Maladaptive cardiac and behavioral reactivity to repeated vicarious stress exposure in socially bonded male prairie vole siblings.

Behaviors, emotions, and cardiovascular functions are influenced by stress. But these detrimental effects are not exclusive to an individual that directly experiences stress. Stress is also experienced vicariously through observation of another individual undergoing stress. The current study used the strong social bonds in socially monogamous prairie voles to determine effects of repeated vicarious stress on cardiac and behavioral outcomes. Male prairie voles were exposed to either a 5-minute open field chamber alone [separate (control)] or while concurrently witnessing their sibling undergo a tail-suspension stressor [concurrent (experimental)], repeated across 4 sessions. Cardiac responses in animals in the open field were evaluated for heart rate and heart rate variability prior to, during, and after each test session, and behaviors were evaluated for motion, exploration, stress reactivity, and anxiety-relevant behaviors during each test session. The concurrent condition (versus separate) displayed increased heart rate and reduced heart rate variability during repeated test sessions, and impaired recovery of these parameters following the test sessions. The pattern of disturbances suggests that both increased sympathetic and reduced parasympathetic influence contributed to the cardiac responses. Animals in the concurrent condition (versus separate) displayed disrupted rearing, grooming, and motion; reduced duration of center section exploration; and increased freezing responses across repeated test sessions. Collectively, cardiac and behavioral stress reactivity are increased as a function of vicarious stress in prairie voles, which are evident across repeated experiences of stress. These results inform our understanding of the experience of vicarious stress in social species, including humans.

Differential paraventricular nucleus activation and behavioral responses to social isolation in prairie voles following environmental enrichment with and without physical exercise.

Social stressors produce neurobiological and emotional consequences in social species. Environmental interventions, such as environmental enrichment and exercise, may modulate physiological and behavioral stress responses. The present study investigated the benefits of environmental enrichment and exercise against social stress in the socially monogamous prairie vole. Female prairie voles remained paired with a sibling (control) or were isolated from a sibling for 4 weeks. The isolated groups were assigned to isolated sedentary, isolated with environmental enrichment, or isolated with both enrichment and exercise conditions. Behaviors related to depression, anxiety, and sociality were investigated using the forced swim test (FST), elevated plus maze (EPM), and a social crowding stressor (SCS), respectively. cFos expression was evaluated in stress-related circuitry following the SCS. Both enrichment and enrichment with exercise protected against depression-relevant behaviors in the FST and social behavioral disruptions in the SCS, but only enrichment with exercise protected against anxiety-related behaviors in the EPM and altered cFos expression in the hypothalamic paraventricular nucleus in isolated prairie voles. Enrichment may improve emotion-related and social behaviors, however physical exercise may be an important component of environmental strategies for protecting against anxiety-related behaviors and reducing neural activation as a function of social stress.

Physiological and behavioral responses to observing a sibling experience a direct stressor in prairie voles.

Uncontrollable stress precipitates negative mental and physical health outcomes. Furthermore, the vicarious experience of stress (e.g. observing another individual experience a direct stressor) can mimic the effects of directly experiencing the stressor. The current experiment examined the behavioral and physiological effects of the vicarious experience of stress using the socially monogamous prairie vole. Male prairie voles were exposed to either an empty open field chamber, or a chamber in which the animal observed a sibling undergoing a concurrent direct physical stressor (tail suspension test) for five minutes. Exploratory and anxiety-like behaviors were recorded in all observers during the test session. Cardiac indices of heart rate and heart rate variability were recorded in a subset of observers prior to, during, and following the test session. Corticosterone levels were measured in all observers and siblings following the test session. When compared to animals exposed to an empty open field chamber, animals that observed a sibling undergo a direct physical stressor exhibited increased heart rate and circulating corticosterone, and decreased heart rate variability. These physiological stress indicators were supported by behavioral changes, including increased freezing followed immediately by orienting of the head toward the center of the apparatus, and decreased locomotion, grooming, and rearing. These preliminary results suggest that prairie voles experience stress vicariously, and provide a foundation for additional studies focused on the underlying mechanisms of vicarious stress. The use of this model may inform our understanding of the social transmission of stress among social species, including humans.LAY SUMMARYThe experience of stress, including observing stress in a loved one, has negative consequences on mental and physical health. This study used a social rodent (prairie voles) to demonstrate that stress transfers among social individuals, consequently producing an increased physiological and behavioral stress response in prairie voles observing their siblings experience stress. This research informs our understanding of the interactions of social experiences and stress in humans.