Restraint increases dopaminergic burst firing in awake rats

Abstract

In anesthetized animals, dopamine neurons fire in tonic and phasic firing modes hypothesized to be regulated by dissociable circuit mechanisms. Salient events critical to learning, reward processing, and attentional selection elicit transient phasic bursts. It is unclear, however, how burst activity contributes to sustained firing patterns in awake animals and if behavioral conditions known to affect dopaminergic neurotransmission change impulse activity levels. Acute stress is known to increase extracellular dopamine in the striatum and the prefrontal cortex. In this study, we have used multiunit recording to define and follow activity patterns in single dopaminergic neurons across days and to determine how restraint, a model of acute stress, changes tonic and phasic firing patterns. Long-term recording shows that a population of 23 putative dopamine neurons has heterogeneous firing profiles under baseline conditions. In all, 62% showed significant burst activity under resting conditions, while others showed predominantly regular (17%) or random (21%) activity patterns. Restraint increased mean firing rate in all dopamine neurons, but preferentially increased burst firing in neurons with higher burst rates under resting conditions. Finally, we show that increased burst firing can persist 24 h after a single exposure to stress. These data indicate that subsets of dopamine neurons may be sensitive to circuit mechanisms activated by stress and that persistent changes in burst firing may be evidence of synaptic plasticity. Furthermore, increased burst firing may be a mechanism through which stress augments extracellular dopamine in selected terminal regions.