Home LiteratureArticle Details
PMID: 8756418 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Changes in the electrical properties of supraoptic nucleus oxytocin and vasopressin neurons during lactation.

Stern JE, Armstrong WE

Abstract

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 Ca(2+)- 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.

MeSH Terms
Action Potentials Animals Electrophysiology Female Immunohistochemistry Lactation/physiology Neurons/physiology Oxytocin/physiology Rats Supraoptic Nucleus/cytology,physiology Vasopressins/physiology
Chemicals
Vasopressins Oxytocin
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Stern J E
Department of Anatomy and Neurobiology, College of Medicine, University of Tennessee, Memphis 38163, USA.
Armstrong W E
References (38)
38 references, click to expand
  1. The role of patterned burst and interburst interval on the excitation-coupling mechanism in the isolated rat neural lobe.
    J Physiol. 1985 Dec;369:45-60 PMID: 4093889
  2. Burst discharge in mammalian neuroendocrine cells involves an intrinsic regenerative mechanism.
    Science. 1983 Sep 9;221(4615):1050-2 PMID: 6879204
  3. Release of oxytocin within the supraoptic nucleus during the milk ejection reflex in rats.
    Exp Brain Res. 1989;76(3):593-602 PMID: 2792248
  4. A biotin-containing compound N-(2-aminoethyl)biotinamide for intracellular labeling and neuronal tracing studies: comparison with biocytin.
    J Neurosci Methods. 1991 Apr;37(2):141-50 PMID: 1715497
  5. GABA-induced facilitation of the periodic bursting activity of oxytocin neurones in suckled rats.
    J Physiol. 1995 Oct 1;488 ( Pt 1):103-14 PMID: 8568646
  6. Action potentials and release of neurohypophysial hormones in vitro.
    J Physiol. 1971 Jul;215(3):805-17 PMID: 4326309
  7. Emerging concepts of structure-function dynamics in adult brain: the hypothalamo-neurohypophysial system.
    Prog Neurobiol. 1990;34(6):437-504 PMID: 2202017
  8. Transient calcium-dependent potassium current in magnocellular neurosecretory cells of the rat supraoptic nucleus.
    J Physiol. 1988 Mar;397:331-47 PMID: 2457699
  9. Transient outward current in adult rat supraoptic neurones with slice patch-clamp technique: inhibition by angiotensin II.
    J Physiol. 1995 May 15;485 ( Pt 1):87-96 PMID: 7658385
  10. Central inhibitory effects of muscimol and bicuculline on the milk ejection reflex in the anaesthetized rat.
    J Physiol. 1995 Feb 15;483 ( Pt 1):211-24 PMID: 7776233
  11. Osmoregulation of the magnocellular system during pregnancy and lactation.
    Am J Physiol. 1993 Mar;264(3 Pt 2):R555-60 PMID: 8457007
  12. Somatic currents contribute to frequency-dependent spike-broadening in supraoptic neuroendocrine cells.
    Neurosci Lett. 1993 Oct 29;161(2):169-73 PMID: 8272261
  13. Characterization of the responses of oxytocin- and vasopressin-secreting neurones in the supraoptic nucleus to osmotic stimulation.
    J Physiol. 1977 Sep;271(1):253-71 PMID: 562405
  14. Comparison of firing patterns in oxytocin- and vasopressin-releasing neurones during progressive dehydration.
    Brain Res. 1978 Jun 16;148(2):425-40 PMID: 656941
  15. Calcium-dependent action potentials in rat supraoptic neurosecretory neurones recorded in vitro.
    J Physiol. 1985 Jun;363:419-28 PMID: 3926994
  16. Dye coupling among immunocytochemically identified neurons in the supraoptic nucleus: increased incidence in lactating rats.
    Neuroscience. 1987 Jun;21(3):923-30 PMID: 2819770
  17. Ionic basis for the intrinsic activation of rat supraoptic neurones by hyperosmotic stimuli.
    J Physiol. 1989 Oct;417:263-77 PMID: 2621593
  18. Apamin and d-tubocurarine block the afterhyperpolarization of rat supraoptic neurosecretory neurons.
    Neurosci Lett. 1987 Nov 23;82(2):185-90 PMID: 3696492
  19. Characterization of three types of potassium current in cultured neurones of rat supraoptic nucleus area.
    J Physiol. 1989 Mar;410:443-62 PMID: 2552082
  20. Phasic firing enhances vasopressin release from the rat neurohypophysis.
    J Physiol. 1979 May;290(2):433-40 PMID: 469785
  21. Synaptic plasticity in the rat supraoptic nucleus during lactation involves GABA innervation and oxytocin neurons: a quantitative immunocytochemical analysis.
    J Neurosci. 1994 May;14(5 Pt 1):2861-9 PMID: 8182444
  22. Electrophysiological characteristics of immunochemically identified rat oxytocin and vasopressin neurones in vitro.
    J Physiol. 1994 Feb 15;475(1):115-28 PMID: 8189384
  23. Electrophysiological differences between oxytocin and vasopressin neurones recorded from female rats in vitro.
    J Physiol. 1995 Nov 1;488 ( Pt 3):701-8 PMID: 8576859
  24. Tuberal supraoptic neurons--I. Morphological and electrophysiological characteristics observed with intracellular recording and biocytin filling in vitro.
    Neuroscience. 1990;38(2):469-83 PMID: 2124666
  25. Intrinsic inhibition in magnocellular neuroendocrine cells of rat hypothalamus.
    J Physiol. 1984 Aug;353:171-85 PMID: 6090639
  26. Analysis of intracellularly recorded phasic bursting by mammalian neuroendocrine cells.
    J Neurophysiol. 1984 Mar;51(3):552-66 PMID: 6321696
  27. Spike broadening in magnocellular neuroendocrine cells of rat hypothalamic slices.
    Brain Res. 1985 May 13;334(1):176-9 PMID: 3995311
  28. The milk-ejection reflex of the rat: a 20- to 40-fold acceleration in the firing of paraventricular neurones during oxytocin release.
    J Endocrinol. 1973 Jun;57(3):477-93 PMID: 4577217
  29. Diffusion characteristics and extracellular volume fraction during normoxia and hypoxia in slices of rat neostriatum.
    J Neurophysiol. 1991 Feb;65(2):264-72 PMID: 2016641
  30. Calcium-dependent potassium conductance in rat supraoptic nucleus neurosecretory neurons.
    J Neurophysiol. 1985 Dec;54(6):1375-82 PMID: 4087038
  31. Intracellular studies in the facial nucleus illustrating a simple new method for obtaining viable motoneurons in adult rat brain slices.
    Synapse. 1989;3(4):331-8 PMID: 2740992
  32. Activity dependence of action potential duration in rat supraoptic neurosecretory neurones recorded in vitro.
    J Physiol. 1985 Jun;363:429-39 PMID: 3926995
  33. Reduced oxytocin response to osmotic stimulus and immobilization stress in lactating rats.
    J Endocrinol. 1988 Feb;116(2):225-30 PMID: 3351419
  34. Potassium currents responsible for inward and outward rectification in rat neostriatal spiny projection neurons.
    J Neurosci. 1995 Jun;15(6):4449-63 PMID: 7790919
  35. 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.
    Neuroscience. 1993 Dec;57(4):1027-38 PMID: 8309542
  36. Electrophysiological differentiation of oxytocin- and vasopressin-secreting neurones.
    Proc R Soc Lond B Biol Sci. 1977 Apr;196(1125):367-84 PMID: 17859
  37. Prevention of Ca(2+)-mediated action potentials in GABAergic local circuit neurones of rat thalamus by a transient K+ current.
    J Physiol. 1994 Aug 1;478 Pt 3:403-22 PMID: 7965855
  38. M-currents and other potassium currents in bullfrog sympathetic neurones.
    J Physiol. 1982 Sep;330:537-72 PMID: 6294290
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
0270-6474
Published
1996-08-15
Pages
4861-71
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6579285
Subset
IM
Grants
NINDS NIH HHS · R01 NS023941 · United States
NINDS NIH HHS · R56 NS023941 · United States
NIADDK NIH HHS · AM16166 · United States
NINDS NIH HHS · NS23941 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com