Advertisement

Mechanisms of Neuroendocrine Cell Excitability

  • Glenn I. Hatton
  • Zhenhui Li
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 449)

Abstract

Oxytocin (OT) and vasopressin (VP), two neuronally synthesized nonapeptides, are made in the hypothalamic paraventricular and supraoptic nuclei of mammals and released into their blood, eventually to have profound hormonal actions on peripheral tissues. In the rat both OT and VP neurons fire slowly and irregularly under conditions of low demand for peptide release, but natural or artificial depolarizing stimuli result in differential patterns of activity: either regular continuous firing, strongly associated with OT cells, or phasic bursting, characteristic of VP neurons. Recently published findings offer an explanation for the dominant presence of certain Ca2+-dependent membrane potentials that typically lead to phasic firing in VP neurons. Mechanisms of excitability involved in the differential activities of the two cell types, as well as of the same cell type under different physiological conditions, include such factors as Ca2+ binding proteins, voltage-and ligand-gated ion channels, release of Ca2+ from internal stores and gap junctional conductances. The evidence for these factors is reviewed here.

Keywords

Firing Pattern Internal Store Supraoptic Nucleus Magnocellular Neuron Phasic Firing 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Hatton GI 1990 Emerging concepts of structure-function dynamics in adult brain: the hypothalamo-neurohypophysial system. Prog Neurobiol 34:437–504.PubMedCrossRefGoogle Scholar
  2. 2.
    Poulain DA, Wakerley JB 1982 Electrophysiology of hypothalamic neurones secreting oxytocin and vasopressin. Neuroscience 7:773–808.PubMedCrossRefGoogle Scholar
  3. 3.
    Renaud LP, Bourque CW 1991 Neurophysiology and neuropharmacology of hypothalamic magnocellular neurons secreting vasopressin and oxytocin. Prog Neurobiol 36:131–169.PubMedCrossRefGoogle Scholar
  4. 4.
    Li Z, Decavel C, Hatton GI 1995 Calbindin-D28k: Role in determining intrinsically generated firing patterns in rat supraoptic neurones. J Physiol (Lond) 488:601–608.Google Scholar
  5. 5.
    Bourque CW, Oliet SHR, Richard D 1994 Osmoreceptors, osmoreception, and osmoregulation. Front Neuroendocrin 15:231–274.CrossRefGoogle Scholar
  6. 6.
    Bourque CW, Renaud LP 1990 Electrophysiology of mammalian magnocellular vasopressin and oxytocin neurosecretory neurons. Front Neuroendocrin 11:183–212.Google Scholar
  7. 7.
    Legendre P, Poulain DA 1992 Intrinsic mechanisms involved in the electrophysiological properties of the vasopressin-releasing neurons of the hypothalamus. Prog Neurobiol 38:1–17.PubMedCrossRefGoogle Scholar
  8. 8.
    Connor JA, Stevens CF 1971 Inward and delayed outward membrane currents in isolated neural somata under voltage clamp. J Physiol (Lond) 213:1–19.Google Scholar
  9. 9.
    Galvan M, Sedlmeir C 1984 Outward currents in voltage-clamped rat sympathetic neurones. J Physiol (Lond) 356:115–133.Google Scholar
  10. 10.
    Meech RW, Standen NB 1975 Potassium activation in Helix Aspersa neurones under voltage clamp: a component mediated by calcium influx. J Physiol (Lond) 249:211–239.Google Scholar
  11. 11.
    Thompson SH 1977 Three pharmacologically distinct potassium channels in molluscan neurones. J Physiol (Lond) 265:465–488.Google Scholar
  12. 12.
    Cobbett P, Legendre P, Mason WT 1989 Characterization of three types of potassium current in cultured neurones of rat supraoptic nucleus area. J Physiol (Lond) 410:443–462.Google Scholar
  13. 13.
    Li Z, Ferguson AV 1996 Electrophysiological properties of paraventricular magnocellular neurons in rat brain slices: modulation of IA by angiotensin II. Neuroscience 71:133–145.PubMedCrossRefGoogle Scholar
  14. 14.
    Nagatomo T, Inenaga K, Yamashita H 1995 Transient outward current in adult rat supraoptic neurones with slice patch-clamp technique: Inhibition by angiotensin II. J Physiol (Lond) 485:87–96.Google Scholar
  15. 15.
    Erickson KR, Ronnekleiv OK, Kelly MJ 1990 Inward rectification (Ih) in immunocytochemically-identifled vasopressin and oxytocin neurons of guinea-pig supraoptic nucleus. J Neuroendocrinology 2:261–265.CrossRefGoogle Scholar
  16. 16.
    Erickson KR, Ronnekleiv OK, Kelly MJ 1993 Electrophysiology of guinea-pig supraoptic neurones: role of a hyperpolarization-activated cation current in phasic firing. J Physiol (Lond) 460:407–425.Google Scholar
  17. 17.
    Li Z, Hatton GI 1996 Histamine-induced prolonged depolarization in rat supraoptic neurons: G-protein mediated, Ca2+-independent suppression of K+ leakage conductance. Neuroscience 70:145–158.PubMedCrossRefGoogle Scholar
  18. 18.
    Stern JE, Armstrong WE 1995 Electrophysiological differences between oxytocin and vasopressin neurones recorded from female rats in vitro. J Physiol (Lond) 488:701–708.Google Scholar
  19. 19.
    Stern JE, Armstrong WE 1997 Sustained outward rectification of oxytocinergic neurones in the rat supraoptic nucleus: ionic dependence and pharmacology. J Physiol (Lond) 500:497–508.Google Scholar
  20. 20.
    Li Z, Hatton GI 1996 Oscillatory bursting of phasically firing rat supraoptic neurones in low-Ca2+ medium: Na+ influx, cytosolic Ca2+ and junctional conductance. J Physiol (Lond) 496:379–394.Google Scholar
  21. 21.
    Kang J, Sumners C, Posner P 1993 Angiotensin II type 2 receptor-modulated changes in potassium currents in cultured neurons. Am J Physiol 265:C607–C616.PubMedGoogle Scholar
  22. 22.
    Bourque CW 1988 Transient calcium-dependent potassium current in magnocellular neurosecretory cells of the rat supraoptic nucleus. J Physiol (Lond) 397:331–347.Google Scholar
  23. 23.
    Connor JA, Stevens CF 1971 Voltage clamp studies of a transient outward membrane current in gastropod neural somata. J Physiol (Lond) 213:21–30.Google Scholar
  24. 24.
    Sah P, McLachlan EM 1992 Potassium currents contributing to action potential repolarization and the afterhyperpolarization in rat vagal motoneurons. J Neurophysiol 68:1834–1841.PubMedGoogle Scholar
  25. 25.
    Bourque CW 1988 Noradrenaline (NA) inhibits a transient outward current in rat supraoptic (SON) neurons. Soc Neurosci Abstr 14:1089.Google Scholar
  26. 26.
    Armstrong WE, Gallagher MJ, Sladek CD 1986 Noradrenergic stimulation of supraoptic neuronal activity and vasopressin release in vitro: mediation by an a1-receptor. Brain Res 365:192–197.PubMedCrossRefGoogle Scholar
  27. 27.
    Randle JCR, Bourque CW, Renaud LP 1986 a1-Adrenergic receptor activation depolarizes rat supraoptic neurosecretory neurons in vitro. Am J Physiol 251:R569–R574.PubMedGoogle Scholar
  28. 28.
    Okuya S, Inenaga K, Kaneko T, Yamashita H 1987 Angiotensin II sensitive neurons in the supraoptic nucleus, subfornical organ and anteroventral third ventricle of rats in vitro. Brain Res 402:58–67.PubMedCrossRefGoogle Scholar
  29. 29.
    Li Z, Ferguson AV 1993 Subfomical organ efferents to paraventricular nucleus utilize angiotensin as a neurotransmitter. Am J Physiol 265:R302–R309.PubMedGoogle Scholar
  30. 30.
    Li Z, Ferguson AV 1993 Angiotensin II responsiveness of rat paraventricular and subfomical organ neurons in vitro. Neuroscience 55:197–207.PubMedCrossRefGoogle Scholar
  31. 31.
    Kirkpatrick K, Bourque CW 1991 Dual role for calcium in the control of spike duration in rat supraoptic neuroendocrine cells. Neurosci Lett 133:271–274.PubMedCrossRefGoogle Scholar
  32. 32.
    Inenaga K, Akamatsu N, Nagatomo T, Ueta Y, Yamashita H 1992 Intracellular EGTA alters phasic firing of neurons in the rat supraoptic nucleus in vitro. Neurosci Lett 147:189–192.PubMedCrossRefGoogle Scholar
  33. 33.
    Andrew RD, Dudek FE 1984 Intrinsic inhibition in magnocellular neuroendocrine cells of rat hypothalamus. J Physiol (Lond) 353:171–185.Google Scholar
  34. 34.
    Bourque CW, Brown DA 1987 Apamin and d-tubocurarine block the afterhyperpolarization of rat supraoptic neurosecretory neurons. Neurosci Lett 82:185–190.PubMedCrossRefGoogle Scholar
  35. 35.
    Fagan M, Andrew RD 1991 Intracellular study of calcium-related events in cat magnocellular neuroendocrine cells. J Physiol (Lond) 434:337–349.Google Scholar
  36. 36.
    Armstrong WE, Smith BN, Tian M 1994 Electrophysiological characteristics of immunochemically identified rat oxytocin and vasopressin neurones in vitro. J Physiol (Lond) 475:115–128.Google Scholar
  37. 37.
    Sah, P 1996 Ca2+-activated K+currents in neurones: types, physiological roles and modulation. TINS. 19:150–154.PubMedGoogle Scholar
  38. 38.
    Kirkpatrick K, Bourque CW 1995 Effects of neurotensin on rat supraoptic nucleus neurones in vitro. J Physiol (Lond) 482:373–381.Google Scholar
  39. 39.
    Hatton GI, Young WS, Yang QZ, Miyata S, Li Z 1996 Targeted reduction of oxytocin gene expression: electrophysiological and immunocytochemical studies of supraoptic nucleus neurons. Soc Neurosci Abstr 22:629.Google Scholar
  40. 40.
    Tasker JG, Dudek FE 1991 Electrophysiological properties of neurones in the region of the paraventricular nucleus in slices of rat hypothalamus. J Physiol (Lond) 434:271–293.Google Scholar
  41. 41.
    Madison DV, Lancaster B, Nicoll RA 1987 Voltage clamp analysis of cholinergic action in the hippocampus. J Neurosci 7:733–741.PubMedGoogle Scholar
  42. 42.
    Benson DM, Blitzer RD, Landau EM 1988 An analysis of the depolarization produced in guinea-pig hippo-campus by cholinergic receptor stimulation. J Physiol (Lond) 404:479–496.Google Scholar
  43. 43.
    McCormick DA, Williamson A 1991 Modulation of neuronal firing mode in cat and guinea pig LGNd by histamine: possible cellular mechanisms of histaminergic control of arousal. J Neurosci 11:3188–3199.PubMedGoogle Scholar
  44. 44.
    Munakata M, Akaike N 1994 Regulation of K’ conductance by histamine H, and H, receptors in neurones dissociated from rat neostriatum. J Physiol (Lond) 480:233–245.Google Scholar
  45. 45.
    Brown DA, Adams PR 1980 Muscarinic suppression of a novel voltage-sensitive K+ current in a vertebrate neurone. Nature 283:673–676.PubMedCrossRefGoogle Scholar
  46. 46.
    Fisher TE, Bourque CW 1995 Voltage-gated calcium currents in the magnocellular neurosecretory cells of the supraoptic nucleus. J Physiol (Lond) 486:571–580.Google Scholar
  47. 47.
    Foehring RC, Armstrong WE 1996 Pharmacological dissection of high-voltage-activated Ca“ current types in acutely dissociated rat suproptic magnocellular neurons. J Neurophysiol 76:977–983.PubMedGoogle Scholar
  48. 48.
    Li Z, Hatton GI 1997 Ca2+ release from internal stores: Role in generating depolarizing afterpotentials in supraoptic nucleus neurons. J Physiol (Lond) 498:339–350.Google Scholar
  49. 49.
    Erickson KR, Ronnekleiv OK, Kelly MJ 1993 Role of a T-type calcium current in supporting a depolarizing potential, damped oscillations, and phasic firing in vasopressinergic guinea pig supaoptic neurons. Neuroendocrinology 57:789–800.PubMedCrossRefGoogle Scholar
  50. 50.
    Oliet SHR, Bourque CW 1992 Properties of supraoptic magnocellular neurones isolated from the adult rat. J Physiol (Lond) 455:291–306.Google Scholar
  51. 51.
    Fisher TE, Bourque CW 1995 Distinct co-agatoxin-sensitive calcium currents in somata and axon terminals of rat supraoptic neurones. J Physiol (Lond) 489:383–388.Google Scholar
  52. 52.
    Cobbett P, Mason WT 1987 Whole cell voltage clamp recordings from cultured neurons of the supraoptic area of neonatal rat hypothalamus. Brain Res 409:175–180.PubMedCrossRefGoogle Scholar
  53. 53.
    Jahnsen H, Llinas R 1984 Ionic basis for the electroresponsiveness and oscillatory properties of guinea-pig thalamic neurones in vitro. J Physiol (Lond) 349:227–247.Google Scholar
  54. 54.
    Stafstrom CE, Schwindt PC, Chubb MC, Crill WE 1985 Properties of persistent sodium conductance and calcium conductance of layer V neurons from cat sensorimotor cortex in vitro. J Neurosci 53:153–170.Google Scholar
  55. 55.
    Moczydlowski E, Schild L. 1994 Unitary properties of the batrachotoxin-trapped state of voltage-sensitive sodium channels. In: Peracchia C (ed) Handbook of membrane channels: molecular and cellular physiology. Academic Press, Inc., San Diego, pp 137–160.Google Scholar
  56. 56.
    Yang CR, Bourque CW, Renaud LP 1991 Dopamine D, receptor activation depolarizes rat supraoptic neurones in hypothalamic explants. J Physiol (Lond) 443:465–419.Google Scholar
  57. 57.
    Yang CR, Phillips MI, Renaud LP 1992 Angiotensin II receptor activation depolarizes rat supraoptic neurons in vitro. Am J Physiol 263:R1333–R1338.PubMedGoogle Scholar
  58. 58.
    Hiruma H, Bourque CW 1995 P-2 purinoceptor-mediated depolarization of rat supraoptic neurosecretory cells in vitro. J Physiol (Lond) 489:805–811.Google Scholar
  59. 59.
    Chakfe Y, Bourque CW 1996 Angiotensin II (AII), cholecystokinin 1–8 (CCK) and neurotensin 8–13 (NT) modulate cationic conductance in magnocellular neurosecretory cells (MNCs) isolated from supraoptic nucleus of the adult rat. Soc Neurosci Abstr 22:1555.Google Scholar
  60. 60.
    Oliet SHR, Bourque CW 1993 Mechanosensitive channels transduce osmosensitivity in supraoptic neurons. Nature 364:341–343.PubMedCrossRefGoogle Scholar
  61. 61.
    Li Z, Hatton GI 1997 Reduced outward K. conductances generate depolarizing afterpotentials in supraoptic neurons. Soc Neurosci Abstr 23: in press.Google Scholar
  62. 62.
    Andrew RD, Dudek FE 1983 Burst discharge in mammalian neuroendocrine cells involves an intrinsic regenerative mechanism. Science 221:1050–1052.PubMedCrossRefGoogle Scholar
  63. 63.
    Jande SS, Maler L, Lawson DE 1981 Immunohistochemical mapping of vitamin D-dependent calcium-binding protein in brain. Nature 294:765–767.PubMedCrossRefGoogle Scholar
  64. 64.
    Celio MR 1990 Calbindin D28k and parvalbumin in the rat nervous system. Neuroscience 35:375–475.PubMedCrossRefGoogle Scholar
  65. 65.
    Lledo PM, Somasundaram B, Morton AJ, Emson PC, Mason WT 1992 Stable transfection of Calbindin D28k into the GH3 cell line alters Ca2+ current and intracellular Ca2+ homeostasis. Neuron 9:943–954.PubMedCrossRefGoogle Scholar
  66. 66.
    Chard PS, Bleakman D, Christakos S, Fullmer CS, Miller RJ 1993 Calcium buffering properties of calbindin D28k and parvalbumin in rat sensory neurones. J Physiol (Lond) 472:341–357.Google Scholar
  67. 67.
    Lacopino AM, Christakos S 1990 Specific reduction of calcium binding protein (28-kilodalton calbindin-D) gene expression in aging and neurodegenerative diseases. Proc Natl Acad Sci USA 87:4078–4082.CrossRefGoogle Scholar
  68. 68.
    Kohr G, Lambert CE, Mody I 1991 Calbindin-D28K (CaBP) level and calcium currents in acutely dissociated epileptic neurons. Exp Brain Res 85:543–551.PubMedCrossRefGoogle Scholar
  69. 69.
    Sanchez F, Alonso JR, Arevalo R, Carretero J, Vazquez R, Aijon J 1992 Calbindin D28K-and parvalbuminreacting neurons in the hypothalamic magnocellular neurosecretory neuclei of the rat. Brain Res Bull 28:39–46.PubMedCrossRefGoogle Scholar
  70. 70.
    Arai R, Jacobowitz DM, Deura S 1993 Immunohistochemical localization of calretinin-, calbindin-D28kand parvalbumin-containing cells in the hypothalamic paraventricular and supraoptic nuclei of the rat. Brain Res 618:323–327.PubMedCrossRefGoogle Scholar
  71. 71.
    Henzi V, MacDermott AB 1992 Characteristics and function of Ca2+-and inositol I,4,5-trisphosphate-releasable stores of Ca2+ in neurons. Neuroscience 46:251–273.PubMedCrossRefGoogle Scholar
  72. 72.
    Sah P, McLachlan EM 1991 Ca2+-activated K+ currents underlying the afterhyperpolarization in guinea pig vagal neurons: a role for Ca2+-activated Ca2+ release. Neuron 7:257–264.PubMedCrossRefGoogle Scholar
  73. 73.
    Yoshizaki K, Hoshino T, Sato M, Koyano H, Nohmi M, Hua SY, Kuba K 1995 Ca2+-induced Ca2+ release and its activation in response to a single action potential in rabbit otic ganglion cells. J Physiol (Lond) 486:177–187.Google Scholar
  74. 74.
    Zhang L, Valiante TA, Carlen PL 1993 Contribution of the low-threshold T-type calcium current in generating the post-spike depolarizing afterpotential in dentate granule neurons of immature rats. J Neurophysiol 70:223–231.PubMedGoogle Scholar
  75. 75.
    Barish ME, Thompson SH 1983 Calcium buffering and slow recovery kinetics of calcium-dependent outward current in molluscan neurones. J Physiol (Lond) 337:201–219.Google Scholar
  76. 76.
    Andrew RD, MacVicar BA, Dudek FE, Hatton GI 1981 Dye transfer through gap junctions between neuroendocrine cells of rat hypothalamus. Science 211:1187–1189.PubMedCrossRefGoogle Scholar
  77. 77.
    Yang QZ, Hatton GI 1987 Dye coupling among supraoptic nucleus neurons without dendritic damage: differential incidence in nursing mother and virgin rats. Brain Res Bull 19:559–565.PubMedCrossRefGoogle Scholar
  78. 78.
    Yang QZ, Hatton GI 1988 Direct evidence for electrical coupling among rat supraoptic nucleus neurons. Brain Res 463:47–56.PubMedCrossRefGoogle Scholar
  79. 79.
    Miyata S, Hatton GI 1997 Connexin-32 protein in magnocellular neurons of the rat hypothalamus: light and electron microscopic immunohistochemistry. Soc Neurosci Abstr 23: in press.Google Scholar
  80. 80.
    Micevych PE, Popper P Hatton GI 1996 Connexon-32 mRNA levels in the rat supraoptic nucleus: up-regulation prior to parturition and during lactation. Neuroendocrinology 63:39–45PubMedCrossRefGoogle Scholar
  81. 81.
    Hatton GI, Yang QZ 1994 Incidence of neuronal coupling in supraoptic nuclei of virgin and lactating rats: estimation by neurobiotin and Lucifer Yellow. Brain Res 650:63–69.PubMedCrossRefGoogle Scholar
  82. 82.
    Hatton GI, Yang QZ 1996 Synaptically released histamine increases dye coupling among vasopressinergic neurons of the supraoptic nucleus: mediation by H -receptors and cyclic nucleotides. J Neurosci 16:123–129.PubMedGoogle Scholar
  83. 83.
    Hatton GI, Yang QZ 1990 Activation of excitatory amino acid inputs to supraoptic neurons: I. Induced increases in dye coupling in lactating, but not virgin or male rats. Brain Res 513:264–269.PubMedCrossRefGoogle Scholar
  84. 84.
    Kumamoto K, Yang QZ, Hatton GI 1997 Dye coupling among supraoptic nucleus oxytocin neurons in peripartum rats: relation to connexin-32 expression. Soc Neurosci Abstr 22: in press.Google Scholar
  85. 85.
    Perez-Velazquez JL, Valiante TL, Carlen PL 1994 Modulation of gap junctional mechanisms during calcium-free induced field burst activity: a possible role for electrotonic coupling in epileptogenesis. J Neurosci 14:4308–4317.PubMedGoogle Scholar
  86. 86.
    Summerlee AJS, Parry LJ 1988 Stimulus-secretion coupling in the oxytocin system. In: Ganten D, Pfaff D (eds) Stimulus-secretion coupling in neuroendocrine systems. Springer-Verlag, Berlin, pp 29–72.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1998

Authors and Affiliations

  1. 1.Department of NeuroscienceUniversity of CaliforniaRiversideUSA

Personalised recommendations