Noxious or Non-noxious Inputs to Oxytocin Neurons: Possible Roles in the Control of Behaviors

Abstract

Oxytocin plays an essential role in milk ejection and parturition in mammals. Oxytocin has also been shown to be involved in the control of various behaviors, including anxiety-related behaviors, food intake and affiliative behaviors.We previously showed that noxious stimuli or stimuli previously paired with noxious stimuli (conditioned fear stimuli) activate hypothalamic oxytocin neurons via activation of brainstem catecholaminergic/prolactin-releasing peptide (PrRP)-positive neurons. Oxytocin neurons are activated not only by noxious stimuli but also by nonnoxious touch stimuli. Social contact has been suggested to activate oxytocin neurons. Non-noxious tactile stimuli induce 50-kHz ultrasonic vocalization, an index of positive states in rats, and activate hypothalamic oxytocin neurons, suggesting that pleasant tactile stimuli activate oxytocin neurons.Physiological roles of oxytocin released during noxious or non-noxious tactile stimuli remain to be clarified. Noxious stimuli increase anxiety-related behavior, while pleasant sensory stimuli have pro-social actions. We have shown that endogenous oxytocin reduces anxiety-related behaviors, induces a decrease in amounts of food intake per meal, and facilitates social recognition via distinct neural pathways. Roles of oxytocin released during sensory stimuli may be dependent upon the sensory stimuli used, and oxytocin may contribute to the prevention of overreactions to noxious stimuli or mediate pro-social or anxiolytic actions of pleasant tactile stimuli.

Roles of Oxytocin in Stress Responses, Allostasis and Resilience

“…Animal studies have shown that various physiological and psychological stressful stimuli, such as noxious stimuli [ 8 ], conditioned fear stimuli [ 9 ], social defeat stress [ 10 , 11 , 12 , 13 , 14 ], immobilization stress [ 15 ], shaker stress [ 16 ], forced swimming [ 17 , 18 ], cold stress [ 19 ], high-intensity exercise [ 20 ] and immune challenges by lipopolysaccharides [ 21 ] or interleukin-1 [ 22 ], activate oxytocin neurons and facilitate the release of oxytocin into the plasma and within the brains of mice and rats [ 23 , 24 , 25 ]. Social instability stress in adolescent female rats has been reported to decrease oxytocin immunoreactivity in the hypothalamic paraventricular nucleus [ 26 ] possibly due to oxytocin release.…”

Role of oxytocin in the control of stress and food intake

“…9 Some stressful stimuli, including noxious stimuli, 10 conditioned fear stimuli, 11 social defeat, [12][13][14][15][16] immobilisation stress, 17 shaker stress 18 and forced swimming 19,20 , as well as administration of lipopolysaccharide 21 and interleukin-1, 22 activate oxytocin-synthesising neurones in the hypothalamus and facilitate oxytocin release into the plasma or within the brain of mice or rats. 9 Some stressful stimuli, including noxious stimuli, 10 conditioned fear stimuli, 11 social defeat, [12][13][14][15][16] immobilisation stress, 17 shaker stress 18 and forced swimming 19,20 , as well as administration of lipopolysaccharide 21 and interleukin-1, 22 activate oxytocin-synthesising neurones in the hypothalamus and facilitate oxytocin release into the plasma or within the brain of mice or rats.…”

“…Stressful stimuli induce stereotypical alarm responses, especially in the neuroendocrine system, autonomic nervous system and immune system and in behaviours, and influence health conditions in humans. 9 Some stressful stimuli, including noxious stimuli, 10 conditioned fear stimuli, 11 social defeat, [12][13][14][15][16] immobilisation stress, 17 shaker stress 18 and forced swimming 19,20 , as well as administration of lipopolysaccharide 21 and interleukin-1, 22 activate oxytocin-synthesising neurones in the hypothalamus and facilitate oxytocin release into the plasma or within the brain of mice or rats. 23,24 Exercise has also been shown to facilitate oxytocin release in horses.…”

“…Activation of oxytocin neurones in response to conditioned fear stimuli is mediated, at least in part, by A2 noradrenergic/prolactinreleasing peptide (PrRP) neurones in the nucleus tractus solitarius of the medulla oblongata 35 and by neurones of the medial amygdala, 36 whereas activation of oxytocin neurones after noxious stimuli has been suggested to be mediated by A1 noradrenergic neurones in the medulla oblongata. 10 The hypothalamic paraventricular and supraoptic nuclei have also been shown to receive inputs not only from noradrenergic neurones in the medulla oblongata, but also from neurones in other stress-related areas, including the amygdala, septum, bed nucleus of the stria terminalis, dorsomedial hypothalamus, parabrachial nucleus and raphe nuclei. 37 Further studies are needed to clarify the roles of these regions in activation of oxytocin neurones in response to stressful stimuli.…”