Analysis of bursting responses of oxytocin neurones in the rat in late pregnancy, lactation and after weaning.

Abstract

1. Electrophysiological recordings were undertaken to compare bursting characteristics of oxytocin (OT) neurones at four reproductive stages: day 20 pregnancy, day 22 of pregnancy (expected day of parturition), day 7‐11 of lactation, and day 5‐6 after weaning. 2. Each OT neurone was recorded for 1 h of suckling, combined with cervico‐vaginal probing at 5 min intervals as an additional stimulus for bursting. Intracerebroventricular (I.C.V.) oxytocin (2.2 ng) was given after 30 min to facilitate bursting responses. Bursts observed during suckling were classified as ‘spontaneous’ or ‘probe‐evoked’. 3. The percentage of cells displaying spontaneous and/or probe‐evoked bursts during the recording was low in day 20 pregnant animals, high in lactators and intermediate in day 20 pregnant and weaner groups. These differences may relate to variation in the proportion of animals with a responsive milk‐ejection reflex, as well as the relative size of the population of bursting OT neurones. 4. In the period before I.C.V. OT, overall burst frequency (including both spontaneous and probe‐evoked bursts) was similar across groups. After I.C.V. OT, overall burst frequency was much higher in lactators compared with other groups. Similar results were obtained when spontaneous bursts were analysed separately. 5. Burst amplitude (action potentials per burst, including both spontaneous and probe‐evoked bursts) prior to I.C.V. OT was similar between the day 20 pregnant, day 22 pregnant and lactating groups, but was lower in weaners. All groups showed an increase in burst amplitude after I.C.V. OT, but values in weaners remained lower than in other groups. In a separate analysis of spontaneous bursts, burst amplitude after I.C.V. OT was higher in lactators, and lower in weaners, than in pregnant animals. 6. Background firing rates of OT cells were higher in the day 20 and day 22 pregnant groups compared with lactators, and lower in weaners. Only OT cells in lactators showed a significant increase in background firing rates following I.C.V. OT. 7. It is concluded that the bursting characteristics of OT cells change markedly between late pregnancy, mid‐lactation and weaning. The factors underlying these changes, which are only loosely correlated with the sequence of morphological adaptations in OT cells surrounding lactation, remain to be established.

Differential sensitivity of intranuclear and systemic oxytocin release to central noradrenergic receptor stimulation during mid- and late gestation in rats

“…Because the NE system is involved in OT release during parturition and lactation (2,3,9,12,16,25,29,38), it is likely that increased sensitivity of the OT system to noradrenergic receptor stimulation during LATEP will have important implications for peri-and postpartum events. Although it is not certain what causes the increased sensitivity, this may be related to alterations in electrophysiological (18,35) and/or morphological (37) characteristics of OT magnocellular neurons present during LATEP.…”

“…Another potential explanation is that the progressive increase in systemic OT concentration, without a concomitant change in intranuclear OT release, results from the fall in opioid inhibition of OT nerve terminals in the neural lobe occurring between mid-and late gestation (11). Finally, it is possible that the gains relating stimulation of central noradrenergic and/or OT receptors and systemic OT secretion are increased in LATEP by some other mechanism, such as anatomic (37) or electrophysiological (18,35) adaptations known to be present in late gestation. However, the precise mechanism(s) mediating the dissociation between central and systemic OT during LATEP remains to be investigated.…”

“…A number of changes in the OT system have been documented during late gestation: central OT mRNA is increased (7,26,33,39,41), morphological rearrangements of magnocellular nuclei facilitate increased connectivity of soma and dendrites in OT neurons (37), and electrophysiological changes in OT neuronal firing patterns (18) and in active membrane properties (35) are associated with increases in spontaneous bursting. As a likely consequence of these changes, OT concentrations in the neural lobe (13,22) and systemic OT release (22) are increased during late gestation, consistent with the increased sensitivity to excitatory stimuli and neurotransmission.…”

Plasticity in GABAAReceptor Subunit mRNA Expression by Hypothalamic Magnocellular Neurons in the Adult Rat

“…Although similar studies have not, as yet, been undertaken in pregnant or parturient animals, it is highly likely that a powerful GABAergic influence also exists on magnocellular oxytocin neurons at this time. On the day of parturition, oxytocin neurons exhibit an increase in basal firing rate, which is followed later by the onset of intermittent, synchronized bursts of electrical activity leading to birth of the pups (Summerlee, 1981;Jiang and Wakerley, 1995). The mechanisms involved in changing the electrical and biosynthetic activity of magnocellular oxytocin neurons over this period remain unclear.…”

Model Roles of the Hypothalamo-Neurohypophysial System in Neuroscience Study

“…2) Immaturity of the OXT-secreting system for lactation. Around the term, the SON experiences a significant morphological and functional remodeling [25,26] that facilitates milk-ejection reflex [147]. However, maternal separation days after the parturition can reverse the facilitatory morphologic changes in the hypothalamus [148] and results in reduction of the secretion of prolactin [149] and OXT [150] along with increased corticosteroid levels [151].…”