Abstract
Caregiving by nonparents (alloparenting) and fathers is a defining aspect of human social behavior, yet this phenomenon is rare among mammals. Male prairie voles (Microtus ochrogaster) spontaneously exhibit high levels of alloparental care, even in the absence of reproductive experience. In previous studies, exposure to a pup was selectively associated with increased activity in oxytocin and vasopressin neurons along with decreased plasma corticosterone. In the present study, physiological, pharmacological and neuroanatomical methods were used to explore the autonomic and behavioral consequences of exposing male prairie voles to a pup. Reproductively naïve, adult male prairie voles were implanted with radiotransmitters used for recording ECG, temperature and activity. Males responded with a sustained increase in heart-rate during pup exposure. This prolonged increase in heart rate was not explained by novelty, locomotion or thermoregulation. Although heart rate was elevated during pup exposure, respiratory sinus arrhythmia (RSA) did not differ between these males and males exposed to control stimuli indicating that vagal inhibition of the heart was maintained. Blockade of beta-adrenergic receptors with atenolol abolished the pup-induced heart rate increase, implicating sympathetic activity in the pup-induced increase in heart rate. Blockade of vagal input to the heart delayed the males’ approach to the pup. Increased activity in brainstem autonomic regulatory nuclei was also observed in males exposed to pups. Together, these findings suggest that exposure to a pup activates both vagal and sympathetic systems. This unique physiological state (i.e. increased sympathetic excitation of the heart, while maintaining some vagal cardiac tone) associated with male caregiving behavior may allow males to both nurture and protect infants.
Highlights
Caregiving directed toward infants by nonparents, sometimes called alloparenting, is common to many human cultures [1] and is critical to human evolution and development [2,3,4]
Across the 20 minutes of stimulus exposure, the correlations between heart rate and respiratory sinus arrhythmia (RSA) were significantly stronger in the pup condition (–.546.06), compared to either the dowel condition (–.256.12) or the female condition (– .166.11, p,0.02 for both comparisons, Fig. 1B)
Due to the small sample sizes and short duration of stimulus presentation in the pup attacking subset, data from the animals that did not show alloparenting were not analyzed. The results of this series of experiments revealed that alloparental behavior in male prairie voles is associated with a sustained increase in heart rate
Summary
Caregiving directed toward infants by nonparents, sometimes called alloparenting, is common to many human cultures [1] and is critical to human evolution and development [2,3,4]. Understanding alloparental care is critically important for many reasons including the fact that children are between eight [7] and fifty [8] times more likely to suffer fatal abuse when living with an unrelated adult male, i.e. while under alloparental care. Prairie voles (Microtus ochrogaster) are small, socially monogamous rodents that have been useful for understanding the neurobiological basis of various social behaviors [9,10]. Male prairie voles display high levels of alloparental behavior [11] and often remain with their natal family, serving as alloparents [12]. Stressful experiences, such as a forced swim or treatment with exogenous corticosterone, facilitate subsequent alloparental behavior in male, but not female prairie voles [13]. Our studies of the immediate consequences of pup exposure revealed a decreased concentration of plasma corticosterone compared to control subjects [14], initially suggesting the hypothesis that interactions with the pup might have anxiolytic properties; that is, males may approach and huddle over the pup as a means to cope emotionally with negative experiences
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