Cardioacceleration in alloparents in response to stimuli from prairie vole pups: The significance of thermoregulation

Abstract

Autonomic responses, including changes in heart rate and respiratory sinus arrhythmia (RSA) can provide indications of emotional reactivity to social stimuli in mammals. We have previously reported that male prairie voles (Microtus ochrogaster) spontaneously care for unfamiliar infants, showing a robust and sustained increase in heart rate in the presence of a pup, thus providing an opportunity to examine the physiology of care-giving in reproductively naïve animals. However, the purpose of such heart rate increases has not been explained by previous efforts. In the present study, we first compared male and female prairie vole cardiac responses in the presence of a pup and found no evidence of sex differences in heart rate or RSA. Using male prairie voles, we then examined the characteristics of pups that were capable of eliciting physiological responses, including age of the pup and pup odors. As prairie vole pups increased in age they vocalized less and there was an associated decline in alloparental cardioacceleration. Exposure to pup-related odors induced cardioacceleration in adult males and this effect also diminished with increasing pup age. Finally, we were able to block the cardioacceleratory effect when the testing environment was warmed to a temperature of 36° C [versus ambient room temperature (approximately 22° C)]. These findings suggest that pup-induced cardioacceleration is a robust phenomenon across alloparental prairie voles of both sexes, and depends on multi-modal processing of different stimuli from the pups. Young pups require care-giving behavior, which appears to drive cardioacceleration in the alloparent. This study also supports the usefulness of autonomic measures in the evaluation of social experiences.

The neurobiological causes and effects of alloparenting

“…This response persists throughout a typical 20 minute pup exposure, and does not attenuate nor habituate upon repeated exposures across 3 days, nor extended exposures lasting 60 minutes (Kenkel et al, ). Pup‐induced cardioacceleration can be seen in virgin males (Kenkel et al, ), virgin females (Kenkel et al, ), and sexually experienced fathers (Kenkel et al, ). Pup‐induced cardioacceleration coincided with a decrease in locomotor activity and was dependent on close physical proximity to the pup; merely experiencing pup stimuli was insufficient (Kenkel et al, ).…”

“…The isolation‐induced vocalizations emitted by pups also diminish with advancing pup age, which suggested the pups were becoming more independent and less reliant on alloparental care. Isolation‐induced vocalizations were almost completely abolished in the presence of an alloparent or when the ambient temperature was raised to a thermoneutral 36° (Kenkel et al, ). This then led us to test for pup‐induced cardioacceleration in thermoneutral conditions, where we found it too was greatly diminished.…”

Voluntary exercise facilitates pair-bonding in male prairie voles

“…However, consistent with previous studies [4, 14], the majority of prairie voles tested here responded parentally towards the pup (one animal in the Sedentary treatment attacked the pup). Based on previous research, the high levels of alloparental behavior in this species do not differ between males with and without reproductive experience [15]. Thus, detecting effects of exercise may have been occluded by a ceiling effect.…”

BOLD fMRI in awake prairie voles: A platform for translational social and affective neuroscience

“…It is likely that voles experience a high level of arousal during many commonly used testing paradigms. For example, the maximal heart rate observed during restraint is no different than that displayed during unfettered interaction with a 1-3 day old pup (Kenkel et al, 2015) or while spending time in a novel metabolic cage with wire mesh floor.…”

“…Here, we report on heart rate changes induced by 15 min exposures to: the odor of an unrelated pup (1-3 days old) in the home cage; a freely behaving unrelated pup (1-3 days old) in the home cage; and lastly, exposure to a wire mesh floored cage used for urine collection in metabolic studies (Fig 6c). Data from the pup and pup odor conditions are reprinted with permission from previous work in our lab (Kenkel et al, 2015). All conditions were comprised of 5 adult male and 3 adult females, similar to restraint acclimation.…”