Positive social behaviours are induced and retained after oxytocin manipulations mimicking endogenous concentrations in a wild mammal

Abstract

The neuropeptide hormone oxytocin modulates numerous social and parental behaviours across a wide range of species, including humans. We conducted manipulation experiments on wild grey seals (Halichoerus grypus) to determine whether oxytocin increases proximity-seeking behaviour, which has previously been correlated with endogenous oxytocin concentrations in wild seal populations. Pairs of seals that had never met previously were given intravenous injections of 0.41 µg kg−1 oxytocin or saline and were observed for 1 h post-manipulation. The dose was designed to mimic endogenous oxytocin concentrations during the observation period, and is one of the lowest doses used to manipulate behaviour to date. Seals given oxytocin spent significantly more time in close proximity to each other, confirming that oxytocin causes conspecifics to seek others out and remain close to one another. Aggressive and investigative behaviours also significantly fell after oxytocin manipulations. Despite using a minimal oxytocin dose, pro-social behavioural changes unexpectedly persisted for 2 days despite rapid dose clearance from circulation post-injection. This study verifies that oxytocin promotes individuals staying together, demonstrating how the hormone can form positive feedback loops of oxytocin release following conspecific stimuli, increased motivation to remain in close proximity and additional oxytocin release from stimuli received while in close proximity.

Effects of route of administration on oxytocin-induced changes in regional cerebral blood flow in humans

“…We provide first evidence that the intravenous infusion of OT echoes the effects of a standard spray administration on brain's physiology within key neural circuits at rest. These effects are consistent with previous observations of improved repetitive behaviours and social cognition in ASD patients after intravenous administration of OT [21][22][23][24] and provide a possible mechanism by which these therapeutical effects may arise. Therefore, our findings challenge the current assumption that key effects of intranasal OT on brain function and behaviour are entirely derived by direct nose-to-brain transport.…”

“…These mechanisms might account for the effects of peripherally administered OT (e.g. intravenous infusion) on behaviour [21][22][23][24] .…”

Effects of route of administration on oxytocin-induced changes in regional cerebral blood flow in humans

“…We provide first evidence that the intravenous infusion of OT echoes the effects of a standard spray administration on brain's physiology within key neural circuits at rest. These effects are consistent with previous observations of improved repetitive behaviours and social cognition in ASD patients after intravenous administration of OT (24)(25)(26)(27) and provide a possible mechanism by which these therapeutical effects on behaviour may arise. Therefore, our findings challenge the current assumption that key effects of intranasal OT on brain function and behaviour are entirely derived by direct nose-to-brain transport.…”

“…These mechanisms might explain why OT when administered peripherally (e.g. intravenous infusion) can still impact behaviour (24)(25)(26)(27).…”

Social creatures: Model animal systems for studying the neuroendocrine mechanisms of social behaviour

“…Neuroendocrine systems play an important role in social behaviour because they can act on both the peripheral and central structures needed for its expression. Neuropeptides acting within a variety of brain regions regulate how signals from conspecifics are interpreted and responded to, whereas hormones acting throughout the body of an individual ensure that the tissues and organs needed to successfully perform social behaviours such as reproduction are present and functioning . Neuroendocrine systems and the brain structures they act on to promote social behaviour are well conserved across vertebrate species and, in some cases, are also present in invertebrates .…”