Phase relationships support a role for coordinated activity in the indirect pathway in organizing slow oscillations in basal ganglia output after loss of dopamine

Neuroscience. 2007 Jan 19;144(2):762-76. doi: 10.1016/j.neuroscience.2006.10.006. Epub 2006 Nov 15.

Abstract

The goal of the present study was to determine the phase relationships of the slow oscillatory activity that emerges in basal ganglia nuclei in anesthetized rats after dopamine cell lesion in order to gain insight into the passage of this oscillatory activity through the basal ganglia network. Spike train recordings from striatum, subthalamic nucleus (STN), globus pallidus (GP), and substantia nigra pars reticulata (SNpr) were paired with simultaneous local field potential (LFP) recordings from SNpr or motor cortex ipsilateral to a unilateral lesion of substantia nigra dopamine neurons in urethane-anesthetized rats. Dopamine cell lesion induced a striking increase in incidence of slow oscillations (0.3-2.5 Hz) in firing rate in all nuclei. Phase relationships assessed through paired recordings using SNpr LFP as a temporal reference showed that slow oscillatory activity in GP spike trains is predominantly antiphase with oscillations in striatum, and slow oscillatory activity in STN spike trains is in-phase with oscillatory activity in cortex but predominantly antiphase with GP oscillatory activity. Taken together, these results imply that after dopamine cell lesion in urethane-anesthetized rats, increased oscillatory activity in GP spike trains is shaped more by increased phasic inhibitory input from the striatum than by phasic excitatory input from STN. In addition, results show that oscillatory activity in SNpr spike trains is typically antiphase with GP oscillatory activity and in-phase with STN oscillatory activity. While these observations do not rule out additional mechanisms contributing to the emergence of slow oscillations in the basal ganglia after dopamine cell lesion in the anesthetized preparation, they are compatible with 1) increased oscillatory activity in the GP facilitated by an effect of dopamine loss on striatal 'filtering' of slow components of oscillatory cortical input, 2) increased oscillatory activity in STN spike trains supported by convergent antiphase inhibitory and excitatory oscillatory input from GP and cortex, respectively, and 3) increased oscillatory activity in SNpr spike trains organized by convergent antiphase inhibitory and excitatory oscillatory input from GP and STN, respectively.

MeSH terms

  • Action Potentials / drug effects
  • Action Potentials / physiology*
  • Adrenergic Agents / pharmacology
  • Analysis of Variance
  • Animals
  • Basal Ganglia / cytology*
  • Behavior, Animal
  • Biological Clocks / drug effects
  • Biological Clocks / physiology*
  • Cell Death / drug effects
  • Dopamine / metabolism*
  • Male
  • Neural Pathways / physiology*
  • Neurons / drug effects
  • Neurons / physiology*
  • Oxidopamine / pharmacology
  • Rats
  • Rats, Sprague-Dawley
  • Statistics, Nonparametric
  • Substantia Nigra / drug effects
  • Substantia Nigra / physiology

Substances

  • Adrenergic Agents
  • Oxidopamine
  • Dopamine