Electrophysiological characterization of dopamine neuronal activity in the ventral tegmental area across the light-dark cycle

Synapse. 2014 Oct;68(10):454-67. doi: 10.1002/syn.21757. Epub 2014 Jul 4.

Abstract

Direct evidence that dopamine (DA) neurotransmission varies during the 24 h of the day is lacking. Here, we have characterized the firing activity of DA neurons located in the ventral tegmental area (VTA) using single-unit extracellular recordings in anesthetized rats kept on a standard light-dark cycle. DA neuronal firing activity was measured under basal conditions and in response to intravenous administration of increasing doses of amphetamine (AMPH: 0.5, 1, 2, 5 mg/kg), apomorphine (APO: 25, 50, 100, 200 µg/kg) and melatonin (MLT: 0.1, 1, 10 mg/kg) at different time intervals of the light-dark cycle. DA firing activity peaked between 07:00 and 11:00 h (3.5 ± 0.3 Hz) and between 19:00 and 23:00 h (4.1 ± 0.7 Hz), with lowest activity occurring between 11:00 and 15:00 h (2.4 ± 0.2 Hz) and between 23:00 and 03:00 h (2.6 ± 0.2 Hz). The highest number of spontaneously active neurons was observed between 03:00 and 06:00 h (2.5 ± 0.3 neurons/track), whereas the lowest was between 19:00 and 23:00 h (1.5 ± 0.2 neurons/track). The inhibitory effect of AMPH on DA firing rate was similar in both phases. The inhibitory effect of low dose of APO (25 μg/kg, dose selective for D2 autoreceptor) was more potent in the dark phase, whereas APO effects at higher doses were similar in both phases. Finally, MLT administration (1 mg/kg) produced a moderate inhibition of DA cell firing in both phases. These experiments demonstrate the existence of an intradiurnal rhythmic pattern of VTA DA neuronal firing activity and a higher pharmacological response of D2 autoreceptors in the dark phase.

Keywords: amphetamine; apomorphine; cosinor; diurnal rhythm; firing activity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials / drug effects
  • Amphetamine / pharmacology
  • Animals
  • Apomorphine / pharmacology
  • Central Nervous System Depressants / pharmacology
  • Circadian Rhythm / drug effects
  • Circadian Rhythm / physiology*
  • Dopamine Agonists / pharmacology
  • Dopamine Uptake Inhibitors / pharmacology
  • Dopaminergic Neurons / drug effects
  • Dopaminergic Neurons / physiology*
  • Dose-Response Relationship, Drug
  • Male
  • Melatonin / pharmacology
  • Microelectrodes
  • Photoperiod
  • Rats, Sprague-Dawley
  • Ventral Tegmental Area / drug effects
  • Ventral Tegmental Area / physiology*

Substances

  • Central Nervous System Depressants
  • Dopamine Agonists
  • Dopamine Uptake Inhibitors
  • Amphetamine
  • Melatonin
  • Apomorphine