Oxytocin has often been called the ‘social hormone’ or ‘love hormone’ (e.g., Pedersen, 2004)–a characterization that is enormously over-simplified (see Yong, 2012; Beery, 2015; Carter, 2021). Although the hormone is involved in parturition (i.e., the birth process; e.g., Kenkel, 2021), lactation (e.g., Crowley & Armstrong, 1992), and the formation of social bonds (see Carter et al., 2008) for many mammals, oxytocin (OT) is also deeply involved in a variety of homeostatic processes. From metabolism and energetics, to smooth muscle tone and blood pressure regulation, to salt balance and thermal homeostasis, OT plays a critical role.
Recent findings from our lab, for example, highlight that OT not only modulates both social behavior and temperature homeostasis, but that the social and thermal effects of OT act together to produce adaptive outcomes in mice. Huddling is a critical behavior for many small mammals, including rats and mice. Previous studies demonstrated that when pups experience cool temperatures they fire up deposits of thermogenic brown adipose tissue (BAT), which both produce heat for individual comfort and become ‘hot spots’ that attract contact from nearby pups seeking warmth (e.g., Sokoloff & Blumberg, 2001; Harshaw et al., 2014). When researchers inactivate these BAT deposits pups are thus less attractive to each other and huddles fall apart (Sokoloff & Blumberg, 2001).
In a recent study we documented that OT is a critical modulator of multiple aspects of this dynamic process (Harshaw et al., 2018). As illustrated below, mouse pups with the OT gene inactivated (OTKO) showed severe deficits in BAT thermogenesis, which significantly interfered with their ability to huddle at a room temperature–room temperature for humans being quite cold for mice (see Maloney et al., 2014). As can be seen in the right panel, OTKO pups were often forced to the outside of the group or else to huddle with each other. We also found that male OTKO pups displayed an apparent deficit in attraction to warmth (i.e., thermotaxis) when placed on a thermocline (i.e., a carefully calibrated device with a controlled thermal gradient). Such findings suggests that the physiological and neural systems that support energetics and metabolism have co-evolved to support adaptive social behavior (cf. Harshaw et al., 2017). The “warm and fuzzy” feeling sometimes elicited by close attachment relationships is almost certainly a byproduct of this.
Because the thermal effects of OT in the context of huddling by young animals could theoretically be a highly specific ontogenetic adaptation, the question remains as to whether OT has a similar role in other social behaviors, particularly during adulthood. In a series of follow-up experiments we are thus exploring whether the social effects of OT depend at all on the hormone’s thermal effects in adult mice. In a recent study, for example, we examined how the OT receptor (OTR) contributes to the temperature elevation that typically occurs during social interaction (i.e., ‘social hyperthermia’; Harshaw et al., 2021). As illustrated below, when we administered a drug that blocked the OTR receptor (i.e., an OTR antagonist) this significantly diminished the display of social hyperthermia in response to a 10 min test involving interaction with a stranger (Harshaw et al., 2021). Blocking β3 adrenergic receptors, which are known to mediate stress-induced hyperthermia, had no such effect (data not shown).
We also examined the relationship between social hyperthermia and specific social behaviors. Despite the fact that OTR-A treatment significantly reduced both social hyperthermia and initiated social behavior, the amount of temperature elevation displayed by individuals during social interaction was most closely associated with behaviors indicative of anxiety, including caution and avoidance (Harshaw et al., 2021). This finding adds to a growing literature suggesting that OT contributes both to the positive and negative aspects of social behavior (see Yong, 2012; Masis-Calvo et al., 2018).
In a follow up study funded by the Louisiana Board of Regents (grant # LEQSF(2022-25)-RD-A-29) we are replicating key aspects of our prior study using a more precise method of quantifying social hyperthermia (i.e., temperature reporting RFID tags). In addition, we are examining the contribution of both OT and V1AR to the display of hyperthermia in both social and non-social contexts. This will help to answer the question of whether OT-dependent social hyperthermia is a unique response to specifically social situations or simply a specific instance of the general phenomenon of emotional hyperthermia.