The animal and human neuroendocrinology of social cognition, motivation and behavior

Max Planck Institute for Human Cognitive and Brain Sciences, Department of Social Neuroscience, Leipzig, Germany.
Nature Neuroscience (Impact Factor: 16.1). 04/2012; 15(5):681-8. DOI: 10.1038/nn.3084
Source: PubMed


Extensive animal and recent human research have helped inform neuroendocrinological models of social cognition, motivation and behavior. In this review, we first summarize important findings regarding oxytocin, arginine vasopressin and testosterone in the domains of affiliation, social cognition, aggression and stress/anxiety. We then suggest ways in which human research can continue to profit from animal research, particularly by exploring the interactive nature of neuromodulatory effects at neurochemical, organismic and contextual levels. We further propose methods inspired by the animal literature for the ecologically valid assessment of affiliative behavior in humans. We conclude with suggestions for how human research could advance by directly assessing specific social cognitive and motivational mechanisms as intermediate variables. We advocate a more comprehensive look at the distinct networks identified by social neuroscience and the importance of a motivational state, in addition to approach and avoidance, associated with quiescence and homeostatic regulation.

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Available from: Cade McCall, Aug 19, 2014
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    • "This work has been reviewed elsewhere extensively (e.g. Macdonald and Feifel, 2013; Guastella and MacLeod, 2012; McCall and Singer, 2012; Kumsta and Heinrichs, 2013). Single dose studies in healthy volunteers have reported on increased trust (Kosfeld et al., 2005), empathic accuracy (Domes et al., 2006, Guastella et al., 2009), time spent looking at eyes (Guastella et al., 2008), and face identity recognition memory (Savaskan et al., 2008; Rimelle et al., 2009). "
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    ABSTRACT: Background There is a paucity of treatments targeting core symptom domains in autism spectrum disorder (ASD). Several animal models and research in typically developing volunteers suggests that manipulation of the oxytocin system may have therapeutic potential for the treatment of social deficits. We review the literature for oxytocin and ASD and report on early dosing, safety and efficacy data of multi-dose oxytocin on aspects of social cognition/function, as well as repetitive behaviors and co-occurring anxiety within ASD. Methods Fifteen children and adolescents with verbal IQs ≥70 were diagnosed with ASD using the ADOS and the ADI-R. They participated in a modified maximum tolerated dose study of intranasal oxytocin (Syntocinon). Data were modeled using repeated measures regression analysis controlling for week, dose, age, and sex. Results Among 4 doses tested, the highest dose evaluated, 0.4 IU/kg/dose, was found to be well tolerated. No serious or severe adverse events were reported and adverse events reported/observed were mild to moderate. Over 12 weeks of treatment, several measures of social cognition/function, repetitive behaviors and anxiety showed sensitivity to change with some measures suggesting maintenance of effect 3 months past discontinuation of intranasal oxytocin. Conclusions This pilot study suggests that daily administration of intranasal oxytocin at 0.4 IU/kg/dose in children and adolescents with ASD is safe and has therapeutic potential. Larger studies are warranted.
    Brain research 09/2014; 1580. DOI:10.1016/j.brainres.2014.01.049 · 2.84 Impact Factor
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    • "Although we did not measure depressive behaviors per se in the current study, this would be worth pursing in the future, particularly in relation to clinical evidence that psychosocial stressors contribute to depressive symptoms and psychological distress after TBI [74], as well as an emerging association between depression and compromised sexuality amongst TBI survivors [75], [76]. An alternative possibility is that sexual anhedonia may reflect injury-induced disturbances in the endocrine system and reduced levels of key neuropeptides and androgens [67], [77], [78]. Recent clinical studies have highlighted the prevalence of endocrine disturbances after TBI in both children and adults [79], [80], [81], whereby pituitary function may appear normal acutely but become impaired over months post-injury [82], [83]. "
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    ABSTRACT: Despite the life-long implications of social and communication dysfunction after pediatric traumatic brain injury, there is a poor understanding of these deficits in terms of their developmental trajectory and underlying mechanisms. In a well-characterized murine model of pediatric brain injury, we recently demonstrated that pronounced deficits in social interactions emerge across maturation to adulthood after injury at postnatal day (p) 21, approximating a toddler-aged child. Extending these findings, we here hypothesized that these social deficits are dependent upon brain maturation at the time of injury, and coincide with abnormal sociosexual behaviors and communication. Age-dependent vulnerability of the developing brain to social deficits was addressed by comparing behavioral and neuroanatomical outcomes in mice injured at either a pediatric age (p21) or during adolescence (p35). Sociosexual behaviors including social investigation and mounting were evaluated in a resident-intruder paradigm at adulthood. These outcomes were complemented by assays of urine scent marking and ultrasonic vocalizations as indices of social communication. We provide evidence of sociosexual deficits after brain injury at p21, which manifest as reduced mounting behavior and scent marking towards an unfamiliar female at adulthood. In contrast, with the exception of the loss of social recognition in a three-chamber social approach task, mice that received TBI at adolescence were remarkably resilient to social deficits at adulthood. Increased emission of ultrasonic vocalizations (USVs) as well as preferential emission of high frequency USVs after injury was dependent upon both the stimulus and prior social experience. Contrary to the hypothesis that changes in white matter volume may underlie social dysfunction, injury at both p21 and p35 resulted in a similar degree of atrophy of the corpus callosum by adulthood. However, loss of hippocampal tissue was greater after p21 compared to p35 injury, suggesting that a longer period of lesion progression or differences in the kinetics of secondary pathogenesis after p21 injury may contribute to observed behavioral differences. Together, these findings indicate vulnerability of the developing brain to social dysfunction, and suggest that a younger age-at-insult results in poorer social and sociosexual outcomes.
    PLoS ONE 08/2014; 9(8):e103386. DOI:10.1371/journal.pone.0103386 · 3.23 Impact Factor
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    • "Paranoid patients have also been found to take longer to make judgements about gaze direction (Franck et al., 2002), make more errors in gaze discrimination (Russell et al., 2001) and also misinterpret averted gaze as being directed towards them (Hooker and Park, 2005). The neuropeptide oxytocin has been extensively investigated in terms of its role in social behaviour (McCall and Singer, 2012), and as a potential therapeutic tool for enhancing prosocial behaviour (e.g. Yamasue et al., 2012). "
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    ABSTRACT: Patients with schizophrenia suffer from dysfunctional social behaviour. Social approach and avoidance (AA) has been associated with motor responses, as the affective valence and gaze direction of facial stimuli can bias push and pull motor tendencies. The aim of this study was to investigate the role of endogenous oxytocin in social AA behaviour in schizophrenia. Basal plasma oxytocin levels were collected from 28 patients who were then given a joystick-based Approach-Avoidance Task (AAT). Reaction times were recorded and AAT effect scores calculated for responses to happy and angry faces, which either had direct or averted gaze. Individual differences in basal oxytocin had a significant relationship with AAT responses, and patients with higher levels of oxytocin tended to avoid angry faces more. Furthermore, greater avoidance of angry faces was correlated with more severe psychotic (positive and general) symptoms and greater paranoia. This suggests that the endogenous effects of oxytocin may be specific to the interpretation of negative threatening emotions in schizophrenia patients, and also provides evidence that psychotic symptoms and paranoia can impact on social AA behaviour by heightening threat avoidance.
    Psychiatry Research 07/2014; DOI:10.1016/j.psychres.2014.06.038 · 2.47 Impact Factor
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