The mysterious motivational functions of mesolimbic dopamine

Abstract

Nucleus accumbens dopamine is known to play a role in motivational processes, and dysfunctions of mesolimbic dopamine may contribute to motivational symptoms of depression and other disorders, as well as features of substance abuse. Although it has become traditional to label dopamine neurons as "reward" neurons, this is an overgeneralization, and it is important to distinguish between aspects of motivation that are differentially affected by dopaminergic manipulations. For example, accumbens dopamine does not mediate primary food motivation or appetite, but is involved in appetitive and aversive motivational processes including behavioral activation, exertion of effort, approach behavior, sustained task engagement, Pavlovian processes, and instrumental learning. In this review, we discuss the complex roles of dopamine in behavioral functions related to motivation.

Figure 1

For several years, researchers have been making distinctions between aspects of motivated behavior, many of which are differentially affected by dopaminergic manipulations. Motivated behavior takes places in phases, in which the animal first must approach or seek the reinforcing goal stimulus (e.g. appetitive, instrumental, approach, preparatory or seeking behavior). Eventually, the organism gains access to the motivational stimulus, and directly interacts with it (consummatory or taking behavior). In addition, the distinction between activational (vigor, persistence, stimulation of sustained activity) and directional (i.e., behavior is directed towards or away from a particular stimulus) aspects of motivation has been made in the behavioral literature for many years. More recently, Berridge and colleagues have emphasized the distinction between liking (i.e., the hedonic reaction to the stimulus) and wanting (the desire for the stimulus, the tendency to consume or pursue the stimulus). These distinctions are highly relevant for characterizing the effects of DA antagonists and accumbens DA depletions on motivated behavior; several papers indicate that DA antagonism and accumbens DA depletions have a greater effect on appetitive, instrumental, preparatory or seeking behavior, as well as behavioral activation and “wanting”, while having less effect on consummatory behavior, directional aspects of motivation, and “liking”.

Figure 2

This figure emphasizes the dependence of some aspects of appetitive and aversive instrumental (i.e., seeking) behavior on nucleus accumbens DA transmission. Salamone (1991) noted that highly active instrumental behaviors elicited and supported by conditioned stimuli are very sensitive to disruption of accumbens DA transmission. Koob et al. (1978) reported that neurotoxic depletions of accumbens DA decreased behavioral activation, but actually tended to increase food consumption. Nicola (2010) emphasized the importance of accumbens DA for flexible approach to the reinforcing stimulus.

Figure 3

This figure illustrates that there are multiple dimensions that are relevant for understanding the impact of DAergic manipulations on motivated behavior. Interference with accumbens DA transmission is very likely to disrupt vigorous or effortful instrumental behaviors that are instigated or supported by conditioned stimuli. In contrast, consummatory behaviors such as food intake, which involves direct interaction with a primary motivational stimulus, as well as aversive behaviors induced by a primary aversive stimulus (e.g., escape), tend to be less easily disrupted by DAergic manipulations (see references in text). Although these factors are depicted as distinct dimensions, they also interact. For example, instrumental behaviors are generally instigated by conditioned stimuli, and conditioned stimuli also have activating properties.