Phasic spike patterning in rat supraoptic neurones in vivo and in vitro

In vivo, most vasopressin cells of the hypothalamic supraoptic nucleus fire action potentials in a ‘phasic’ pattern when the systemic osmotic pressure is elevated, while most oxytocin cells fire continuously. The phasic firing pattern is believed to arise as a consequence of intrinsic activity‐dependent changes in membrane potential, and these have been extensively studied in vitro. Here we analysed the discharge patterning of supraoptic nucleus neurones in vivo, to infer the characteristics of the post‐spike sequence of hyperpolarization and depolarization from the observed spike patterning. We then compared patterning in phasic cells in vivo and in vitro, and we found systematic differences in the interspike interval distributions, and in other statistical parameters that characterized activity patterns within bursts. Analysis of hazard functions (probability of spike initiation as a function of time since the preceding spike) revealed that phasic firing in vitro appears consistent with a regenerative process arising from a relatively slow, late depolarizing afterpotential that approaches or exceeds spike threshold. By contrast, in vivo activity appears to be dominated by stochastic rather than deterministic mechanisms, and appears consistent with a relatively early and fast depolarizing afterpotential that modulates the probability that random synaptic input exceeds spike threshold. Despite superficial similarities in the phasic firing patterns observed in vivo and in vitro, there are thus fundamental differences in the underlying mechanisms.

[1]  B. Smith,et al.  Electrophysiological characteristics of immunochemically identified rat oxytocin and vasopressin neurones in vitro. , 1994, The Journal of physiology.

[2]  D. Pfaff,et al.  Immunohistochemical analysis of magnocellular elements in rat hypothalamus: Distribution and numbers of cells containing neurophysin, oxytocin, and vasopressin , 1981, The Journal of comparative neurology.

[3]  G Leng,et al.  κ-Opioid Regulation of Neuronal Activity in the Rat Supraoptic Nucleus In Vivo , 1998, The Journal of Neuroscience.

[4]  Peter Roper,et al.  Burst Initiation and Termination in Phasic Vasopressin Cells of the Rat Supraoptic Nucleus: A Combined Mathematical, Electrical, and Calcium Fluorescence Study , 2004, The Journal of Neuroscience.

[5]  Gary S Bhumbra,et al.  Measuring spike coding in the rat supraoptic nucleus , 2004, The Journal of physiology.

[6]  F. Dudek,et al.  In vivo Intracellular Recording of Neurons in the Supraoptic Nucleus of the Rat Hypothalamus , 1991, Journal of neuroendocrinology.

[7]  W. Armstrong Morphological and electrophysiological classification of hypothalamic supraoptic neurons , 1995, Progress in Neurobiology.

[8]  D. Poulain,et al.  Comparison of firing patterns in oxytocin- and vasopressin-releasing neurones during progressive dehydration , 1978, Brain Research.

[9]  R. Dyball,et al.  Identification of oxytoxin cells in the rat supraoptic nucleus by their response to cholecystokinin injection , 1991, Neuroscience Letters.

[10]  L. Renaud,et al.  Membrane properties of rat magnocellular neuroendocrine cells in vivo , 1991, Brain Research.

[11]  W. Mason,et al.  Complex action potential waveform recorded from supraoptic and paraventricular neurones of the rat: Evidence for sodium and calcium spike components at different membrane sites , 2004, Experimental Brain Research.

[12]  C. Bourque,et al.  Autocrine feedback inhibition of plateau potentials terminates phasic bursts in magnocellular neurosecretory cells of the rat supraoptic nucleus , 2004, The Journal of physiology.

[13]  W. Armstrong,et al.  Changes in the Active Membrane Properties of Rat Supraoptic Neurones During Pregnancy and Lactation , 2002, Journal of neuroendocrinology.

[14]  G. Leng,et al.  Autoinhibition of Supraoptic Nucleus Vasopressin Neurons In Vivo: A Combined Retrodialysis/Electrophysiological Study in Rats , 1997, The European journal of neuroscience.

[15]  G. I. Hatton Phasic bursting activity of rat paraventricular neurones in the absence of synaptic transmission , 1982, The Journal of physiology.

[16]  R. Dyball,et al.  Characterization of the responses of oxytocin‐ and vasopressin‐secreting neurones in the supraoptic nucleus to osmotic stimulation , 1977, The Journal of physiology.

[17]  G. Leng,et al.  Uterine Contractile Activity Stimulates Supraoptic Neurons in Term Pregnant Rats Via a Noradrenergic Pathway**This work was supported by The Wellcome Trust (Project Grant 047318/Z/96/Z) and the Biotechnology and Biological Sciences Research Council. , 2001, Endocrinology.

[18]  G. Leng,et al.  Opioid modulation of magnocellular neurosecretory cell activity , 2000, Neuroscience Research.

[19]  F. Dudek,et al.  Burst discharge in mammalian neuroendocrine cells involves an intrinsic regenerative mechanism. , 1983, Science.

[20]  W. Mason Excitation by dopamine of putative oxytocinergic neurones in the rat supraoptic nucleus in vitro: Evidence for two classes of continuously firing neurones , 1983, Brain Research.

[21]  Koji Hara,et al.  Anesthetic Pharmacology International Society for Anaesthetic Pharmacology the Anesthetic Mechanism of Urethane: the Effects on Neurotransmitter-gated Ion Channels , 2022 .

[22]  F. Dudek,et al.  Analysis of intracellularly recorded phasic bursting by mammalian neuroendocrine cells. , 1984, Journal of neurophysiology.

[23]  P. Sawchenko,et al.  Reflex control of magnocellular vasopressin and oxytocin secretion , 1991, Trends in Neurosciences.

[24]  Michael Rudolph,et al.  The high-conductance state of neocortical neurons in vivo , 2003, Nature Reviews Neuroscience.

[25]  L. Renaud,et al.  Regulation of spontaneous phasic firing of rat supraoptic vasopressin neurones in vivo by glutamate receptors. , 1995, The Journal of physiology.

[26]  C. Bourque,et al.  Phasic bursts in rat magnocellular neurosecretory cells are not intrinsically regenerative in vivo , 2004, The European journal of neuroscience.

[27]  Jianfeng Feng,et al.  Responses of Magnocellular Neurons to Osmotic Stimulation Involves Coactivation of Excitatory and Inhibitory Input: An Experimental and Theoretical Analysis , 2001, The Journal of Neuroscience.

[28]  M. Brimble,et al.  Phasic discharge in supraoptic neurones recorded from hypothalamic slices , 1978, Experimental Brain Research.

[29]  L. Renaud,et al.  Calcium-dependent potassium conductance in rat supraoptic nucleus neurosecretory neurons. , 1985, Journal of neurophysiology.

[30]  G Leng,et al.  Induction of c-fos expression in hypothalamic magnocellular neurons requires synaptic activation and not simply increased spike activity , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  L. Renaud,et al.  Neurophysiology and neuropharmacology of hypothalamic magnocellular neurons secreting vasopressin and oxytocin , 1991, Progress in Neurobiology.

[32]  G. I. Hatton,et al.  Ca2+ release from internal stores: role in generating depolarizing after‐potentials in rat supraoptic neurones. , 1997, The Journal of physiology.

[33]  E. W. Haller,et al.  Electrophysiological studies of paraventricular and supraoptic neurones recorded in vitro from slices of rat hypothalamus. , 1980, The Journal of physiology.

[34]  L. Renaud,et al.  Electrophysiology of mammalian magnocellular vasopressin and oxytocin neurosecretory neurons , 1990 .

[35]  G. I. Hatton Emerging concepts of structure-function dynamics in adult brain: The hypothalamo-neurohypophysial system , 1990, Progress in Neurobiology.

[36]  M. Kawata,et al.  Phasically firing neurons in the supraoptic nucleus of the rat hypothalamus: Immunocytochemical and electrophysiological studies , 1983, Neuroscience Letters.

[37]  A. Summerlee,et al.  Extracellular recordings from oxytocin neurones during the expulsive phase of birth in unanaesthetized rats. , 1981, The Journal of physiology.

[38]  W. Mason Electrical properties of neurons recorded from the rat supraoptic nucleus in vitro , 1983, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[39]  H. Kannan,et al.  Inward sodium current involvement in regenerative bursting activity of rat magnocellular supraoptic neurones in vitro. , 1993, The Journal of physiology.

[40]  E. Stricker,et al.  Oxytocin and vasopressin secretion in response to stimuli producing learned taste aversions in rats. , 1986, Behavioral neuroscience.

[41]  Peter Roper,et al.  AHP's, HAP's and DAP's: How Potassium Currents Regulate the Excitability of Rat Supraoptic Neurones , 2003, Journal of Computational Neuroscience.

[42]  A. Douglas,et al.  Nitric Oxide and the Oxytocin System in Pregnancy , 2000, The Journal of Neuroscience.

[43]  E. Stricker,et al.  Oxytocin secretion in response to cholecystokinin and food: differentiation of nausea from satiety. , 1986, Science.

[44]  G. I. Hatton,et al.  Calbindin‐D28k: role in determining intrinsically generated firing patterns in rat supraoptic neurones. , 1995, The Journal of physiology.

[45]  Y. Ueta,et al.  Intracellular EGTA alters phasic firing of neurons in the rat supraoptic nucleus in vitro , 1992, Neuroscience Letters.

[46]  E. Stricker,et al.  Cholecystokinin and gastric distension activate oxytocinergic cells in rat hypothalamus. , 1987, The American journal of physiology.

[47]  Gareth Leng,et al.  Physiological pathways regulating the activity of magnocellular neurosecretory cells , 1999, Progress in Neurobiology.

[48]  G. Leng,et al.  Temporal dissociation of the feedback effects of dendritically co-released peptides on rhythmogenesis in vasopressin cells , 2004, Neuroscience.

[49]  F. Dudek,et al.  Synaptic activation of slow depolarization in rat supraoptic nucleus neurones in vitro. , 1987, The Journal of physiology.