Reward functions of the basal ganglia

Abstract

Besides their fundamental movement function evidenced by Parkinsonian deficits, the basal ganglia are involved in processing closely linked non-motor, cognitive and reward information. This review describes the reward functions of three brain structures that are major components of the basal ganglia or are closely associated with the basal ganglia, namely midbrain dopamine neurons, pedunculopontine nucleus, and striatum (caudate nucleus, putamen, nucleus accumbens). Rewards are involved in learning (positive reinforcement), approach behavior, economic choices and positive emotions. The response of dopamine neurons to rewards consists of an early detection component and a subsequent reward component that reflects a prediction error in economic utility, but is unrelated to movement. Dopamine activations to non-rewarded or aversive stimuli reflect physical impact, but not punishment. Neurons in pedunculopontine nucleus project their axons to dopamine neurons and process sensory stimuli, movements and rewards and reward-predicting stimuli without coding outright reward prediction errors. Neurons in striatum, besides their pronounced movement relationships, process rewards irrespective of sensory and motor aspects, integrate reward information into movement activity, code the reward value of individual actions, change their reward-related activity during learning, and code own reward in social situations depending on whose action produces the reward. These data demonstrate a variety of well-characterized reward processes in specific basal ganglia nuclei consistent with an important function in non-motor aspects of motivated behavior.

Dysregulation of the dopamine system in the pathophysiology of schizophrenia and depression

“…When exposed to behaviourally salient stimuli, such as a potential threat or a reward-related event, VTA DA neurons transition to a phasic burst firing pattern 12, 28 . Burst firing is defined by a rapid series of action potentials occurring with a short interspike interval (3–10 action potentials with 40–80 msec interspike interval) followed by a prolonged post-burst inhibition 29 .…”

Functional connectivity changes following interpersonal reactivity

“…Attachment anxiety reflects feelings of insecurity and insufficiency in a relationship, while attachment avoidance describes the tendency to avoid closeness to a partner. The Adult Attachment Interview (AAI, George, Kaplan, & Main, 1984, 1996, on the other hand, determines attachment representations with a semistructured interview investigating the evaluation of childhood experiences with one's caregivers, but also addresses current experiences in relationships. The AAI classifies secure and insecure attachment representations with insecurity further divided into insecure-dismissing and insecure-preoccupied attachment representation (Hesse, 2008) (Figure 1).…”

“…Two neuroendocrine systems are involved in attachment behavior: the oxytonergic bonding system and the dopaminergic reward system (Bartels & Zeki, 2004;Strathearn, Fonagy, Amico, & Montague, 2009;Strathearn, Li, Fonagy, & Montague, 2008). Reward regions, in particular the caudate nucleus (CN), are rich in dopaminergic neurons and therefore largely involved in positive reinforcement and reward processing of social situations (Schultz, 2016). CN also shows high density of receptors for the hormones oxytocin and vasopressin, which are neural modulators of attachment processing (Loup, Tribollet, Dubois-Dauphin, & Dreifuss, 1991;Pan et al, 2016).…”

Meta-analytic clustering dissociates brain activity and behavior profiles across reward processing paradigms

“…Reward learning is a fundamental cognitive process vital for adaptive functioning that consequently, when disrupted, has a significant impact on mental health. Widely accepted and commonly adopted neurocognitive models of reward learning propose that value predictions are formed and updated based on dopaminergic reward prediction error (RPE) signals (Glimcher, 2011;Hollerman & Schultz, 1998;Knutson et al, 2001;Schultz, 1998;Schultz, 2016;Schultz, Dayan & Montague, 1997). RPE signals represent the discrepancy between expected outcomes and actual outcomes (Rescorla, 1972).…”