Performance, properties and plasticity of identified oxytocin and vasopressin neurones in vitro

William Armstrong, L. Wang, C. Li, R. Teruyama

Research output: Contribution to journalReview article

35 Citations (Scopus)

Abstract

The neurohypophysial hormones oxytocin (OT) and vasopressin (VP) originate from hypothalamic neurosecretory cells in the paraventricular and supraoptic (SON) nuclei. The firing rate and pattern of action potentials arising from these neurones determine the timing and quantity of peripheral hormone release. We have used immunochemical identification of biocytin-filled SON neurones in hypothalamic slices in vitro to uncover differences between OT and VP neurones in membrane and synaptic properties, firing patterns, and plasticity during pregnancy and lactation.In this review, we summarise some recent findings from this approach: (i) VP neuronal excitability is influenced by slow (sDAP) and fast (fDAP) depolarising afterpotentials that underlie phasic bursting activity. The fDAP may relate to a transient receptor potential (TRP) channel, type melastatin (TRPM4 and /or TRPM5), both of which are immunochemically localised more to VP neurones, and especially, to their dendrites. Both TRPM4 and TRPM5 mRNAs are found in the SON, but single cell reverse transcriptase-polymerisation suggests that TRPM4 might be the more prominent channel. Phasic bursting in VP neurones is little influenced by spontaneous synaptic activity in slices, being shaped largely by intrinsic currents. (ii) The firing pattern of OT neurones ranges from irregular to continuous, with the coefficient of variation determined by randomly distributed, spontaneous GABAergic, inhibitory synaptic currents (sIPSCs). These sIPSCs are four- to five-fold more frequent in OT versus VP neurones, and much more frequent than spontaneous excitatory synaptic currents. (iii) Both cell types express Ca 2+ -dependent afterhyperpolarisations (AHPs), including an apamin-sensitive, medium duration AHP and a slower, apamin-insensitive AHP (sAHP). In OT neurones, both AHPs are enhanced during pregnancy and lactation. During pregnancy, the plasticity of the sAHP is blocked by antagonism of central OT receptors. AHP enhancement is mimicked by exposing slices from day 19 pregnant rats to OT and oestradiol, suggesting that central OT and sex steroids programme this plasticity during pregnancy by direct hypothalamic actions. In conclusion, the differences in VP and OT neuronal function are underlain by differences in both membrane and synaptic properties, and differentially modulated by reproductive state.

Original languageEnglish (US)
Pages (from-to)330-342
Number of pages13
JournalJournal of Neuroendocrinology
Volume22
Issue number5
DOIs
StatePublished - May 1 2010

Fingerprint

Oxytocin
Vasopressins
Neurons
Apamin
Pregnancy
Synaptic Membranes
Lactation
Posterior Pituitary Hormones
Oxytocin Receptors
Transient Receptor Potential Channels
Supraoptic Nucleus
In Vitro Techniques
RNA-Directed DNA Polymerase
Dendrites
Polymerization
Action Potentials
Estradiol
Steroids
Hormones
Messenger RNA

All Science Journal Classification (ASJC) codes

  • Endocrinology, Diabetes and Metabolism
  • Endocrinology
  • Endocrine and Autonomic Systems
  • Cellular and Molecular Neuroscience

Cite this

Performance, properties and plasticity of identified oxytocin and vasopressin neurones in vitro. / Armstrong, William; Wang, L.; Li, C.; Teruyama, R.

In: Journal of Neuroendocrinology, Vol. 22, No. 5, 01.05.2010, p. 330-342.

Research output: Contribution to journalReview article

@article{a37812592f7043b98f6e1ba854d71017,
title = "Performance, properties and plasticity of identified oxytocin and vasopressin neurones in vitro",
abstract = "The neurohypophysial hormones oxytocin (OT) and vasopressin (VP) originate from hypothalamic neurosecretory cells in the paraventricular and supraoptic (SON) nuclei. The firing rate and pattern of action potentials arising from these neurones determine the timing and quantity of peripheral hormone release. We have used immunochemical identification of biocytin-filled SON neurones in hypothalamic slices in vitro to uncover differences between OT and VP neurones in membrane and synaptic properties, firing patterns, and plasticity during pregnancy and lactation.In this review, we summarise some recent findings from this approach: (i) VP neuronal excitability is influenced by slow (sDAP) and fast (fDAP) depolarising afterpotentials that underlie phasic bursting activity. The fDAP may relate to a transient receptor potential (TRP) channel, type melastatin (TRPM4 and /or TRPM5), both of which are immunochemically localised more to VP neurones, and especially, to their dendrites. Both TRPM4 and TRPM5 mRNAs are found in the SON, but single cell reverse transcriptase-polymerisation suggests that TRPM4 might be the more prominent channel. Phasic bursting in VP neurones is little influenced by spontaneous synaptic activity in slices, being shaped largely by intrinsic currents. (ii) The firing pattern of OT neurones ranges from irregular to continuous, with the coefficient of variation determined by randomly distributed, spontaneous GABAergic, inhibitory synaptic currents (sIPSCs). These sIPSCs are four- to five-fold more frequent in OT versus VP neurones, and much more frequent than spontaneous excitatory synaptic currents. (iii) Both cell types express Ca 2+ -dependent afterhyperpolarisations (AHPs), including an apamin-sensitive, medium duration AHP and a slower, apamin-insensitive AHP (sAHP). In OT neurones, both AHPs are enhanced during pregnancy and lactation. During pregnancy, the plasticity of the sAHP is blocked by antagonism of central OT receptors. AHP enhancement is mimicked by exposing slices from day 19 pregnant rats to OT and oestradiol, suggesting that central OT and sex steroids programme this plasticity during pregnancy by direct hypothalamic actions. In conclusion, the differences in VP and OT neuronal function are underlain by differences in both membrane and synaptic properties, and differentially modulated by reproductive state.",
author = "William Armstrong and L. Wang and C. Li and R. Teruyama",
year = "2010",
month = "5",
day = "1",
doi = "10.1111/j.1365-2826.2010.01989.x",
language = "English (US)",
volume = "22",
pages = "330--342",
journal = "Journal of Neuroendocrinology",
issn = "0953-8194",
publisher = "Wiley-Blackwell",
number = "5",

}

TY - JOUR

T1 - Performance, properties and plasticity of identified oxytocin and vasopressin neurones in vitro

AU - Armstrong, William

AU - Wang, L.

AU - Li, C.

AU - Teruyama, R.

PY - 2010/5/1

Y1 - 2010/5/1

N2 - The neurohypophysial hormones oxytocin (OT) and vasopressin (VP) originate from hypothalamic neurosecretory cells in the paraventricular and supraoptic (SON) nuclei. The firing rate and pattern of action potentials arising from these neurones determine the timing and quantity of peripheral hormone release. We have used immunochemical identification of biocytin-filled SON neurones in hypothalamic slices in vitro to uncover differences between OT and VP neurones in membrane and synaptic properties, firing patterns, and plasticity during pregnancy and lactation.In this review, we summarise some recent findings from this approach: (i) VP neuronal excitability is influenced by slow (sDAP) and fast (fDAP) depolarising afterpotentials that underlie phasic bursting activity. The fDAP may relate to a transient receptor potential (TRP) channel, type melastatin (TRPM4 and /or TRPM5), both of which are immunochemically localised more to VP neurones, and especially, to their dendrites. Both TRPM4 and TRPM5 mRNAs are found in the SON, but single cell reverse transcriptase-polymerisation suggests that TRPM4 might be the more prominent channel. Phasic bursting in VP neurones is little influenced by spontaneous synaptic activity in slices, being shaped largely by intrinsic currents. (ii) The firing pattern of OT neurones ranges from irregular to continuous, with the coefficient of variation determined by randomly distributed, spontaneous GABAergic, inhibitory synaptic currents (sIPSCs). These sIPSCs are four- to five-fold more frequent in OT versus VP neurones, and much more frequent than spontaneous excitatory synaptic currents. (iii) Both cell types express Ca 2+ -dependent afterhyperpolarisations (AHPs), including an apamin-sensitive, medium duration AHP and a slower, apamin-insensitive AHP (sAHP). In OT neurones, both AHPs are enhanced during pregnancy and lactation. During pregnancy, the plasticity of the sAHP is blocked by antagonism of central OT receptors. AHP enhancement is mimicked by exposing slices from day 19 pregnant rats to OT and oestradiol, suggesting that central OT and sex steroids programme this plasticity during pregnancy by direct hypothalamic actions. In conclusion, the differences in VP and OT neuronal function are underlain by differences in both membrane and synaptic properties, and differentially modulated by reproductive state.

AB - The neurohypophysial hormones oxytocin (OT) and vasopressin (VP) originate from hypothalamic neurosecretory cells in the paraventricular and supraoptic (SON) nuclei. The firing rate and pattern of action potentials arising from these neurones determine the timing and quantity of peripheral hormone release. We have used immunochemical identification of biocytin-filled SON neurones in hypothalamic slices in vitro to uncover differences between OT and VP neurones in membrane and synaptic properties, firing patterns, and plasticity during pregnancy and lactation.In this review, we summarise some recent findings from this approach: (i) VP neuronal excitability is influenced by slow (sDAP) and fast (fDAP) depolarising afterpotentials that underlie phasic bursting activity. The fDAP may relate to a transient receptor potential (TRP) channel, type melastatin (TRPM4 and /or TRPM5), both of which are immunochemically localised more to VP neurones, and especially, to their dendrites. Both TRPM4 and TRPM5 mRNAs are found in the SON, but single cell reverse transcriptase-polymerisation suggests that TRPM4 might be the more prominent channel. Phasic bursting in VP neurones is little influenced by spontaneous synaptic activity in slices, being shaped largely by intrinsic currents. (ii) The firing pattern of OT neurones ranges from irregular to continuous, with the coefficient of variation determined by randomly distributed, spontaneous GABAergic, inhibitory synaptic currents (sIPSCs). These sIPSCs are four- to five-fold more frequent in OT versus VP neurones, and much more frequent than spontaneous excitatory synaptic currents. (iii) Both cell types express Ca 2+ -dependent afterhyperpolarisations (AHPs), including an apamin-sensitive, medium duration AHP and a slower, apamin-insensitive AHP (sAHP). In OT neurones, both AHPs are enhanced during pregnancy and lactation. During pregnancy, the plasticity of the sAHP is blocked by antagonism of central OT receptors. AHP enhancement is mimicked by exposing slices from day 19 pregnant rats to OT and oestradiol, suggesting that central OT and sex steroids programme this plasticity during pregnancy by direct hypothalamic actions. In conclusion, the differences in VP and OT neuronal function are underlain by differences in both membrane and synaptic properties, and differentially modulated by reproductive state.

UR - http://www.scopus.com/inward/record.url?scp=77956497400&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=77956497400&partnerID=8YFLogxK

U2 - 10.1111/j.1365-2826.2010.01989.x

DO - 10.1111/j.1365-2826.2010.01989.x

M3 - Review article

VL - 22

SP - 330

EP - 342

JO - Journal of Neuroendocrinology

JF - Journal of Neuroendocrinology

SN - 0953-8194

IS - 5

ER -