Transient extracellular glutamate events in the basolateral amygdala track reward-seeking actions

J Neurosci. 2012 Feb 22;32(8):2734-46. doi: 10.1523/JNEUROSCI.5780-11.2012.

Abstract

The ability to make rapid, informed decisions about whether or not to engage in a sequence of actions to earn reward is essential for survival. Modeling in rodents has demonstrated a critical role for the basolateral amygdala (BLA) in such reward-seeking actions, but the precise neurochemical underpinnings are not well understood. Taking advantage of recent advancements in biosensor technologies, we made spatially discrete near-real-time extracellular recordings of the major excitatory transmitter, glutamate, in the BLA of rats performing a self-paced lever-pressing sequence task for sucrose reward. This allowed us to detect rapid transient fluctuations in extracellular BLA glutamate time-locked to action performance. These glutamate transients tended to precede lever-pressing actions and were markedly increased in frequency when rats were engaged in such reward-seeking actions. Based on muscimol and tetrodotoxin microinfusions, these glutamate transients appeared to originate from the terminals of neurons with cell bodies in the orbital frontal cortex. Importantly, glutamate transient amplitude and frequency fluctuated with the value of the earned reward and positively predicted lever-pressing rate. Such novel rapid glutamate recordings during instrumental performance identify a role for glutamatergic signaling within the BLA in instrumental reward-seeking actions.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials / drug effects
  • Amygdala / drug effects
  • Amygdala / metabolism*
  • Analysis of Variance
  • Animals
  • Behavior, Animal
  • Conditioning, Operant / drug effects
  • Conditioning, Operant / physiology*
  • Efferent Pathways / drug effects
  • Efferent Pathways / physiology
  • Electrodes, Implanted
  • Frontal Lobe / cytology
  • Frontal Lobe / drug effects
  • Frontal Lobe / physiology
  • Functional Laterality / drug effects
  • GABA-A Receptor Agonists / pharmacology
  • Glutamates / metabolism*
  • Male
  • Muscimol / pharmacology
  • Neurons / drug effects
  • Neurons / physiology
  • Rats
  • Rats, Sprague-Dawley
  • Reaction Time / drug effects
  • Reward*
  • Sodium Channel Blockers / pharmacology
  • Sucrose / administration & dosage
  • Sweetening Agents / administration & dosage
  • Tetrodotoxin / pharmacology

Substances

  • GABA-A Receptor Agonists
  • Glutamates
  • Sodium Channel Blockers
  • Sweetening Agents
  • Muscimol
  • Tetrodotoxin
  • Sucrose