Calling for help is independently modulated by brain systems underlying goal-directed behavior and threat perception

Abstract

In primates, during times of need, calling for help is a universal experience. Calling for help recruits social support and promotes survival. However, calling for help also can attract predators, and it is adaptive to inhibit calls for help when a potential threat is perceived. Based on this, we hypothesized that individual differences in calling for help would be related to the activity of brain systems that mediate goal-directed behavior and the detection of threat. By using high-resolution positron emission tomography in rhesus monkeys undergoing social separation, we demonstrate that increased [ 18 F]-fluoro-2-deoxy-D-glucose uptake in the right dorsolateral prefrontal cortex and decreased uptake in the amygdala independently predict individual differences in calling for help. When taken together, these two regions account for 76% of the variance in calling for help. This result suggests that the drive for affiliation and the perception of threat determine the intensity of an individual's behavior during separation. These findings in monkeys are relevant to humans and provide a conceptual neural framework to understand individual differences in how primates behave when in need of social support.anxiety ͉ monkey ͉ positron emission tomography S table attachment bonds are fundamentally important to the success of social primates. Moreover, when attachment bonds are disrupted, separated individuals are more vulnerable to threatening environmental stressors, including predation. During separation, individuals experience varying levels of distress that motivate them to engage in behaviors that increase their likelihood of reunion. Vocalizations expressed during separation are vital because they signal the need for social support and help other group members locate the individual in need.Extensive studies in rhesus monkeys have characterized the parameters of separation-induced vocalizations, or coo calls, as well as the neurochemical mechanisms that modulate their expression (1). Furthermore, it has been suggested that these high-pitched vocalizations are analogous to human cries (2). Rhesus monkeys are particularly well suited to study mechanisms underlying individual differences in human responses to separation because of similarities between the two species in social behavior, the expression of psychopathology, and in brain systems, such as the prefrontal cortex, that are involved in the regulation of emotion (3).In any given situation, the degree to which an individual calls for help is related to numerous factors. These factors include not only the amount of distress that an individual experiences and the importance of social support at that time but also the risks related to calling for help. Research from our laboratory demonstrates that when separated monkeys are exposed to a potential threat, they decrease their calling for help (1). In the process of assessing the extent to which potential predatorial threat is real, the adaptive response is to engage in behaviors that reduce the likelihood of detectio...

Neonatal perirhinal cortex lesions impair monkeys’ ability to modulate their emotional responses.

“…Increased cooing in adulthood could be related to the increase in anxiety-like behaviors reported, a finding consistent with the classification of “coos” in the basic measures of primate anxiety/displacement behaviors (Hinde & Rowell, 1962; Jiang et al, 2013; Mcfarland, 1966; Redican, 1975). This increase in cooing behavior may have resulted from a decrease in amygdala drive after the lack of PRh inputs since amygdala activity has been negatively correlated with frequency of separation-induced coo vocalization in adolescent monkeys (Fox et al, 2005) and amygdala lesions increase coos (Kalin, Shelton, & Davidson, 2004; Kalin et al, 2001; Raper et al, 2013a)…”

Neuropeptide Y Receptor Gene Expression in the Primate Amygdala Predicts Anxious Temperament and Brain Metabolism

“…We have established a non-human primate model of childhood AT, facilitating the identification of the neural mechanisms underlying the development of early life anxiety. In rhesus monkeys, AT is assessed as a composite of threat-induced freezing behavior, inhibition of vocalizations and increased plasma cortisol levels (4, 5). We previously demonstrated that metabolic activity in the central nucleus (Ce) of the amygdala, indexed using high-resolution [ 18 F]-fluorodeoxyglucose-positron emission tomography (FDG-PET), strongly predicts individual differences in AT (6, 7).…”

The serotonin transporter genotype is associated with intermediate brain phenotypes that depend on the context of eliciting stressor

“…Furthermore, the impacts of different types of ethologically relevant stressors on behavioral, neurochemical, physiological and brain functional responses have been well characterized in this species. [26][27][28] We have been performing highresolution FDG microPET scans in rhesus monkeys to explore the relation between patterns of brain metabolic activity and individual differences in anxiety-related traits. For example, we previously demonstrated that when threatened by a human intruder for a 30-min period, monkeys' individual differences in metabolic activity in the bed nucleus of the stria terminalis (BNST) are strongly predictive of individual differences in monkeys' anxiety-related freezing responses.…”