The Role of Oxytocin Release in the Paraventricular Nucleus in the Control of Maternal Behaviour in the Sheep

Abstract

Oxytocin (OT) release within the brain is thought to play a major role in inducing maternal behaviour in a number of mammalian species but little is known about the sites of release which are important in this respect. We have investigated whether the paraventricular nucleus of the hypothalamus (PVN) is a site of OT action on maternal behaviour in the sheep. In vivo microdialysis and retrodialysis was used to determine whether OT is released in the region of the PVN during the post-partum induction of maternal behaviour and if its release at this site can stimulate maternal behaviour in non-pregnant animals. In vivo sampling showed that OT concentrations increased significantly in the region of PVN at birth. When OT was retrodialysed bilaterally into the PVN (1 or 10 microM) of multiparous ewes treated with progesterone and oestradiol to stimulate lactation, maternal behaviour was induced in a significant number of animals (1 microM, 6/8 and 10 microM, 5/8) compared with controls (0/8 ewes). Similar infusions of the ring structure of OT, tocinoic acid (TOC-10 microM), also induced maternal behaviour in a significant proportion of animals (5/6 ewes) as did intracerebroventricular (ICV) OT (6/8 ewes) and artificial stimulation of the vagina and cervix (VCS, 8/9 ewes). On the other hand, vasopressin (AVP) 1 microM did not induce maternal behaviour in any ewes and a 10 microM dose only induced it in 2/8 animals. The neurochemical changes accompanying the above treatments were also investigated. Noradrenaline concentrations increased in the PVN after the retrodialysis administration of OT 1 microM and 10 microM, TOC 10 microM and AVP 1 microM, OT ICV and VCS. Dopamine concentrations were also increased by OT 10 microM, TOC 10 microM, AVP 1microM and OT ICV. Aspartate and glutamate concentrations were significantly reduced by retrodialysis infusions of OT 1 microM and AVP 1 and 10 microM but not by any other treatment. Finally, the retrodialysis infusion of OT and TOC, as well as ICV OT, significantly increased plasma OT release whereas AVP infusions did not. These results provide evidence that OT is released in the PVN during parturition and is important for the induction of maternal behaviour. It seems probable that OT release at this site has a positive feedback effect on both parvocellular and magnocellular OT neurons to facilitate co-ordinated OT release both in central OT terminal regions (to facilitate maternal behaviour) and peripherally into the blood (to facilitate uterine contractions/milk let down). The potential functional roles for the actions of OT on monoamine and amino acid transmitter release in the PVN are discussed.

Mother–infant bonding and the evolution of mammalian social relationships

“…Because the paraventricular nucleus is the main source of OT release into the brain, upgrading autoreceptors on OT-containing neurons serves to promote further OT release throughout the brain. Certainly, during parturition, levels of OT in cerebrospinal fluid (CSF) increase to 400 pg ml K1 and reach all areas of the brain including the OB, where receptors are upregulated during pregnancy (da Costa et al 1996). Since there are no OT terminals in the OB, this humoral transport serves an important function in the context of receptor terminal mismatch (Yu et al 1996a,b).…”

Maternal responsiveness and maternal selectivity in domestic sheep and goats: The two facets of maternal attachment

“…Indeed, in vivo microdialysis revealed that OT is released in the PVN at lambing as well as during artificial VCS. Furthermore, retrodialysis infusion of OT stimulates maternal behavior in nonpregnant animals primed with a steroid treatment (Da Costa, Guevara-Guzman, Ohkura, Goode, & Kendrick, 1996). However, OT release also occurs in the BNST, MPOA, and the olfactory bulb during parturition and/or following VCS (Da Costa et al, 1996;Kendrick, Keverne, Hinton, & Goode, 1992a).…”

Molecular approaches to aggregation behavior and social attachment

“…Presumably OT release at some of the other targets of the PVN mediates positive maternal responses, but this remains to be tested. Strikingly, OT infusion into the PVN itself induces full maternal responses in steroid primed ewes (Da Costa et al, 1996). This is thought to be due an autocrine loop of OT-induced OT release at all terminal target sites of the oxytocinergic PVN neurons, because these neu- , and A6) from the brain stem.…”

“…Parturition or vaginocervical stimulation induces release of the neuropeptide OT in several brain areas in both sheep and rats, and this release appears to coordinate the onset of maternal behavior with birth (Kendrick et al, 1986(Kendrick et al, , 1988(Kendrick et al, , 1997Kendrick and Keverne, 1992;Levy et al, 1992;Neumann et al, 1993;Da Costa et al, 1996). Intracerebroventricular (ICV) infusion of OT in steroid primed nonpregnant animals of both species rapidly induces maternal responses (Pedersen et al, 1982;Kendrick et al, 1987).…”

“…rons express OT receptor mRNA (Da Costa et al, 1996). In the rat, one effect of central OT release is inhibition of olfactory processing in the olfactory bulb (Yu et al, 1996b).…”