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

Abstract

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.