Elsevier

Neuroscience

Volume 53, Issue 1, March 1993, Pages 77-89
Neuroscience

Oxytocin neuron activation and fos expression: A quantitative immunocytochemical analysis of the effect of lactation, parturition, osmotic and cardiovascular stimulation

https://doi.org/10.1016/0306-4522(93)90286-OGet rights and content

Abstract

As c-fos expression is generally thought to be linked to neuronal activation, we compared Fos immunoreactivity in identified oxytocinergic and vasopressinergic neurons of female rats under various conditions known to elicit particular patterns of electrophysiological and secretory activity in these neurons. In suckled lactating animals, Fos immunoreactivity was visible only in rare oxytocinergic and vasopressinergic neurons of the paraventricular and supraoptic nuclei, even after interruption of suckling for 18–72 h. On the other hand, many Fos-positive cells were visible in the nuclei of parturient rats; they involved about 25% of supraoptic oxytocinergic elements. Even more Fos-positive elements were visible in the nuclei of lactating rats that had also undergone 24 h water deprivation or haemorrhage. This involved about 75% vasopressinergic neurons and 25% oxytocinergic neurons of the supraoptic nucleus. Fos immunoreactivity was particularly conspicuous in oxytocin neurons of the anterior commissural nucleus after haemorrhage. After water deprivation or haemorrhage, Fos-positive oxytocinergic neurons in the supraoptic nucleus were significantly more numerous in virgin rats than in lactating rats.

Our observations show that suckling, although a most potent stimulus for oxytocin neuron activation and oxytocin release, is inefficient in inducing Fos synthesis in magnocellular neurons, even after a period of interruption. On the other hand, parturition, water deprivation and haemorrhage were more potent stimuli for both neurosecretory systems. However, under each type of stimulation, only part of the neuronal populations within each nucleus were Fos-positive, suggesting that different stimulus-specific pathways are involved in these regulations.

In so far as electrical activity is one possible mechanism for c-fos expression, comparison of the patterns of c-fos activation with the known electrophysiological behaviour of hypothalamic magnocellular neurons suggests that Fos synthesis in these neurons is linked to the number of action potentials generated over a period of time, more than to the pattern of electrical activity, whatever the physiological impact of this pattern. Furthermore, within a group of neurons, the heterogeneity of the response in terms of Fos synthesis may be correlated to the variability of the electrophysiological response within this group.

References (37)

  • ArenanderA.T. et al.

    Induction of c-fos and TIS in cultured rat astrocytes by neurotransmitters

    J. Neurosci. Res.

    (1992)
  • Ben-BarakY. et al.

    Neurophysin in the hypothalamoneurohypophysial system: I. Production and characterization of monoclonal antibodies

    J. Neurosci.

    (1985)
  • BourqueC.W. et al.

    Calcium-dependent action potentials in rat supraoptic neurosecretory neurones recordedin vitro

    J. Physiol., Lond.

    (1985)
  • CarterD.A. et al.

    Oxytocin responses to stress in lactating and hyperprolactinaemic rats

    Neuroendocrinology

    (1987)
  • CeccatelliS. et al.

    Expression of c-fos immunoreactivity in transmittercharacterized neurons after stress

  • CurranT.

    The fos oncogene

  • DarlingtonD.N. et al.

    Hypotensive hemorrhage elevates corticotropin-releasing hormone messenger ribonucleic acid (mRNA) but not vasopressin mRNA in the rat hypothalamus

    Endocrinology

    (1992)
  • HamamuraM. et al.

    Electrical activation and c-fos mRNA expression in rat neurosecretory neurones after systemic administration of cholecystokinin

    J. Physiol. Lond.

    (1991)
  • Cited by (123)

    • Intranasal oxytocin reduces attentional bias to food stimuli

      2022, Appetite
      Citation Excerpt :

      Individuals on a vegan diet, with diabetes or food allergies were excluded due to the food provided. Pregnant and breastfeeding women (by self-report) were also excluded from participation due to their altered oxytocin function and sensitivity (e.g. Crowley, Parker, Armstrong, Spinolo, & Grosvenor, 1992; Fenelon, Poulain, & Theodosis, 1993). Altered endogenous oxytocin function is associated with high emotional arousal or stress (e.g. bereavement, financial windfall) so participants reporting such events were also excluded (Engelmann, Ebner, Landgraf, Holsboer, & Wotjak, 1999; Kovacs, 1986, pp. 91–128).

    • Sweet and bitter taste stimuli activate VTA projection neurons in the parabrachial nucleus

      2019, Brain Research
      Citation Excerpt :

      Sucrose tended to activate more VTA-projecting neurons than either quinine or water, although this effectiveness was dependent on which PBN region was examined. Although Fos immunoreactivity is a useful technique for visualization of neuronal activity in a spatially informative manner throughout the brains of animals, it has several aspects that should be considered: The relative strength of a response is not particularly evident in single neurons, physiological activity and Fos expression are not always correlated (Fenelon et al., 1993), and some brain areas show constitutive expression of Fos protein, making discrimination of actual stimulus-evoked activity problematic (e.g. Kovács, 2008). Furthermore, the strength of Fos expression in sensory cortices (including gustatory cortex) depends on the experience of the animal (Bamji-Stocke et al., 2018).

    • Central Nervous System Control of Oxytocin Secretion during Lactation

      2015, Knobil and Neill's Physiology of Reproduction: Two-Volume Set
    View all citing articles on Scopus
    View full text