Effects of pedunculopontine nucleus (PPN) stimulation on caudal pontine reticular formation (PnC) neurons in vitro

J Neurophysiol. 2002 Jun;87(6):3033-47. doi: 10.1152/jn.2002.87.6.3033.

Abstract

Stimulation of the pedunculopontine nucleus (PPN) is known to induce changes in arousal and postural/locomotor states. Previously, PPN stimulation was reported to induce prolonged responses (PRs) in extracellularly recorded PnC neurons in the decerebrate cat. The present study used intracellular recordings in semihorizontal slices from rat brain stem (postnatal days 12-21) to determine responses in PnC neurons following PPN stimulation. Two-thirds (65%) of PnC neurons showed PRs after PPN stimulation. PnC neurons with PRs had higher amplitude afterhyperpolarizations (AHP) than non-PR (NPR) neurons. Both PR and NPR neurons were of mixed cell types characterized by "A" and/or "LTS," or neither of these types of currents. PnC cells showed decreased AHP duration with age, due mostly to decreased AHP duration in NPR cells. The longest mean duration PRs were induced by stimulation at 60 and 90 Hz compared with 10 or 30 Hz. Maximal firing rates in PnC cells during PRs were induced by PPN stimulation at 60 Hz compared with 10, 30, or 90 Hz. BaCl2 superfusion blocked PPN stimulation-induced PRs, suggesting that PRs may be mediated by blockade of potassium channels, in keeping with increased input resistance observed during PRs. Depolarizing pulses failed to elicit, and hyperpolarizing pulses failed to reset, PPN stimulation-induced PRs, suggesting that PRs may not be plateau potentials. Pharmacological testing revealed that nifedipine superfusion failed to block PPN stimulation-induced PRs; i.e., PRs may not be calcium channel-dependent. The muscarinic cholinergic agonist carbachol induced depolarization in most PR neurons tested, and the muscarinic cholinergic antagonist scopolamine reduced or blocked PPN stimulation-induced PRs in some PnC neurons, suggesting that some PRs may be due to muscarinic receptor activation. The nonspecific ionotropic glutamate receptor antagonist kynurenic acid failed to block PPN stimulation-induced PRs, as did the metabotropic glutamate receptor antagonist (R, S)-alphamethyl-4-carboxyphenylglycine, suggesting that PRs may not be mediated by glutamate receptors. These findings suggest that PPN stimulation-induced PRs may be due to increased excitability following closing of muscarinic receptor-sensitive potassium channels, allowing PnC neurons to respond to a transient, frequency-dependent depolarization with long-lasting stable states. PPN stimulation appears to induce PRs using parameters known best to induce locomotion. This mechanism may be related to switching from one state to another (e.g., locomotion vs. standing or sitting, waking vs. non-REM sleep or REM sleep).

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Action Potentials / drug effects
  • Action Potentials / physiology
  • Anesthetics, Local / pharmacology
  • Animals
  • Carbachol / pharmacology
  • Cholinergic Agonists / pharmacology
  • Electric Stimulation
  • Electrophysiology
  • Excitatory Amino Acid Antagonists / pharmacology
  • Female
  • Kynurenic Acid / pharmacology
  • Muscarinic Antagonists / pharmacology
  • Neurons / physiology
  • Organ Culture Techniques
  • Pons / cytology
  • Pons / physiology*
  • Pregnancy
  • Rats
  • Rats, Sprague-Dawley
  • Reticular Formation / cytology
  • Reticular Formation / physiology*
  • Scopolamine / pharmacology
  • Tegmentum Mesencephali / cytology
  • Tegmentum Mesencephali / physiology*
  • Tetrodotoxin / pharmacology

Substances

  • Anesthetics, Local
  • Cholinergic Agonists
  • Excitatory Amino Acid Antagonists
  • Muscarinic Antagonists
  • Tetrodotoxin
  • Carbachol
  • Scopolamine
  • Kynurenic Acid