Oxytocin and vasopressin release in the olfactory bulb of parturient ewes: changes with maternal experience and effects on acetylcholine, gamma-aminobutyric acid, glutamate and noradrenaline release.
Maternal behaviour and the ewe's ability to recognize her lamb depend on olfactory cues and parturition, and are facilitated by maternal experience. Parturition induces a variety of neurochemical changes in the brain and, in particular, oxytocin (OT) release. This peptide injected centrally induces maternal behaviour. Oxytocin release occurs in the olfactory bulb (OB) at parturition and yet this structure is involved in the process of selective bonding with lamb. The present study therefore investigated the possibility that oxytocin release in the OB might modulate the release of classical transmitters that are known to be important in controlling selective recognition and whether maternal experience has any effect on this. We have first used in vivo microdialysis to measure OT release, as well as that of the related peptide, arginine-vasopressin (AVP), in the OB of maternally experienced and inexperienced ewes during parturition. While OT release significantly increased in both primiparous and multiparous ewes at parturition this increase was significantly greater in multiparous ewes. No significant change of AVP release was observed in either group. However, vagino-cervical stimulation (VCS) performed at 6 h post-partum caused similar increases in OT but not AVP release in both primiparous and multiparous ewes suggesting that the first birth experience potentiates the ability of VCS to evoke OT release within 6 h of parturition. Using retrodialysis, either OT (10 microM) or AVP (10 microM) were infused into the OB of multiparous and nulliparous ewes and their effects on modulating acetylcholine (ACh), noradrenaline (NA), glutamate and gamma-aminobutyric acid (GABA) release were monitored. Both peptides produced an increase of ACh and NA in multiparous animals and this effect was either absent or less pronounced in nulliparous animals. OT, but not AVP, also increased GABA release equivalently in nulliparous and multiparous animals. Glutamate release was not altered in response to OT or AVP infusion. These results suggest that OT release in the OB at parturition may facilitate the recognition of lamb odours by modulating NA, ACh and GABA release which are of primary importance for olfactory memory. The reduced release of OT in the OB of primiparous ewes at parturition, together with its reduced ability to modulate NA and ACh release, might also partly explain why maternally inexperienced animals require a longer period to selectively bond with their lambs.
Lévy
F
F
BBSRC Babraham Institute, Cambridge, UK.
Kendrick
K M
KM
Goode
J A
JA
Guevara-Guzman
R
R
Keverne
E B
EB
D000109:Acetylcholine / Q000378:metabolism; D000818:Animals; D001127:Arginine Vasopressin / Q000502:physiology*; D005260:Female; D018698:Glutamic Acid / Q000378:metabolism; D008425:Maternal Behavior / Q000502:physiology*; D009638:Norepinephrine / Q000378:metabolism; D009830:Olfactory Bulb / Q000502:physiology*; D010121:Oxytocin / Q000502:physiology*; D011247:Pregnancy; D011270:Pregnancy, Animal / Q000502:physiology*; D012756:Sheep; D005680:gamma-Aminobutyric Acid / Q000378:metabolism
D001127:Arginine Vasopressin; D018698:Glutamic Acid; D010121:Oxytocin; D005680:gamma-Aminobutyric Acid; D000109:Acetylcholine; D009638:Norepinephrine