Acute Stress Enhances Associative Learning via Dopamine Signaling in the Ventral Lateral Striatum

Abstract

Acute stress transiently increases vigilance, enhancing the detection of salient stimuli in one's environment. This increased perceptual sensitivity is thought to promote the association of rewarding outcomes with relevant cues. The mesolimbic dopamine system is critical for learning cue-reward associations. Dopamine levels in the ventral striatum are elevated following exposure to stress. Together, this suggests that the mesolimbic dopamine system could mediate the influence of acute stress on cue-reward learning. To address this possibility, we examined how a single stressful experience influenced learning in an appetitive pavlovian conditioning task. Male rats underwent an episode of restraint prior to the first conditioning session. This acute stress treatment augmented conditioned responding in subsequent sessions. Voltammetry recordings of mesolimbic dopamine levels demonstrated that acute stress selectively increased reward-evoked dopamine release in the ventral lateral striatum (VLS), but not in the ventral medial striatum. Antagonizing dopamine receptors in the VLS blocked the stressinduced enhancement of conditioned responding. Collectively, these findings illustrate that stress engages dopamine signaling in the VLS to facilitate appetitive learning.

Dopamine release and its control over early Pavlovian learning differs between the NAc core and medial NAc shell

“…We monitored head entries into the food tray across training sessions. Conditioned responding was quantified as the change in the rate of head entries during the 5 s CS relative to the 5 s preceding the CS delivery [8,14].…”

“…The injectors were removed 1 min after the infusion ended. Behavioral sessions commenced 30 min after the microinjections [14,15].…”

“…Indwelling carbon fiber microelectrodes were connected to a head-mounted amplifier to monitor dopamine release in behaving rats using fast-scan cyclic voltammetry [8,14,[16][17][18][19].…”

“…Voltammetry data for a session were excluded from analysis if the detected voltammetry signal did not satisfy the chemical verification criteria [8,14,17]. Dopamine was isolated from the voltammetry signal using chemometric analysis [20] with a standard training set accounting for dopamine, pH and drift.…”

“…All quantification of dopamine responses was performed on signals that had been smoothed via a 3-point moving average. CS-evoked dopamine release was quantified as the mean dopamine level during the 5 s CS relative to the 5 s prior to the CS delivery [8,14]. The slope of the CS response was calculated by taking the difference in the mean dopamine levels during the peak (1.5 -2 s) and the end of the CS (4.5 -5 s).…”