Pedunculopontine tegmental stimulation evokes striatal dopamine efflux by activation of acetylcholine and glutamate receptors in the midbrain and pons of the rat

Eur J Neurosci. 2003 Feb;17(4):751-62. doi: 10.1046/j.1460-9568.2003.02511.x.

Abstract

The pedunculopontine tegmental nucleus appears to influence striatal dopamine activity via cholinergic and glutamatergic afferents to dopaminergic cells of the substantia nigra pars compacta. We measured changes in striatal dopamine oxidation current (dopamine efflux) in response to electrical stimulation of the pedunculopontine tegmental nucleus using in vivo electrochemistry in urethane-anaesthetized rats. Pedunculopontine tegmental nucleus stimulation evoked a three-component change in striatal dopamine efflux, consisting of: (i) an initial rapid increase of 2 min duration; followed by (ii) a decrease below prestimulation levels of 9 min duration; then by (iii) a prolonged increase lasting 35 min. Intra-nigral infusions of the ionotropic glutamate receptor antagonist kynurenate (10 microg/ microL) or the nicotinic cholinergic receptor antagonist mecamylamine (5 microg/0.5 microL) selectively attenuated the rapid first component, while systemic injections of the muscarinic cholinergic antagonist scopolamine (5 mg/kg, i.p.) diminished the second and third components. In addition, intra-pedunculopontine tegmental nucleus infusions of the M2 muscarinic antagonist methoctramine (50 microg/ microL) selectively abolished the inhibitory second component, while intranigral infusions of scopolamine (200 microg/ microL) selectively abolished the prolonged third component. Intra-nigral infusions of the metabotropic glutamate receptor antagonist (+)-alpha-methyl-4-carboxyphenylglycine (2 microg/ microL) had no effect on pedunculopontine tegmental nucleus-elicited striatal dopamine efflux. These results suggest that the pedunculopontine tegmental nucleus utilizes nicotinic and ionotropic glutamate receptors in the substantia nigra to mediate rapid activation, M2-like muscarinic autoreceptors in the pedunculopontine tegmental nucleus to mediate decreased activation, and muscarinic receptors in the substantia nigra (probably of the M5 subtype) to mediate prolonged activation, of the nigrostriatal dopaminergic system.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Corpus Striatum / cytology
  • Corpus Striatum / metabolism*
  • Dopamine / metabolism*
  • Electric Stimulation / methods
  • Electrophysiology
  • Excitatory Amino Acid Antagonists / pharmacology
  • Functional Laterality
  • Injections, Intraperitoneal
  • Male
  • Mesencephalon / drug effects
  • Mesencephalon / metabolism*
  • Microinjections
  • Muscarinic Antagonists / pharmacology
  • Neurons / cytology
  • Neurons / drug effects
  • Neurons / metabolism
  • Pedunculopontine Tegmental Nucleus / metabolism*
  • Pedunculopontine Tegmental Nucleus / radiation effects
  • Pons / drug effects
  • Pons / metabolism*
  • Rats
  • Rats, Wistar
  • Receptors, Cholinergic / metabolism*
  • Receptors, Glutamate / metabolism*
  • Substantia Nigra / cytology
  • Substantia Nigra / drug effects
  • Substantia Nigra / metabolism
  • Time Factors

Substances

  • Excitatory Amino Acid Antagonists
  • Muscarinic Antagonists
  • Receptors, Cholinergic
  • Receptors, Glutamate
  • Dopamine