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PMID: 2873241 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Actions of noradrenaline recorded intracellularly in rat hippocampal CA1 pyramidal neurones, in vitro.

The Journal of physiology ·Vol. 372 ·1986-03-00 ·Pages 221-44

Madison DV, Nicoll RA

Abstract

CA1 pyramidal neurones were studied in rat in vitro hippocampal slices using standard intracellular and single-electrode voltage-clamp recording techniques to examine the actions of noradrenaline (NA). NA had two different effects on the resting membrane potential of pyramidal neurones; either a hyperpolarization accompanied by a decrease in membrane input resistance, or less commonly, a depolarization accompanied by an increase in input resistance. In many cells, both effects, a hyperpolarization followed by a depolarization were observed. The depolarization was mediated by a noradrenergic beta-receptor. The hyperpolarization was more difficult to characterize, but may result from alpha-receptor activation. NA reduced the amplitude and duration of the slow calcium-activated potassium after-hyperpolarization (a.h.p.) that follows depolarization-induced action potentials. This action of NA was mediated by beta 1-noradrenergic receptors. NA, in the presence of tetrodotoxin and tetraethylammonium, reduced the a.h.p. without reducing the size of the calcium action potential which preceded it. This was unlike the action of the calcium channel blocker, cadmium, which reduced the calcium action potential and the a.h.p. in parallel. Furthermore, NA did not reduce the amplitude of calcium or barium currents recorded under voltage clamp after blockade of potassium currents. A functional consequence of this blockade of the calcium-activated a.h.p. was a reduction of the accommodation of action potential discharge such that the excitatory responses of the neurone to depolarizing stimuli, such as glutamate application or current passed through the recording electrode, were enhanced. We conclude that the effects of NA on calcium-activated potassium conductance and on resting membrane potential can interact to increase the signal-to-noise ratio of hippocampal pyramidal neurone responsiveness.

MeSH Terms
Action Potentials/drug effects Adrenergic Agonists/pharmacology Adrenergic beta-Agonists/pharmacology Adrenergic beta-Antagonists/pharmacology Animals Cadmium/pharmacology Calcium/pharmacology Hippocampus/cytology,physiology In Vitro Techniques Membrane Potentials/drug effects Neurons/drug effects Norepinephrine/pharmacology Potassium/physiology Propranolol/pharmacology Rats Time Factors
Chemicals
Adrenergic Agonists Adrenergic beta-Agonists Adrenergic beta-Antagonists Cadmium Propranolol Potassium Calcium Norepinephrine
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Madison D V
Nicoll R A
References (67)
67 references, click to expand
  1. Norepinephrine elicits both excitatory and inhibitory responses from Purkinje cells in the in vitro rat cerebellar slice.
    Brain Res. 1984 Mar 26;296(1):15-25 PMID: 6713205
  2. Characterization of a slow cholinergic post-synaptic potential recorded in vitro from rat hippocampal pyramidal cells.
    J Physiol. 1984 Jul;352:173-88 PMID: 6747887
  3. Control of the repetitive discharge of rat CA 1 pyramidal neurones in vitro.
    J Physiol. 1984 Sep;354:319-31 PMID: 6434729
  4. Inactivation of Ca conductance dependent on entry of Ca ions in molluscan neurons.
    Proc Natl Acad Sci U S A. 1979 Mar;76(3):1497-500 PMID: 286336
  5. Modulatory actions of norepinephrine in the central nervous system.
    Fed Proc. 1979 Jun;38(7):2109-16 PMID: 446766
  6. alpha 2 and alpha 1-Adrenoceptors mediate opposing actions on parasympathetic neurons.
    Brain Res. 1984 Dec 10;323(2):349-53 PMID: 6098344
  7. Catecholamine inhibition of calcium action potentials in rat locus coeruleus neurones.
    Neuroscience. 1985 Jan;14(1):103-9 PMID: 2579349
  8. Cyclic adenosine 3',5'-monophosphate mediates beta-receptor actions of noradrenaline in rat hippocampal pyramidal cells.
    J Physiol. 1986 Mar;372:245-59 PMID: 2425084
  9. Spontaneous inhibitory post-synaptic potentials in hippocampus: mechanism for tonic inhibition.
    Brain Res. 1980 Oct 27;200(1):195-200 PMID: 7417806
  10. Modulation of lateral geniculate neurone excitability by noradrenaline microiontophoresis or locus coeruleus stimulation.
    Nature. 1980 Oct 23;287(5784):731-4 PMID: 6253811
  11. The adrenergic blocking activity of N-tert.-butylmethoxamine (butoxamine).
    J Pharmacol Exp Ther. 1966 Mar;151(3):413-22 PMID: 4380047
  12. Micro-electrophoretic studies of neurones in the cat hippocampus.
    J Physiol. 1966 Mar;183(2):341-59 PMID: 5942816
  13. Alpha-[(t-Butylamino)methyl]-4-hydroxy-m-xylene-alpha 1,alpha 3-diol (AH.3365): a selective beta-adrenergic stimulant.
    Nature. 1968 Aug 24;219(5156):862-3 PMID: 5673352
  14. Salbutamol: a new, selective beta-adrenoceptive receptor stimulant.
    Br J Pharmacol. 1969 Jan;35(1):141-51 PMID: 5762037
  15. Effects of catecholamines in the cat superior cervical ganglion and their postulated rôle as physiological modulators of ganglionic transmission.
    Prog Brain Res. 1969;31:61-72 PMID: 4310256
  16. Cyclic adenosine monophosphate and norepinephrine: effects on transmembrane properties of cerebellar Purkinje cells.
    Science. 1971 Jan 15;171(3967):192-4 PMID: 4322158
  17. Studies on norepinephrine-containing afferents to Purkinje cells of rat cerebellum. II. Sensitivity of Purkinje cells to norepinephrine and related substances administered by microiontophoresis.
    Brain Res. 1971 Feb 5;25(3):523-34 PMID: 4395919
  18. Activation of the pathway from locus coeruleus to rat cerebellar Purkinje neurons: pharmacological evidence of noradrenergic central inhibition.
    J Pharmacol Exp Ther. 1973 Mar;184(3):553-69 PMID: 4347049
  19. Dynamic synaptic communication: finding the vocabulary.
    Brain Res. 1973 Nov 23;62(2):299-305 PMID: 4148549
  20. Influence of norepinephrine-containing neurons derived from the locus coeruleus on lateral geniculate neuronal activities of cats.
    Brain Res. 1974 May 10;71(1):47-60 PMID: 4362502
  21. The action of norepinephrine in the rat hippocampus. I. Iontophoretic studies.
    Brain Res. 1974 May 31;72(1):79-97 PMID: 4364476
  22. The action of norepinephrine in the rat hippocampus. II. Activation of the input pathway.
    Brain Res. 1974 May 31;72(1):99-114 PMID: 4364477
  23. Dobutamine: development of a new catecholamine to selectively increase cardiac contractility.
    Circ Res. 1975 Jan;36(1):185-96 PMID: 234805
  24. Interaction of norepinephrine with cerebellar activity evoked by mossy and climbing fibers.
    Exp Neurol. 1977 Apr;55(1):269-88 PMID: 849758
  25. Probable calcium spikes in hippocampal neurons.
    Brain Res. 1977 Oct 21;135(1):157-61 PMID: 912429
  26. Cyclic AMP and contractile activity in heart.
    Adv Cyclic Nucleotide Res. 1977;8:363-420 PMID: 21550
  27. The pharmacology of atenolol.
    Postgrad Med J. 1977;53 Suppl 3:58-64 PMID: 928267
  28. The stability of noradrenaline in physiological saline solutions.
    J Pharm Pharmacol. 1978 Feb;30(2):124-6 PMID: 24100
  29. Hyperpolarizing 'alpha 2'-adrenoceptors in rat sympathetic ganglia.
    Br J Pharmacol. 1979 Mar;65(3):435-45 PMID: 218668
  30. Central catecholamine neuron systems: anatomy and physiology of the norepinephrine and epinephrine systems.
    Annu Rev Neurosci. 1979;2:113-68 PMID: 231924
  31. A calcium-activated hyperpolarization follows repetitive firing in hippocampal neurons.
    J Neurophysiol. 1980 Feb;43(2):409-19 PMID: 6247461
  32. Alpha-drenergic inhibition of calcium-dependent potentials in rat sympathetic neurones.
    J Physiol. 1980 Apr;301:191-204 PMID: 6251200
  33. Synaptic modulation of calcium-dependent potassium conductance in myenteric neurones in the guinea-pig.
    J Physiol. 1980 Aug;305:235-48 PMID: 6255145
  34. Epileptiform burst afterhyperolarization: calcium-dependent potassium potential in hippocampal CA1 pyramidal cells.
    Science. 1980 Dec 5;210(4474):1122-4 PMID: 7444438
  35. Effects of EGTA on the calcium-activated afterhyperpolarization in hippocampal CA3 pyramidal cells.
    Science. 1980 Dec 5;210(4474):1125-6 PMID: 6777871
  36. The action of norepinephrine in the rat hippocampus: intracellular studies in the slice preparation.
    Brain Res. 1981 Feb 9;206(1):107-28 PMID: 6258720
  37. Evidence for two types of afterhyperpolarization in CA1 pyramidal cells in the hippocampus.
    Brain Res. 1981 Feb 16;206(2):462-8 PMID: 6260282
  38. Mechanisms of norepinephrine actions on hippocampal pyramidal cells in vitro.
    Brain Res. 1981 Mar 16;208(2):349-62 PMID: 6260288
  39. The membrane potential of cat hippocampal neurons recorded in vivo displays four different reaction-mechanisms to iontophoretically applied transmitter agonists.
    Brain Res. 1981 May 18;212(2):331-43 PMID: 6112049
  40. Noradrenergic responses in rat hippocampus: evidence for medication by alpha and beta receptors in the in vitro slice.
    Brain Res. 1981 Jun 9;214(1):113-26 PMID: 6263414
  41. Effects of sleep and arousal on the processing of visual information in the cat.
    Nature. 1981 Jun 18;291(5816):554-61 PMID: 6165893
  42. A simple chamber for recording from submerged brain slices.
    J Neurosci Methods. 1981 Aug;4(2):153-6 PMID: 7278366
  43. The influence of attentive fixation upon the excitability of the light-sensitive neurons of the posterior parietal cortex.
    J Neurosci. 1981 Nov;1(11):1218-25 PMID: 6796657
  44. Neurotransmitters decrease the calcium conductance activated by depolarization of embryonic chick sensory neurones.
    J Physiol. 1981 Aug;317:519-35 PMID: 6118434
  45. Single cell responses in cat visual cortex to visual stimulation during iontophoresis of noradrenaline.
    Exp Brain Res. 1982;45(3):317-27 PMID: 7067768
  46. Effects of locus coeruleus stimulation on neuronal activities of dorsal lateral geniculate nucleus and perigeniculate reticular nucleus of the rat.
    Neuroscience. 1982 Mar;7(3):655-66 PMID: 6280101
  47. Noradrenergic modulation of dendrodendritic inhibition in the olfactory bulb.
    Nature. 1982 May 20;297(5863):227-9 PMID: 7078637
  48. Hippocampal noradrenergic responses in vivo and in vitro. Characterization of alpha and beta components.
    Naunyn Schmiedebergs Arch Pharmacol. 1982 Mar;318(4):259-66 PMID: 6281666
  49. Physiological role of a slow, voltage-sensitive, synaptic response mediated by an identified serotonin-containing neurone.
    Q J Exp Physiol. 1982 Jan;67(1):179-83 PMID: 7079449
  50. Norepinephrine modulates reactivity of hippocampal cells to chemical stimulation in vitro.
    Exp Neurol. 1982 Jul;77(1):86-93 PMID: 6123441
  51. Activity of norepinephrine-containing locus coeruleus neurons in behaving rats anticipates fluctuations in the sleep-waking cycle.
    J Neurosci. 1981 Aug;1(8):876-86 PMID: 7346592
  52. Norepinephrine-containing locus coeruleus neurons in behaving rats exhibit pronounced responses to non-noxious environmental stimuli.
    J Neurosci. 1981 Aug;1(8):887-900 PMID: 7346593
  53. Control of calcium current in rat sympathetic neurons by norepinephrine.
    Brain Res. 1982 Jul 22;244(1):135-44 PMID: 6288175
  54. Noradrenaline blocks accommodation of pyramidal cell discharge in the hippocampus.
    Nature. 1982 Oct 14;299(5884):636-8 PMID: 6289127
  55. Feed-forward dendritic inhibition in rat hippocampal pyramidal cells studied in vitro.
    J Physiol. 1982 Jul;328:105-23 PMID: 7131309
  56. Ionic mechanisms of cholinergic excitation in mammalian hippocampal pyramidal cells.
    Brain Res. 1982 Oct 14;249(2):333-44 PMID: 6291716
  57. Voltage-clamp analysis of muscarinic excitation in hippocampal neurons.
    Brain Res. 1982 Oct 28;250(1):71-92 PMID: 6128061
  58. Effects of norepinephrine and serotonin upon spontaneous activity and responses to mossy fiber stimulation of CA3 neurons in hippocampal slices.
    Brain Res. 1982 Dec 16;253(1-2):173-83 PMID: 6295549
  59. Pharmacological inhibition of the M-current.
    J Physiol. 1982 Nov;332:223-62 PMID: 6760380
  60. Histamine and noradrenaline decrease calcium-activated potassium conductance in hippocampal pyramidal cells.
    Nature. 1983 Mar 31-Apr 6;302(5907):432-4 PMID: 6300681
  61. Calcium-activated outward current in voltage-clamped hippocampal neurones of the guinea-pig.
    J Physiol. 1983 Apr;337:287-301 PMID: 6875931
  62. Persistent slow inward calcium current in voltage-clamped hippocampal neurones of the guinea-pig.
    J Physiol. 1983 Apr;337:303-20 PMID: 6875932
  63. Corticotropin releasing factor decreases postburst hyperpolarizations and excites hippocampal neurons.
    Science. 1983 Aug 26;221(4613):875-7 PMID: 6603658
  64. Depression of calcium-dependent potassium conductance of guinea-pig myenteric neurones by muscarinic agonists.
    J Physiol. 1983 Sep;342:253-66 PMID: 6631734
  65. Depolarization of rat isolated superior cervical ganglia mediated by beta 2-adrenoceptors.
    Br J Pharmacol. 1983 Jun;79(2):429-39 PMID: 6140042
  66. Noradrenaline-mediated synaptic inhibition in rat locus coeruleus neurones.
    J Physiol. 1983 Dec;345:477-88 PMID: 6141289
  67. Current-to-frequency transduction in CA1 hippocampal pyramidal cells: slow prepotentials dominate the primary range firing.
    Exp Brain Res. 1984;53(2):431-43 PMID: 6705872
Article Info
Journal
The Journal of physiology
Abbr.
J Physiol
ISSN
0022-3751
Published
1986-03-00
Pages
221-44
Language
English
Region
England
NLM ID
0266262
PMCID
PMC1192760
Subset
IM
Grants
NIMH NIH HHS · MH-00437 · United States
NIMH NIH HHS · MH-38256 · United States
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