Autonomic Substrates of the Response to Pups in Male Prairie Voles

• Type of Material: Article
• Authors: William M. Kenkel, University of Illinois at Chicago; Jamespaul Paredes, Emory University; Gregory F. Lewis, University of Illinois at Chicago; Jason R. Yee, University of Illinois at Chicago; Hossein Pournajafi-Nazarloo, University of Illinois at Chicago; Angela J. Grippo, Northern Illinois University; Stephen W. Porges, University of Illinois at Chicago; C. Sue Carter, University of Illinois at Chicago
• Language: English
• Date: 2013-08-05
• Publisher: PLoS One
• Publication Version: Final Published Version
• Copyright Statement: Copyright © 2013 Kenkel et al
• License: Creative Commons Attribution 4.0 International
• Final Published Version (URL): http://dx.doi.org/10.1371/journal.pone.0069965
• Title of Journal or Parent Work: PLoS One
• Volume: 8
• Issue: 8
• Start Page: e69965
• End Page: e69965
• Grant/Funding Information: The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.; This research was supported by National Institutes of Mental Health grants MH73233 (AJG), MH67446 (SWP), and MH72935 (CSC), and National Institute of Child Health and Human Development grant HD38490 (CSC).
• Research Categories: Biology, General; Biology, Neuroscience

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.