Synaptic Modulation of Oscillatory Activity of Hypothalamic Neuronal Networks in Vitro

1. Rhythmic bursts of action potentials in neurosecretory cells are a key factor in hypothalamic neurosecretion. Rhythmicity and synchronization may be accomplished by pacemaker cells synaptically driving follower cells or by a network oscillator. 2. In this review we describe a hypothalamic cell culture which may serve as a model for a hypothalamic network oscillator. An overview is given of neurochemical phenotypes, synaptic mechanisms and their development, properties of receptors for fast synaptic transmission, and membrane properties of cells in dissociated rat embryonic hypothalamic culture. 3. Rhythmic activity spreads in the cultured network through synapses that release glutamate, activating a heteromultimeric AMPA-type receptor containing a GluR2 subunit which is associated with a high-conductance channel for Na+ and K+. Rhythmic activity is controlled by synapses that release GABA to activate GABAA receptors. The presumed function of the two receptor types is facilitated by their respective location, GABAA receptors predominating near the soma and AMPA receptors being abundant in dendrites. 4. Network oscillators may be more reliable for the presumed function than single-cell oscillators. They are controlled through synaptic modulation, which may prove to represent a process important for the release of hormones.

[1]  R. Traub,et al.  Model of synchronized epileptiform bursts induced by high potassium in CA3 region of rat hippocampal slice. Role of spontaneous EPSPs in initiation. , 1990, Journal of neurophysiology.

[2]  J. Connor.  Neural pacemakers and rhythmicity. , 1985, Annual review of physiology.

[3]  S J Korn,et al.  Epileptiform burst activity induced by potassium in the hippocampus and its regulation by GABA-mediated inhibition. , 1987, Journal of neurophysiology.

[4]  B. Sakmann,et al.  Flip and flop: a cell-specific functional switch in glutamate-operated channels of the CNS. , 1990, Science.

[5]  R. Axel,et al.  A family of glutamate receptor genes: Evidence for the formation of heteromultimeric receptors with distinct channel properties , 1990, Neuron.

[6]  D. Swandulla,et al.  Molecular properties of the glutamate receptor mediating synaptic excitation in rat hypothalamic neurons , 1993, Neuroscience Letters.

[7]  B. Gähwiler,et al.  Transition from random to phasic firing induced in neurons cultured from the hypothalamic supraoptic area , 1980, Brain Research.

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

[9]  L. Renaud,et al.  Calcium‐dependent action potentials in rat supraoptic neurosecretory neurones recorded in vitro. , 1985, The Journal of physiology.

[10]  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.

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

[12]  D. Theodosis,et al.  Synaptic plasticity in the rat supraoptic nucleus during lactation involves GABA innervation and oxytocin neurons: a quantitative immunocytochemical analysis , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  T. Stone,et al.  An iontophoretic investigation of the actions of convulsant kynurenines and their interaction with the endogenous excitant quinolinic acid , 1982, Brain Research.

[14]  A. N. van den Pol,et al.  Glutamate, the dominant excitatory transmitter in neuroendocrine regulation. , 1990, Science.

[15]  L. Renaud,et al.  Electrophysiology of Central Pathways Controlling Release of Neurohypophysial Hormones , 1993, Annals of the New York Academy of Sciences.

[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]  R. Petralia,et al.  Light and electron immunocytochemical localization of AMPA‐selective glutamate receptors in the rat brain , 1992, The Journal of comparative neurology.

[18]  R. Traub,et al.  Role of EPSPs in initiation of spontaneous synchronized burst firing in rat hippocampal neurons bathed in high potassium. , 1990, Journal of neurophysiology.

[19]  D. Swandulla,et al.  Functional and Molecular Characteristics of the Glutamate Receptor Involved in Synaptic Transmission in the Hypothalamus a , 1994, Annals of the New York Academy of Sciences.

[20]  D. Swandulla,et al.  DEVELOPMENT OF SPONTANEOUS SYNAPTIC ACTIVITY IN A HYPOTHALAMIC NETWORK GROWN IN CULTURE , 1990, Journal of basic and clinical physiology and pharmacology.

[21]  P. Legendre,et al.  Characterization of three types of potassium current in cultured neurones of rat supraoptic nucleus area. , 1989, The Journal of physiology.

[22]  E. Stark,et al.  Effects of gamma-aminobutyric acid (GABA) and GABA antagonist drugs on ACTH release. , 1974, Neuroendocrinology.

[23]  R K Wong,et al.  Synchronized burst discharge in disinhibited hippocampal slice. I. Initiation in CA2-CA3 region. , 1983, Journal of neurophysiology.

[24]  G. Dayanithi,et al.  The role of patterned burst and interburst interval on the excitation‐coupling mechanism in the isolated rat neural lobe. , 1985, The Journal of physiology.

[25]  U. Misgeld,et al.  Effects of antagonists on quisqualate and nicotinic receptor‐mediated currents of midbrain neurones in culture , 1991, British journal of pharmacology.

[26]  D. Swandulla,et al.  Quisqualate receptor-mediated rhythmic bursting of rat hypothalamic neurons in dissociated cell culture , 1989, Neuroscience Letters.

[27]  D. Pow,et al.  New Anatomical Insights into the Inputs and Outputs from Hypothalamic Magnocellular Neurons a , 1993, Annals of the New York Academy of Sciences.

[28]  S. Heinemann,et al.  Molecular cloning and functional expression of glutamate receptor subunit genes. , 1990, Science.

[29]  A. N. van den Pol,et al.  Ionotropic glutamate‐receptor gene expression in hypothalamus: Localization of AMPA, kainate, and NMDA receptor RNA with in situ hybridization , 1994, The Journal of comparative neurology.

[30]  H. Monyer,et al.  Glutamate-operated channels: Developmentally early and mature forms arise by alternative splicing , 1991, Neuron.

[31]  B. Sakmann,et al.  Structural determinants of ion flow through recombinant glutamate receptor channels , 1991, Science.

[32]  A. N. van den Pol,et al.  GABA: A dominant neurotransmitter in the hypothalamus , 1990, The Journal of comparative neurology.

[33]  U. Misgeld,et al.  Reduction of GABAA receptor-mediated inhibition by the non-NMDA receptor antagonist 6-cyano-7-nitroquinoxaline-2,3-dione in cultured neurons of rat brain , 1991, Neuroscience Letters.

[34]  F. Dudek,et al.  The effects of the excitatory amino acid antagonist kynurenic acid on synaptic transmission to supraoptic neuroendocrine cells , 1988, Brain Research.

[35]  D. Swandulla,et al.  Characterization of neurochemical phenotypes in cultured hypothalamic neurons with immunohistochemistry and in situ hybridization , 1993, Brain Research.

[36]  F. Dudek,et al.  Intrinsic and synaptic mechanisms of hypothalamic neurons studied with slice and explant preparations , 1989, Journal of Neuroscience Methods.

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

[38]  D Swandulla,et al.  Ionic currents in cultured rat hypothalamic neurones. , 1992, The Journal of physiology.

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

[40]  D. Swandulla,et al.  Synaptic Synchronized Burst Activity in a Hypothalamic Network , 1991 .

[41]  W. Müller,et al.  Synaptic feedback excitation has hypothalamic neural networks generate quasirhythmic burst activity. , 1995, Journal of neurophysiology.

[42]  D. Swandulla,et al.  Inhibition of high voltage-activated calcium currents by l-glutamate receptor-mediated calcium influx , 1993, Neuron.

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

[44]  L. Renaud,et al.  Characterization of spontaneous and evoked inhibitory postsynaptic potentials in rat supraoptic neurosecretory neurons in vitro. , 1986, Journal of neurophysiology.

[45]  W. Mason,et al.  Whole cell voltage clamp recordings from cultured neurons of the supraoptic area of neonatal rat hypothalamus , 1987, Brain Research.

[46]  B. Gähwiler,et al.  Phasically firing neurons in long-term cultures of the rat hypothalamic supraoptic area: Pacemaker and follower cells , 1979, Brain Research.

[47]  R. Andrew,et al.  Isoperiodic bursting by magnocellular neuroendocrine cells in the rat hypothalamic slice. , 1987, The Journal of physiology.

[48]  F. Dudek,et al.  Intrinsic inhibition in magnocellular neuroendocrine cells of rat hypothalamus. , 1984, The Journal of physiology.

[49]  J. Simpson.  THE RELEASE OF NEURAL TRANSMITTER SUBSTANCES , 1969 .

[50]  M. Bennett,et al.  Differential expression of three glutamate receptor genes in developing rat brain: an in situ hybridization study. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[51]  R. Zucker.  Intrinsic Electrophysiological Regulation of Firing Patterns of Bursting Neurons in Aplysia , 1988 .

[52]  B. Sakmann,et al.  Quantal components of unitary EPSCs at the mossy fibre synapse on CA3 pyramidal cells of rat hippocampus. , 1993, The Journal of physiology.

[53]  I. Cooke,et al.  Regenerative responses of long duration recorded intracellularly from dispersed cell cultures of fetal mouse hypothalamus. , 1982, Journal of neurophysiology.

[54]  B. Katz.  The release of neural transmitter substances , 1969 .

[55]  D. Swandulla,et al.  Development and properties of synaptic mechanisms in a network of rat hypothalamic neurons grown in culture. , 1990, Journal of neurophysiology.

[56]  R. Andrew.  Endogenous bursting by rat supraoptic neuroendocrine cells is calcium dependent. , 1987, The Journal of physiology.

[57]  D. Poulain,et al.  Electrophysiology of hypothalamic magnocellular neurones secreting oxytocin and vasopressin , 1982, Neuroscience.

[58]  C. Bourque.  Calcium-dependent spike after-current induces burst firing in magnocellular neurosecretory cells , 1986, Neuroscience Letters.

[59]  T. Freund,et al.  GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus , 1988, Nature.