MPP(+) -dependent inhibition of Ih reduces spontaneous activity and enhances EPSP summation in nigral dopamine neurons

Br J Pharmacol. 2013 May;169(1):130-42. doi: 10.1111/bph.12104.

Abstract

Background and purpose: 1-Methyl-4-phenylpyridinium (MPP(+) ), a potent parkinsonizing agent in primates and rodents, is a blocker of mitochondrial complex I, therefore MPP(+) -induced parkinsonism is believed to depend largely on mitochondrial impairment. However, it has recently been proposed that other mechanisms may participate in MPP(+) -induced toxicity. We tackled this issue by probing the effects of an acute application of MPP(+) on substantia nigra pars compacta (SNc) dopamine (DA) neurons.

Experimental approach: The effects of MPP(+) on SNc DA neurons in acute midbrain slices were investigated with electrophysiology techniques.

Key results: MPP(+) (50 μM) was able to (i) hyperpolarize SNc DA neurons by ∼6 mV; (ii) cause an abrupt and marked (over 50%) reduction of the spontaneous activity; and (iii) inhibit the hyperpolarization-activated inward current (Ih ). MPP(+) shifted Ih activation curve towards negative potentials by ∼11 mV both in Wistar rats and in C57/BL6 mice. Inhibition was voltage- and concentration-dependent (Imax = 47%, IC50 = 7.74 μM). MPP(+) slowed Ih activation kinetics at all potentials. These effects were not dependent on (i) block of mitochondrial complex I/fall of ATP levels; (ii) activation of type 2 DA receptor; and (iii) alteration of cAMP metabolism. Finally, MPP(+) -dependent inhibition of Ih facilitated temporal summation of evoked EPSPs in SNc DA, but not in CA1 hippocampal neurons.

Conclusion and implications: Reduced functionality of Ih in SNc DA neurons, via increased responsiveness towards synaptic excitation, might play a role in MPP(+) -induced parkinsonism and, possibly, in the pathogenesis of human Parkinson's.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 1-Methyl-4-phenylpyridinium / administration & dosage
  • 1-Methyl-4-phenylpyridinium / toxicity*
  • Animals
  • Cyclic AMP / metabolism
  • Dopaminergic Neurons / drug effects*
  • Dopaminergic Neurons / metabolism
  • Dose-Response Relationship, Drug
  • Electrophysiological Phenomena
  • Excitatory Postsynaptic Potentials / drug effects*
  • Hippocampus / drug effects
  • Hippocampus / metabolism
  • Inhibitory Concentration 50
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mitochondria / metabolism
  • Rats
  • Rats, Wistar
  • Receptors, Dopamine D2 / drug effects
  • Receptors, Dopamine D2 / metabolism
  • Species Specificity
  • Substantia Nigra / drug effects*
  • Substantia Nigra / metabolism
  • Synapses / drug effects
  • Synapses / metabolism

Substances

  • Receptors, Dopamine D2
  • Cyclic AMP
  • 1-Methyl-4-phenylpyridinium