Abstract
Drug addiction is a syndrome of dysregulated motivation, evidenced by intense drug craving and compulsive drug-seeking behavior. In the search for common neurobiological substrates of addiction to different classes of drugs, behavioral neuroscientists have attempted to determine the neural basis for a number of motivational concepts and describe how they are changed by repeated drug use. Here, we describe these concepts and summarize previous work describing three major neural systems that play distinct roles in different conceptual aspects of motivation: (1) a nigrostriatal system that is involved in two forms of instrumental learning, (2) a ventral striatal system that is involved in Pavlovian incentive motivation and negative reinforcement, and (3) frontal cortical areas that regulate decision making and motivational processes. Within striatal systems, drug addiction can involve a transition from goal-oriented, incentive processes to automatic, habit-based responding. In the cortex, weak inhibitory control is a predisposing factor to, as well as a consequence of, repeated drug intake. However, these transitions are not absolute, and addiction can occur without a transition to habit-based responding, occurring as a result of the overvaluation of drug outcomes and hypersensitivity to incentive properties of drug-associated cues. Finally, we point out that addiction is not monolithic and can depend not only on individual differences between addicts, but also on the neurochemical action of specific drug classes.
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Notes
- 1.
Note that “substance use disorder” in humans is diagnosed on a continuum from mild to severe based on 11 behavioral criteria laid out in the DSM V, which does not mention “addiction.” This choice is in part intended to help identify and treat overuse of drugs (e.g., alcohol and nicotine which can cause or worsen a number of other conditions) and also to avoid social stigmas associated with the term “addiction,” which may result from the lack of clear biological markers that identify the addicted state. We avoid this symptomatological approach to describing addiction in favor of focusing on the core motivational processes involved in drug-taking, in a manner analogous to the National Institute of Mental Health’s Research Domain Criteria (RDoC) initiative (Cuthbert 2014; Litten et al. 2015; NIMH 2015).
- 2.
These models also disagree regarding the relationship between dopamine and hedonia, whereas an altered hedonic set point is proposed to be mediated in part by changes in dopamine; the “liking” reaction to rewards is dopamine independent (Berridge and Robinson 1998; Koob and Le Moal 2008). This discrepancy may lie in the definition of hedonia, which may be referred to generally as affect or pleasure, or operationalized into a specific subjective experience or behavioral measure.
- 3.
Note that this is a deviation from McEwen’s definition of allostasis , which states that allostasis consists of the adaptive physiological changes that are evoked in order to return a system to homeostasis. Thus, this Koob’s allostatic state is better referred to as allostatic load, which McEwen defines as the long-term cost of allostasis that accumulates over time (McEwen 1998).
- 4.
Note that neuroadaptations accompanying psychomotor sensitization are thought to overlap with the neuroadaptations underlying the incentive sensitization that drives drug-seeking and drug-taking behavior. However, psychomotor sensitization and incentive sensitization are neurobiologically dissociable processes that mediate different aspects of behavior. Thus, the presence of psychomotor sensitization is indicative of changes underlying incentive sensitization, but they are not one and the same.
- 5.
The notation for action–outcome (A-O) and stimulus–response (S-R) responding can be confusing because the drug-seeking action is denoted as either A or R in each of these conceptualizations. Indeed, notations such as \( \stackrel{a}{\longrightarrow}O \) (action–outcome), \( S\stackrel{a}{\longrightarrow}O \) (action–outcome in the presence of environmental stimuli), and \( S\stackrel{a}{\longrightarrow} \) (stimulus–response) are sometimes used to avoid this confusion (Redish et al. 2008). The notation for the activation of a conditioned motivational state by Pavlovian cues is \( \left[ {SO} \right]\stackrel{a}{\longrightarrow} \), where O is the conditioned motivational or affective state elicited by drug stimuli S and a is the behavioral response elicited by this state. However, we avoid this notation because O has quite different meanings depending on whether it is the outcome of an action (as in A-O) or the motivational state elicited by a Pavlovian stimulus (as in is \( \left[ {SO} \right]\stackrel{a}{\longrightarrow} \)).
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The authors thank MEJ Newman for making the collaboration network depicted in Fig. 2.
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Meyer, P.J., King, C.P., Ferrario, C.R. (2015). Motivational Processes Underlying Substance Abuse Disorder. In: Simpson, E., Balsam, P. (eds) Behavioral Neuroscience of Motivation. Current Topics in Behavioral Neurosciences, vol 27. Springer, Cham. https://doi.org/10.1007/7854_2015_391
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