Reward Anticipation Is Encoded Differently by Adolescent Ventral Tegmental Area Neurons

Abstract

Background Elucidating the neurobiology of the adolescent brain is fundamental to our understanding of the etiology of psychiatric disorders such as schizophrenia and addiction, the symptoms of which often manifest during this developmental period. Dopamine neurons in the ventral tegmental area (VTA) are strongly implicated in adolescent behavioral and psychiatric vulnerabilities, but little is known about how adolescent VTA neurons encode information during motivated behavior. Methods We recorded daily from VTA neurons in adolescent and adult rats during learning and maintenance of a cued, reward-motivated instrumental task, and extinction from this task. Results During performance of the same motivated behavior, identical events were encoded differently by adult and adolescent VTA neurons. Adolescent VTA neurons with dopamine-like characteristics lacked a reward anticipation signal and showed a smaller response to reward delivery compared to adults. After extinction, however, these neurons maintained a strong phasic response to cues formerly predictive of reward opportunity. Conclusions Anticipatory neuronal activity in the VTA supports preparatory attention and is implicated in error prediction signaling. Absence of this activity, combined with persistent representations of previously rewarded experiences, may provide a mechanism for rash decision making in adolescents.

Age and sex differences in behavioral flexibility, sensitivity to reward value, and risky decision-making

“…Despite evidence for a peri/post-pubertal peak in reward consumption (Friemel et al, 2010;Marshall et al, 2017), motivation (Friemel et al, 2010), and cocaine self-administration in males (Wong, Ford, Pagels, McCutcheon, & Marinelli, 2013), several studies measuring instrumental responding for non-drug reinforcers report either comparable responding (Sturman & Moghaddam, 2011;Kim, Simon, Wood, & Moghaddam, 2016;Naneix, Marchand, Di Scala, Pape, & Coutureau, 2012) or decreased responding in adolescents compared to adults (present study; Andrzejewski et al, 2011;Sturman et al, 2010;Hankosky et al, 2017). One factor that could contribute to the apparent discrepancies between reward consumption and instrumental responding is whether the measure accounts for differences in body weight.…”

Dopamine modulation of prefrontal cortex activity is manifold and operates at multiple temporal and spatial scales

“…Bursts were repeated every 500 ms (Figure 1C). All stimulation parameters were applied for 10-20 min because maze or operant asks typically last for this duration during which multiple trials (approximately 100 for fixed ratio operant tasks) are repeated 23, 28, 29 .…”

Behavioral, physiological, and neural signatures of surprise during naturalistic sports viewing

“…Classically, the VTA 43,44 and NAcc 12,45,46 respond strongly when rewards are larger or earlier than expected (i.e., reward prediction errors, or RPEs). However, the VTA can respond more broadly to variables other than reward 47 , including sensory PEs 48-50 , unexpected events 51,52 , aversive PEs 53 , changes in hidden belief states 31,54 , reward expectation 55,56 , advance information 57 , and stimulusstimulus learning 58 , all in the absence of (or controlling for) reward.…”