Changes in the Electrical Properties of Supraoptic Nucleus Oxytocin and Vasopressin Neurons during Lactation

Magnocellular oxytocin (OT) and vasopressin (VP) neurons adopt different firing patterns in response to relevant physiological stimuli. OT neurons selectively display short (2–4 sec), high-frequency bursts of action potentials that are highly synchronized and correlated with OT release during lactation. The present experiments were done to determine whether the electrophysiological properties of OT neurons differ from those of VP neurons, and whether these properties are modulated during lactation to support short bursting activity. Intracellular recordings in vitro were obtained from immunochemically identified supraoptic neurons of diestrous or lactating female rats. Resting membrane potential, input resistance, membrane time constant, and the depolarizing afterpotential did not differ among groups. However, near spike threshold, OT, but not VP, neurons expressed a sustained outward rectification that was removed by small hyperpolarizing pulses and a rebound depolarization that occurred at the offset of these hyperpolarizing pulses. The rebound depolarization was short (<2 sec), supported brief bursts of action potentials, and was significantly larger during lactation. Neurons expressing the outward rectification also exhibited strong spike frequency adaptation during prolonged (1–4 sec) depolarization. Spike width, the Ca2+-dependent afterhyperpolarization, and the degree of spike broadening of OT, but not VP, neurons were also larger during lactation, suggesting an increase in Ca2+ influx per spike. The results indicate that OT neurons possess properties favoring the expression of short spike trains, and that some of these properties are enhanced during lactation. In addition, spikes in OT neurons may promote more Ca2+ influx in this state.

• Publication year

  1996

• Venue

  Journal of Neuroscience

• Publication date

  1996-08-15

• Fields of study

  Biology, Medicine

• Identifiers
  DOI 10.1523/JNEUROSCI.16-16-04861.1996PMID 8756418PMCID PMC6579285
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

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• Transient outward current in adult rat supraoptic neurones with slice patch‐clamp technique: inhibition by angiotensin II.

  1995cited by this paper
• GABA‐induced facilitation of the periodic bursting activity of oxytocin neurones in suckled rats.

  1995cited by this paper
• Electrophysiological differences between oxytocin and vasopressin neurones recorded from female rats in vitro.

  1995cited by this paper
• Potassium currents responsible for inward and outward rectification in rat neostriatal spiny projection neurons

  1995influential reference
• Central inhibitory effects of muscimol and bicuculline on the milk ejection reflex in the anaesthetized rat.

  1995cited by this paper
• Prevention of Ca(2+)‐mediated action potentials in GABAergic local circuit neurones of rat thalamus by a transient K+ current.

  1994cited by this paper
• Synaptic plasticity in the rat supraoptic nucleus during lactation involves GABA innervation and oxytocin neurons: a quantitative immunocytochemical analysis

  1994cited by this paper
• Electrophysiological characteristics of immunochemically identified rat oxytocin and vasopressin neurones in vitro.

  1994cited by this paper
• Somatic currents contribute to frequency-dependent spike-broadening in supraoptic neuroendocrine cells.

  1993cited by this paper
• Osmoregulation of the magnocellular system during pregnancy and lactation.

  1993cited by this paper
• Action of endogenous oxytocin within the paraventricular or supraoptic nuclei: a powerful link in the regulation of the bursting pattern of oxytocin neurons during the milk-ejection reflex in rats.

  1993cited by this paper
• A biotin-containing compound N-(2-aminoethyl)biotinamide for intracellular labeling and neuronal tracing studies: comparison with biocytin.

  1991cited by this paper
• Diffusion characteristics and extracellular volume fraction during normoxia and hypoxia in slices of rat neostriatum.

  1991cited by this paper
• Tuberal supraoptic neurons--I. Morphological and electrophysiological characteristics observed with intracellular recording and biocytin filling in vitro.

  1990cited by this paper
• Emerging concepts of structure-function dynamics in adult brain: the hypothalamo-neurohypophysial system.

  1990cited by this paper
• Intracellular studies in the facial nucleus illustrating a simple new method for obtaining viable motoneurons in adult rat brain slices

  1989cited by this paper
• Ionic basis for the intrinsic activation of rat supraoptic neurones by hyperosmotic stimuli.

  1989cited by this paper
• Characterization of three types of potassium current in cultured neurones of rat supraoptic nucleus area.

  1989cited by this paper
• Reduced oxytocin response to osmotic stimulus and immobilization stress in lactating rats.

  1988cited by this paper
• Transient calcium‐dependent potassium current in magnocellular neurosecretory cells of the rat supraoptic nucleus.

  1988cited by this paper
• Dye coupling among immunocytochemically identified neurons in the supraoptic nucleus: increased incidence in lactating rats.

  1987cited by this paper
• Apamin and d-tubocurarine block the afterhyperpolarization of rat supraoptic neurosecretory neurons.

  1987cited by this paper
• Spike broadening in magnocellular neuroendocrine cells of rat hypothalamic slices.

  1985cited by this paper
• Calcium‐dependent action potentials in rat supraoptic neurosecretory neurones recorded in vitro.

  1985cited by this paper
• Activity dependence of action potential duration in rat supraoptic neurosecretory neurones recorded in vitro.

  1985cited by this paper
• The role of patterned burst and interburst interval on the excitation‐coupling mechanism in the isolated rat neural lobe.

  1985cited by this paper
• Calcium-dependent potassium conductance in rat supraoptic nucleus neurosecretory neurons.

  1985cited by this paper
• Intrinsic inhibition in magnocellular neuroendocrine cells of rat hypothalamus.

  1984influential reference
• Analysis of intracellularly recorded phasic bursting by mammalian neuroendocrine cells.

  1984influential reference
• Burst discharge in mammalian neuroendocrine cells involves an intrinsic regenerative mechanism.

  1983influential reference
• Phasic pattern of electrical stimulation enhances oxytocin secretion from the isolated neurohypophysis

  1982cited by this paper
• M‐currents and other potassium currents in bullfrog sympathetic neurones

  1982cited by this paper
• Phasic firing enhances vasopressin release from the rat neurohypophysis

  1979cited by this paper
• Comparison of firing patterns in oxytocin- and vasopressin-releasing neurones during progressive dehydration.

  1978cited by this paper
• Electrophysiological differentiation of oxytocin-and vasopressin-secreting neurones

  1977cited by this paper
• Characterization of the responses of oxytocin‐ and vasopressin‐secreting neurones in the supraoptic nucleus to osmotic stimulation

  1977cited by this paper
• Electric current flow in excitable cells

  1975influential reference
• The milk-ejection reflex of the rat: a 20- to 40-fold acceleration in the firing of paraventricular neurones during oxytocin release.

  1973cited by this paper
• Recurrent inhibition of antidromically identified rat supraoptic neurones

  1972cited by this paper
• Action potentials and release of neurohypophysial hormones in vitro

  1971cited by this paper

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  2024cites this paper
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  2020cites this paper
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  2020cites this paper
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  2020cites this paper
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  2019cites this paper
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  2019cites this paper
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  2018cites this paper
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  2018cites this paper
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  2018cites this paper
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  2017cites this paper
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  2017cites this paper
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  2017cites this paper
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  2016cites this paper
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• Oxytocin Neurones: Intrinsic Mechanisms Governing the Regularity of Spiking Activity

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  2008cites this paper
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• Central blockade of oxytocin receptors during mid-late gestation reduces amplitude of slow afterhyperpolarization in supraoptic oxytocin neurons.

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• The neurophysiology of neurosecretory cells

  2007cites this paper
• Somato-dendritic mechanisms underlying the electrophysiological properties of hypothalamic magnocellular neuroendocrine cells: A multicompartmental model study

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  2006cites this paper
• Intranuclear coupling of hypothalamic magnocellular nuclei by glutamate synaptic circuits.

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• Neurohypophyseal Hormones : From Genomics and Physiology to Disease Internuclear coupling of hypothalamic magnocellular nuclei by glutamate synaptic circuits

  2006cites this paper
• CHAPTER 59 – Milk Ejection and Its Control

  2006cites this paper
• Gene array profiling of large hypothalamic CNS regions in lactating and randomly cycling virgin mice.

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• Morphine withdrawal increases intrinsic excitability of oxytocin neurons in morphine‐dependent rats

  2005cites this paper
• Enhancement of calcium‐dependent afterpotentials in oxytocin neurons of the rat supraoptic nucleus during lactation

  2005influential citation
• Neurochemical bases of plasticity in the magnocellular oxytocin system during gestation.

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• Neuroendocrine control of body fluid metabolism.

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• AHP's, HAP's and DAP's: How Potassium Currents Regulate the Excitability of Rat Supraoptic Neurones

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• Postsynaptic GABAB receptors in supraoptic oxytocin and vasopressin neurons.

  2002cites this paper
• Plasticity in the electrophysiological properties of oxytocin neurons

  2002cites this paper
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  2001cites this paper
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  2001cites this paper
• Opioid modulation of magnocellular neurosecretory cell activity.

  2000cites this paper
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  2000cites this paper
• Vasopressin increases GABAergic inhibition of rat hypothalamic paraventricular nucleus neurons in vitro.

  2000cites this paper
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  2000cites this paper
• Enhanced neurotransmitter release at glutamatergic synapses on oxytocin neurones during lactation in the rat

  2000cites this paper
• Changes in properties and neurosteroid regulation of GABAergic synapses in the supraoptic nucleus during the mammalian female reproductive cycle

  1999cites this paper
• Electrophysiological distinctions between oxytocin and vasopressin neurons in the supraoptic nucleus.

  1998cites this paper
• Density of transient K+ current influences excitability in acutely isolated vasopressin and oxytocin neurones of rat hypothalamus

  1998influential citation
• Neurophysiology of magnocellular neuroendocrine cells: recent advances.

  1998cites this paper
• Different effect of oxytocin on membrane potential of supraoptic oxytocin neurons in virgin female and male rats in vitro.

  1998cites this paper
• Phenotypic and state-dependent expression of the electrical and morphological properties of oxytocin and vasopressin neurones.

  1998cites this paper
• Osmoregulation of vasopressin neurons: a synergy of intrinsic and synaptic processes.

  1998cites this paper
• Reorganization of the Dendritic Trees of Oxytocin and Vasopressin Neurons of the Rat Supraoptic Nucleus during Lactation

  1998cites this paper
• Caesium blocks depolarizing after‐potentials and phasic firing in rat supraoptic neurones

  1998cites this paper
• Electrophysiological studies of oxytocin neurons in organotypic slice cultures.

  1998cites this paper
• NMDA Receptor Properties in Rat Supraoptic Magnocellular Neurons: Characterization and Postnatal Development

  1997cites this paper