Elsevier

Neuroscience

Volume 55, Issue 4, August 1993, Pages 1117-1126
Neuroscience

Mutual interactions among cholinergic, noradrenergic and serotonergic neurons studied by ionophoresis of these transmitters in rat brainstem nuclei

https://doi.org/10.1016/0306-4522(93)90325-AGet rights and content

Abstract

In urethane-anesthetized rats, single neuronal activity was recorded in or around the central gray of the caudal mesencephalon to rostral pons with multibarrel microelectrodes for ionophoretic application of acetylcholine, noradrenaline and serotonin. Neurons were classified by spike shape into broad-spike and brief-spike neurons. In the laterodorsal tegmental nucleus, locus coeruleus or dorsal raphe, broad-spike neurons, marked by Pontamine Sky Blue and discriminated in sections processed for histochemistry of reduced nicotinamide adenine dinucleotide phosphate diaphorase or Nissl staining, were presumed to be cholinergic, noradrenergic or serotonergic, respectively. The majority of these neurons were inhibited through autoreceptors, except some laterodorsal tegmental neurons which might not be furnished by autoreceptors. Noradrenaline and serotonin inhibited more than two-thirds of the laterodorsal tegmental neurons tested, while a few neurons were excited by noradrenaline. Though effects of noradrenaline on dorsal raphe neurons and those of serotonin on locus coeruleus neurons were not clear in many neurons tested, neurons affected in these examinations (30%) were all inhibited clearly and no excitatory effect was observed. Acetylcholine exerted inhibition on about one-half of dorsal raphe neurons, while effects of acetylcholine on locus coeruleus neurons were the only case in the present study in which excitation was the major effect, though more than a half of locus coeruleus neurons were not sensitive to this drug.

Thus, in this study some new data on the pharmacological properties of the cholinergic laterodorsal tegmental neurons were obtained. In addition, mutual interactions between brainstem cholinergic, noradrenergic and serotonergic neurons were assayed by comparing the pharmacological properties of these neurons tested with a uniform procedure. The interactions between these diffuse projection neurons may be involved in neural mechanisms controling vigilance, wakefulness and/or sleep.

Reference (50)

  • MoruzziG. et al.

    Brain stem reticular formation and activation of the EEG

    Electroenceph. clin. Neurophysiol.

    (1949)
  • NakamuraS. et al.

    Development and plasticity of the locus coeruleus: a review of recent physiological and pharmacological experimentation

    Prog. Neurobiol.

    (1990)
  • RasmussenK. et al.

    Single unit activity of locus coeruleus neurons in the freely moving cat. I. During naturalistic behaviors and in response to simple and complex stimuli

    Brain Res.

    (1986)
  • SegalM. et al.

    The action of norepinephrine in the rat hippocampus. II. Activation of the input pathway

    Brain Res.

    (1974)
  • TrulsonM.E. et al.

    Role of norepinephrine in regulating the activity of serotonin-containing dorsal raphe neurons

    Life Sci.

    (1984)
  • VincentS.R. et al.

    Neuropeptides and NADPH-diaphorase activity in the ascending cholinergic reticular system of the rat

    Neuroscience

    (1986)
  • YoshimuraM. et al.

    Noradrenaline mediates slow excitatory synaptic potentials in rat dorsal raphe neurons in vitro

    Neurosci. Lett.

    (1985)
  • AghajanianG.K. et al.

    Intracellular identification of central noradrenergic and serotonergic neurons by a new double labeling procedure

    J. Neurosci.

    (1982)
  • AndradeR. et al.

    Opiate- and α2-adrenoceptor hyperpolarization of locus ceruleus neurons in brain slices: reversal by cyclic adenosine 3′:5′-monophosphate analogues

    J. Neurosci.

    (1985)
  • Aston-JonesG. et al.

    Activity of norepinephrine-containing locus coeruleus neurons in behaving rats anticipates fluctuations in the sleep-waking cycle

    J. Neurosci.

    (1981)
  • Aston-JonesG. et al.

    Norepinephrine-containing locus coeruleus neurons in behaving rats exhibit pronounced responses to non-noxious environmental stimuli

    J. Neurosci.

    (1981)
  • Aston-JonesG. et al.

    Serotonin selectively attenuates glutamate-evoked activation of noradrenergic locus coeruleus neurons

    J. Neurosci.

    (1991)
  • BishopP.O. et al.

    The identification of single units in central visual pathways

    J. Physiol.

    (1962)
  • BjörklundA. et al.
  • BjörklundA. et al.
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