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Journal of Neuroscience, Vol 15, 5049-5057, Copyright © 1995 by Society for Neuroscience
Central endogenous opioid inhibition of supraoptic oxytocin neurons in pregnant rats
AJ Douglas, I Neumann, HK Meeren, G Leng, LE Johnstone, G Munro and JA Russell
Department of Physiology, University Medical School, Edinburgh, United Kingdom.
Naloxone increases oxytocin secretion in pregnant rats, suggesting
restraint by endogenous opioids but we have previously reported that
oxytocin nerve terminals in the neural lobe become desensitized to opioid
actions in late pregnancy. Therefore, we sought evidence for opioid
inhibition on oxytocin cell bodies and their inputs at this time. In
conscious 21 d pregnant rats naloxone increased the number of neurons
expressing Fos (an indicator of neuronal activity) in the supraoptic
nucleus (SON) but had no effect on 16 d pregnant or virgin rats. Release of
oxytocin within the SON, measured by microdialysis in conscious rats, was
also increased by naloxone in late pregnancy but not before.
Nor-binaltorphimine, a specific kappa- opioid antagonist, did not increase
Fos or affect oxytocin release within the SON in any group. In anesthetized
rats the firing rate of SON neurons was recorded and oxytocin neurons
identified by an excitatory response to intravenous cholecystokinin.
Naloxone potentiated the cholecystokinin- induced firing rate response on
day 21 of pregnancy but not in 16 d pregnant or virgin rats. Blood sampling
in anesthetized rats showed that naloxone also increased the oxytocin
secretory response to cholecystokinin in late pregnant rats. We conclude
that in late pregnancy, after day 16, endogenous opioids inhibit oxytocin
neurons either directly, on their cell bodies, or presynaptically on
inputs. These endogenous opioids do not act through kappa- opioid receptors
since nor-binaltorphimine was ineffective, but may act via mu-opioid
receptors. Thus, the opioids restrain premature oxytocin secretion until
parturition when there is a high demand for it.
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