Electrical Activity of Dorsal Horn Neurons During the Suckling‐Induced Milk Ejection Reflex in the Lactating Rat

Valérie S. Fénelon, Dominique A. Poulain
J Neuroendocrinol. 1992-10-01; 4(5): 575-584
DOI: 10.1111/j.1365-2826.1992.tb00206.x

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Fénelon VS(1), Poulain DA.

Author information:
(1)Laboratoire de Neuroendocrinologie Morphofonctionnelle, INSERM CJF 91.10, Université de Bordeaux II, Bordeaux, France.

In lactating rats, suckling elicits the milk ejection reflex which consists of an
intermittent synchronous activation of hypothalamic oxytocin neurons which
releases oxytocin into the bloodstream. We here investigated the
electrophysiological behaviour of spinal cord neurons linked to mammary
innervation in relation to suckling and the suckling-induced milk ejection
reflex. Experiments were carried out on 58 urethane-anaesthetized rats, paralysed
with gallamine triethiodide and artificially ventilated. Fixation of the spinal
cord and laminectomy significantly slowed down the reflex, which occurred in only
27% of the animals. In these rats, 31 dorsal horn neurons at the thoraco-lumbar
level were found to be excited by nipple stimulation. During suckling by a litter
of at least nine pups, they displayed an irregular pattern of brief bursts of
activity (peak firing rate 22.0 ± 3.2 Hz, mean ± SD) correlated to the bouts of
suckling of the pups. Seventeen out of 19 cells tested by stimulation of at least
2 adjacent nipples received convergent input from different ipsilateral nipples.
Out of 11 cells tested, 8 were also activated by stimulation of a contralateral
nipple. Fourteen out of 30 units were recorded through at least one reflex milk
ejection. Their firing rate was significantly higher than the firing rate of
cells recorded in animals which failed to milk eject (4.4 Hz ± 2.8 versus 1.5 Hz
± 0.7). At the moment of the high frequency discharge of action potentials,
occurring in oxytocinergic cells 10 to 15 s before each milk ejection, spinal
neurons showed no systematic change in electrical activity. In contrast, the
stretch reaction of the pups, which corresponds to an intense period of suckling
when milk ejection has started, induced, in 12 cells, a considerable increase in
electrical activity. One unit was found to be inhibited by suckling and during
the stretch reaction. Ten more units, which were not activated by stimulation of
the nipples but responded to stimulation of excitatory receptive fields near the
last three pairs of nipples, were recorded through reflex milk ejections: 8
remained silent during reflex milk ejections but 2 were activated when the pups
stimulated their excitatory receptive field. We conclude that some dorsal horn
neurons, able to respond readily to the suckling movements of pups, appear to
receive an ungated input from the nipples. At the time of the activation of
oxytocin neurons, they present no particular pattern of activation or inhibition
which could account in a simple manner for the intermittence of the high
frequency discharge in oxytocinergic cells. However, in so far as these dorsal
horn neurons may be part of the milk ejection reflex pathway, their activity,
showing convergence and summation of input, and being facilitated in milk
ejecting animals, indicates that the reflex does undergo a certain degree of
processing at the spinal cord level.

 

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