affective touch does not result in a change of HRV possibly indicating maintenance of calm physiological state. Thus, newborns showed cardiac sensitivity to different types of touch, suggesting that early somatosensory stimulation represents scaffolding for development of autonomic self-regulation with important implications on infant’s ability to adaptively respond to the surrounding social and physical environment.

Neonatal male circumcision is associated with altered adult socio-affective processing

BackgroundNeonatal male circumcision is a painful skin-breaking procedure that may affect infant physiological and behavioral stress responses as well as mother-infant interaction. Due to the plasticity of the developing nociceptive system, neonatal pain might carry long-term consequences on adult behavior. In this study, we examined whether infant male circumcision is associated with long-term psychological effects on adult socio-affective processing. MethodsWe recruited 408 men circumcised within the first month of life and 211 non-circumcised men and measured socio-affective behaviors and stress via a battery of validated psychometric scales. ResultsEarly-circumcised men reported lower attachment security and lower emotional stability while no differences in empathy or trust were found. Early circumcision was also associated with stronger sexual drive and less restricted socio-sexuality along with higher perceived stress and sensation seeking. LimitationsThis is a cross-sectional study relying on self-reported measures from a US population. ConclusionsOur findings resonate with the existing literature suggesting links between altered emotional processing in circumcised men and neonatal stress. Consistent with longitudinal studies on infant attachment, early circumcision might have an impact on adult socio-affective traits or behavior.

The Impact of Traumatic Injury to the Immature Human Brain: A Scoping Review with Insights from Advanced Structural Neuroimaging

Traumatic brain injury (TBI) during critical periods of early-life brain development can affect the normal formation of brain networks responsible for a range of complex social behaviors. Because of the protracted nature of brain and behavioral development, deficits in cognitive and socioaffective behaviors may not become evident until late adolescence and early adulthood, when such skills are expected to reach maturity. In addition, multiple pre- and post-injury factors can interact with the effects of early brain insult to influence long-term outcomes. In recent years, with advancements in magnetic-resonance-based neuroimaging techniques and analysis, studies of the pediatric population have revealed a link between neurobehavioral deficits, such as social dysfunction, with white matter damage. In this review, in which we focus on contributions from Australian researchers to the field, we have highlighted pioneering longitudinal studies in pediatric TBI, in relation to social deficits specifically. We also discuss the use of advanced neuroimaging and novel behavioral assays in animal models of TBI in the immature brain. Together, this research aims to understand the relationship between injury consequences and ongoing brain development after pediatric TBI, which promises to improve prediction of the behavioral deficits that emerge in the years subsequent to early-life injury.

Acute and Repeated Intranasal Oxytocin Differentially Modulate Brain-wide Functional Connectivity

Central release of the neuropeptide oxytocin (OXT) modulates neural substrates involved in socio-affective behavior. This property has prompted research into the use of intranasal OXT administration as an adjunctive therapy for brain conditions characterized by social impairment, such as autism spectrum disorders (ASD). However, the neural circuitry and brain-wide functional networks recruited by intranasal OXT administration remain elusive. Moreover, little is known of the neuroadaptive cascade triggered by long-term administration of this peptide at the network level. To address these questions, we applied fMRI-based circuit mapping in adult mice upon acute and repeated (seven-day) intranasal dosing of OXT. We report that acute and chronic OXT administration elicit comparable fMRI activity as assessed with cerebral blood volume mapping, but entail largely different patterns of brain-wide functional connectivity. Specifically, acute OXT administration focally boosted connectivity within key limbic components of the rodent social brain, whereas repeated dosing led to a prominent and widespread increase in functional connectivity, involving a strong coupling between the amygdala and extended cortical territories. Importantly, this connectional reconfiguration was accompanied by a paradoxical reduction in social interaction and communication in wild-type mice. Our results identify the network substrates engaged by exogenous OXT administration, and show that repeated OXT dosing leads to a substantial reconfiguration of brain-wide connectivity, entailing an aberrant functional coupling between cortico-limbic structures involved in socio-communicative and affective functions. Such divergent patterns of network connectivity might contribute to discrepant clinical findings involving acute or long-term OXT dosing in clinical populations.

The Relationship Between the Left-Cradling Bias and Attachment to Parents and Partner.

Mothers usually cradle their infants to the left of their body midline, an asymmetry that seems to be a typically female lateral preference. This bias is deemed to be an evolutionary facilitator of communication between cradling and cradled individuals and is believed to be strongly related to hemispheric specialization for complex socio-affective behaviors. Thus, left cradling might facilitate affective interactions in females with typical brain organization, probably due to a right-hemisphere dominance for social attachment. In this study, we investigated cradling-side preferences in 288 young females as a function of their attachment styles to parents and partners. A left-cradling bias was more frequent in participants experiencing positive relationships with their mother and romantic partners. These findings indicate that the left-cradling bias may be associated with high-quality social attachment behaviors in females and, therefore, can be considered as a natural index of socio-emotional attunement between the cradling and cradled individuals.

Music Preferences and Personality in Brazilians.

This article analyzes the relationship between musical preference and type of personality in a large group of Brazilian young and adult participants (N = 1050). The study included 25 of 27 states of Brazil and individuals aged between 16 and 71 years (M = 30.87; SD = 10.50). Of these, 500 were male (47.6%) and 550 were female (52.4%). A correlational study was carried out applying two online questionnaires with quality parameters (content-construct validity and reliability), one on musical preference and the other on personality. The results indicate four main findings: (1) the musical listening of the participants is limited to a reduced number of styles, mainly Pop music and others, typical of Brazilian culture; (2) the Brazilian context supposes a determining aspect in the low preference of non-Brazilian music; (3) there is a positive correlation between most personality types analyzed and the Latin, Brazilian, Classical and Ethnic musical styles. A negative correlation between these types of personality and the consumption of Rock music was also observed; (4) musical preferences are driven not only by personality but in some cases they are also driven by socio-demographic variables (i.e., age and gender). Likewise, this work shows how participants make use of music in personality aspects that may be of interest for the analysis of socio-affective behavior (personality) as well as according to different socio-demographic variables (e.g., age and gender). More cross-cultural research on musical preference and personality would need to be carried out from a global perspective, framed in the context of social psychology and studies of mass communication.

Introduction to the Special Section on Multimedia Computing and Applications of Socio-Affective Behaviors in the Wild

Introduction to the Special Section on Multimedia Computing and Applications of Socio-Affective Behaviors in the Wild

Long-term programing of psychopathology-like behaviors in male rats by peripubertal stress depends on individual’s glucocorticoid responsiveness to stress

Experience of adversity early in life and dysregulation of hypothalamus–pituitary–adrenocortical (HPA) axis activity are risk factors often independently associated with the development of psychopathological disorders, including depression, PTSD and pathological aggression. Additional evidence suggests that in combination these factors may interact to shape the development and expression of psychopathology differentially, though little is known about underlying mechanisms. Here, we studied the long-term consequences of early life stress exposure on individuals with differential constitutive glucocorticoid responsiveness to repeated stressor exposure, assessing both socio-affective behaviors and brain activity in regions sensitive to pathological alterations following stress. Two rat lines, genetically selected for either low or high glucocorticoid responsiveness to repeated stress were exposed to a series of unpredictable, fear-inducing stressors on intermittent days during the peripuberty period. Results obtained at adulthood indicated that having high glucocorticoid responses to repeated stress and having experience of peripuberty stress independently enhanced levels of psychopathology-like behaviors, as well as increasing basal activity in several prefrontal and limbic brain regions in a manner associated with enhanced behavioral inhibition. Interestingly, peripuberty stress had a differential impact on aggression in the two rat lines, enhancing aggression in the low-responsive line but not in the already high-aggressive, high-responsive rats. Taken together, these findings indicate that aberrant HPA axis activity around puberty, a key period in the development of social repertoire in both rats and humans, may alter behavior such that it becomes anti-social in nature.

Exploring Music-Based Rehabilitation for Parkinsonism through Embodied Cognitive Science.

Recent embodied approaches in cognitive sciences emphasize the constitutive roles of bodies and environment in driving cognitive processes. Cognition is thus seen as a distributed system based on the continuous interaction of bodies, brains, and environment. These categories, moreover, do not relate only causally, through a sequential input–output network of computations; rather, they are dynamically enfolded in each other, being mutually implemented by the concrete patterns of actions adopted by the cognitive system. However, while this claim has been widely discussed across various disciplines, its relevance and potential beneficial applications for music therapy remain largely unexplored. With this in mind, we provide here an overview of the embodied approaches to cognition, discussing their main tenets through the lenses of music therapy. In doing so, we question established methodological and theoretical paradigms and identify possible novel strategies for intervention. In particular, we refer to the music-based rehabilitative protocols adopted for Parkinson’s disease patients. Indeed, in this context, it has recently been observed that music therapy not only affects movement-related skills but that it also contributes to stabilizing physiological functions and improving socio-affective behaviors. We argue that these phenomena involve previously unconsidered aspects of cognition and (motor) behavior, which are rooted in the action-perception cycle characterizing the whole living system.

Predictable enriched environment prevents development of hyper-emotionality in the VPA rat model of autism.

Understanding the effects of environmental stimulation in autism can improve therapeutic interventions against debilitating sensory overload, social withdrawal, fear and anxiety. Here, we evaluate the role of environmental predictability on behavior and protein expression, and inter-individual differences, in the valproic acid (VPA) model of autism. Male rats embryonically exposed (E11.5) either to VPA, a known autism risk factor in humans, or to saline, were housed from weaning into adulthood in a standard laboratory environment, an unpredictably enriched environment, or a predictably enriched environment. Animals were tested for sociability, nociception, stereotypy, fear conditioning and anxiety, and for tissue content of glutamate signaling proteins in the primary somatosensory cortex, hippocampus and amygdala, and of corticosterone in plasma, amygdala and hippocampus. Standard group analyses on separate measures were complemented with a composite emotionality score, using Cronbach's Alpha analysis, and with multivariate profiling of individual animals, using Hierarchical Cluster Analysis. We found that predictable environmental enrichment prevented the development of hyper-emotionality in the VPA-exposed group, while unpredictable enrichment did not. Individual variation in the severity of the autistic-like symptoms (fear, anxiety, social withdrawal and sensory abnormalities) correlated with neurochemical profiles, and predicted their responsiveness to predictability in the environment. In controls, the association between socio-affective behaviors, neurochemical profiles and environmental predictability was negligible. This study suggests that rearing in a predictable environment prevents the development of hyper-emotional features in animals exposed to an autism risk factor, and demonstrates that unpredictable environments can lead to negative outcomes, even in the presence of environmental enrichment.

Top-Down Control of Serotonin Systems by the Prefrontal Cortex: A Path toward Restored Socioemotional Function in Depression

Social withdrawal, increased threat perception, and exaggerated reassurance seeking behaviors are prominent interpersonal symptoms in major depressive disorder (MDD). Altered serotonin (5-HT) systems and corticolimbic dysconnectivity have long been suspected to contribute to these symptomatic facets; however, the underlying circuits and intrinsic cellular mechanisms that control 5-HT output during socioemotional interactions remain poorly understood. We review literature that implicates a direct pathway between the ventromedial prefrontal cortex (vmPFC) and dorsal raphe nucleus (DRN) in the adaptive and pathological control of social approach-avoidance behaviors. Imaging and neuromodulation during approach-avoidance tasks in humans point to the cortical control of brainstem circuits as an essential regulator of socioemotional decisions and actions. Parallel rodent studies using viral-based connectomics and optogenetics are beginning to provide a cellular blueprint of the underlying circuitry. In these studies, manipulations of vmPFC synaptic inputs to the DRN have revealed bidirectional influences on socioaffective behaviors via direct monosynaptic excitation and indirect disynaptic inhibition of 5-HT neurons. Additionally, adverse social experiences that result in permanent avoidance biases, such as social defeat, drive long-lasting plasticity in this microcircuit, potentiating the indirect inhibition of 5-HT output. Conversely, neuromodulation of the vmPFC via deep brain stimulation (DBS) attenuates avoidance biases by restoring the direct excitatory drive of 5-HT neurons and strengthening a key subset of forebrain 5-HT projections. Better understanding the cellular organization of the vmPFC-DRN pathway and identifying molecular determinants of its neuroplasticity can open fundamentally novel avenues for the treatment of affective disorders.

HDAC6 Regulates Glucocorticoid Receptor Signaling in Serotonin Pathways with Critical Impact on Stress Resilience

Genetic variations in certain components of the glucocorticoid receptor (GR) chaperone complex have been associated with the development of stress-related affective disorders and individual variability in therapeutic responses to antidepressants. Mechanisms that link GR chaperoning and stress susceptibility are not well understood. Here, we show that the effects of glucocorticoid hormones on socioaffective behaviors are critically regulated via reversible acetylation of Hsp90, a key component of the GR chaperone complex. We provide pharmacological and genetic evidence indicating that the cytoplasmic lysine deacetylase HDAC6 controls Hsp90 acetylation in the brain, and thereby modulates Hsp90-GR protein-protein interactions, as well as hormone- and stress-induced GR translocation, with a critical impact on GR downstream signaling and behavior. Pet1-Cre-driven deletion of HDAC6 in serotonin neurons, the densest HDAC6-expressing cell group in the mouse brain, dramatically reduced acute anxiogenic effects of the glucocorticoid hormone corticosterone in the open-field, elevated plus maze, and social interaction tests. Serotonin-selective depletion of HDAC6 also blocked the expression of social avoidance in mice exposed to chronic social defeat and concurrently prevented the electrophysiological and morphological changes induced, in serotonin neurons, by this murine model of traumatic stress. Together, these results identify HDAC6 inhibition as a potential new strategy for proresilience and antidepressant interventions through regulation of the Hsp90-GR heterocomplex and focal prevention of GR signaling in serotonin pathways. Our data thus uncover an alternate mechanism by which pan-HDAC inhibitors may regulate stress-related behaviors independently of their action on histones.

Long‐term effects of differential early rearing in rhesus macaques: Behavioral reactivity in adulthood

Adverse early experiences are associated with a range of deleterious health outcomes in humans, including higher risk for affective disorders. Studies using a long-standing model of nonhuman primate model of early adversity have demonstrated that nursery-reared (NR) monkeys exhibit alterations in multiple aspects of biobehavioral development; however, few studies have evaluated the persistence of socioaffective behavioral changes through adulthood. We evaluated the effects of early rearing experience on adult animals' response to a well-validated assessment of anxiety-like behavior, the human intruder paradigm (HIP). We tested 22 rhesus monkeys who were either nursery-reared (NR) or reared with their mothers (mother-reared; MR). NR monkeys were inhibited in their behavior compared to MR monkeys, with reduced locomotion and exploratory behaviors. NR animals showed a marginal increase in freezing. Together these findings demonstrate that the consequences of differential infant rearing experience on socioaffective behavior persist into adulthood, with evidence of greater inhibition in NR monkeys.

The cross-generation transmission of oxytocin in humans

Animal studies demonstrated that the neuropeptide oxytocin (OT), implicated in bond formation across mammalian species, is transmitted from mother to young through mechanisms of early social experiences; however, no research has addressed the cross-generation transmission of OT in humans. Fifty-five parents (36 mothers and 19 fathers) engaged in a 15-min interaction with their infants. Baseline plasma OT was sampled from parents and salivary OT was sampled from parents and infants before and after play and analyzed with ELISA methods. Interactions were micro-coded for parent and child's socio-affective behavior. Parent and infant's salivary OT was individually stable across assessments and showed an increase from pre- to post-interaction. Significant correlations emerged between parental and infant OT at both assessments and higher OT levels in parent and child were related to greater affect synchrony and infant social engagement. Parent–infant affect synchrony moderated the relations between parental and infant OT and the associations between OT in parent and child were stronger under conditions of high affect synchrony. Results demonstrate consistency in the neuroendocrine system supporting bond formation in humans and other mammals and underscore the role of early experience in shaping the cross-generation transmission of social affiliation in humans.