Central Oxytocin Stimulates Luteinizing Hormone Release in the Marmoset, a Primate which Fails to Show Lactationally‐lnduced Infertility

Abstract

In several species, including humans, suckling is known to suppress pulsatile gonadotrophin secretion and substantially reduce fertility (1). During suckling high titres of oxytocin are present in both plasma (2, 3) and cerebrospinal fluid (CSF) (4) and there is some evidence that oxytocin is inhibitory to gonadotrophin secretion by an action on t h e central nervous system, (5, 6). The common marmoset, however, has a different physiological response and fails to show lactational infertility; ovarian cyclicity is resumed immediately postpartum (7). W e have therefore examined the effect of centrally administered oxytocin on luteinizing hormone (LH) secretion in this species.W e report that LH release was stimulated with a rapid :esponse and in a dose-dependent manner by oxytocin injected into t h e third cerebral ventricle. In contrast, oxytocin administered intravenously was without effect on LH secretion. These results clearly indicate, for the first time, a stimulatory role for oxytocin in LH secretion in the marmoset, a species which fails to demonstrate lactational infertility.Five sexually mature female marmosets were used. The animals weighed 250 to 410 g and full details of their management have t)een published previously (8). The monkeys were ovariectomized 0 to 56 months before the study, and a cannula was chronically implanted into the third cerebral ventricle at least 6 weeks before ilse. During the experiment the monkeys were placed in a primate Lhair (9) and serial blood samples (0.1 ml) were collected, through 'in indwelling jugular catheter as decribed previously (lo), at 5-to i0-min intervals for 1 h before and 1 h after administration of Oxytocin or vehicle. Three doses of oxytocin (5, 50 and 500 ng) \rere given in 3 pl artificial CSF by intracerebroventricular (icv) ~njection. (Composition of artificial CSF in g/l: NaCl 7.46; KCl @ 1990 Oxford University Press, 0953-8194/90 $3.00 0.19; CaCl 0.14; MgC1,6H20 0.19; NaHCO, 1.76; Na phosphate 0.18; glucose 0.16; pH 7.3). These doses of oxytocin were within the range previously shown by others to facilitate sexual receptivity in the rat (1 1, 12), an animal of comparable body weight. At least 2 weeks lapsed between treatments. In control experiments each monkey received an icv injection of 3 p1 artificial CSF. The effects of iv administration of oxytocin (200 pg in 0.2 ml isotonic saline) were also examined. All treatments were given in a randomized order. Plasma levels of LH were measured using the mouse leydig cell bioassay (1 3). The bioassay system was validated for use with marmoset plasma and the slope obtained for serial dilutions of plasma showed no significant deviation from parallelism with that seen for serial dilutions of macaque LH standard (Lunn SF, unpublished observation). Inter-and intraassay coefficients of variance were 15% and 11%, respectively. Differences in the mean plasma LH concentrations before (mean of samples taken between time 0 and 60min) and after (mean of samples taken between time 65 and 120 min) the treatments wer...

Strongly bonded family members in common marmosets show synchronized fluctuations in oxytocin

“…OT is produced in various peripheral organs as well as in the hypothalamus, from where it is released peripherally and centrally [40,41]. Several studies suggest a direct link [1,11, 42,43] as well as coordination between both systems based on neuroanatomical and physiological evidence [44–46]. This link is probably also triggered indirectly, for example via steroid hormones [47–49] and bidirectional feedback mechanisms with peripheral organs and body states [41], but the topic remains debated [5,50].…”

Oxytocin is associated with infant-care behavior and motivation in cooperatively breeding marmoset monkeys

“…Besides its effects in social bonding and affiliation in mammals (Lim and Young, 2006), peripheral OT is involved in female reproduction (labor and milk letdown: Blanks and Thornton, 2003;Uvnäs-Moberg et al, 2001) and anxiety reduction (Olff et al, 2013). A broadening body of evidence indicates that these central and peripheral OT pathways can be coordinated (Carson et al, 2014;Carter et al, 2007;O'Byrne et al, 1990;Ross and Young, 2009;Wotjak et al, 1998) and may exert crosslinked effects (Ayers et al, 2011;Madden and Clutton-Brock, 2011;Witt et al, 1990). Other studies indicate independent control mechanisms of central and peripheral OT secretion (Amico et al, 1990;Rosenblum et al, 2002;Seckl and Lightman, 1987).…”

Pulsatile gonadotropin-releasing hormone release from hypothalamic explants of male marmoset monkeys compared with male rats

“…Oxytocin is a neurotransmitter that is associated with control of hypothalamic GnRH release in several model systems (6,10,11,27,32,38), including male rats (29,31). In marmosets, oxytocin administered centrally as an intracerabroventricular bolus of 5-500 ng stimulates an increase in plasma LH levels, presumably through an increase in release of hypothalamic GnRH (27). These results are consistent with our direct observation of increased GnRH release from cultured hypothalamic explants in both testis-intact and gonadectomized male marmosets and testis-intact and gonadectomized male rats in response to a 10-min infusion of a 10 nM bolus of oxytocin.…”

“…Such social bonding constraints may have implications for neural oxytocin release in subordinate males that might compromise GnRH release. Because there is indirect evidence that oxytocin stimulates GnRH release in marmosets (27) and rats (38), we challenged both marmoset and rat hypothalamic preparations with a physiological dose of oxytocin to demonstrate its stimulation of GnRH release.…”