GABA neurons in the ventral tegmental area responding to peripheral sensory input

PLoS One. 2012;7(12):e51507. doi: 10.1371/journal.pone.0051507. Epub 2012 Dec 10.

Abstract

Dopamine (DA) neurons in the ventral tegmental area (VTA) not only participate in reward processing, but also respond to aversive stimuli. Although GABA neurons in this area are actively involved in regulating the firing of DA neurons, few data exist concerning the responses of these neurons to aversive sensory input. In this study, by employing extracellular single-unit recording and spectral analysis techniques in paralyzed and ventilated rats, we found that the firing pattern in 44% (47 of 106) of GABA cells in the VTA was sensitive to the sensory input produced by the ventilation, showing a significant ventilation-associated oscillation in the power spectra. Detailed studies revealed that most ventilation-sensitive GABA neurons (38 of 47) were excited by the stimuli, whereas most ventilation-sensitive DA neurons (11 of 14) were inhibited. When the animals were under anesthesia or the sensory pathways were transected, the ventilation-associated oscillation failed to appear. Systemic administration of non-competitive N-methyl-D-aspartase (NMDA) receptor antagonist MK-801 completely disrupted the association between the firing of GABA neurons and the ventilation. Interestingly, local MK-801 injection into the VTA dramatically enhanced the sensitivity of GABA neurons to the ventilation. Our data demonstrate that both GABA and DA neurons in the VTA can be significantly modulated by sensory input produced by the ventilation, which may indicate potential functional roles of VTA in processing sensation-related input.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials / drug effects
  • Action Potentials / physiology
  • Animals
  • Consciousness / drug effects
  • Consciousness / physiology
  • Dizocilpine Maleate / pharmacology
  • Dopaminergic Neurons / drug effects
  • Dopaminergic Neurons / physiology
  • GABAergic Neurons / drug effects
  • GABAergic Neurons / physiology*
  • Male
  • Rats
  • Rats, Sprague-Dawley
  • Receptors, N-Methyl-D-Aspartate / metabolism
  • Sensation / physiology*
  • Somatosensory Cortex / physiology
  • Ventilation
  • Ventral Tegmental Area / drug effects
  • Ventral Tegmental Area / physiology*

Substances

  • Receptors, N-Methyl-D-Aspartate
  • Dizocilpine Maleate

Grants and funding

The authors gratefully acknowledge the financial support from National Basic Research Program of China (2009CB522000, 2011CB5C4403) and the National Natural Science Foundation of China (30825042, 81130023). The support from the Priority Academic Program Development (PAPD) of Jiangsu Higher Education Institutions is also appreciated. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.