Research reportMotivational views of reinforcement: implications for understanding the behavioral functions of nucleus accumbens dopamine
Introduction
One of the most intense and dynamic areas of research in behavioral neuroscience is the study of the functions of brain dopamine (DA). DA has been implicated in several disorders, including schizophrenia, depression and Parkinson's disease. Moreover, the dominant paradigm in drug abuse research has been, for the past several years, the hypothesis that DA is the critical neurotransmitter for the mediation of reinforcement phenomena. The DA hypothesis of ‘reward’ or reinforcement has become one of the most ubiquitous and popular hypotheses in the history of neuroscience. Virtually every textbook in neuroscience, psychopharmacology or physiological psychology makes reference to the DA hypothesis of reinforcement, and one can easily find statements in support of this hypothesis on the world wide web, or in the popular press. For example, in an article in Newsweek magazine (12 February 2001), it was stated that “the pleasure circuit communicates in the language of dopamine” (p. 40). In a popular university-level textbook [29], it declares authoritatively that “Reinforcement occurs when neural circuits detect a reinforcing stimulus and cause the activation of dopaminergic neurons in the ventral tegmental area” (p. 363). In a recent review article, nucleus accumbens was referred to as the ‘Universal Addiction Site’ [48]. Indeed, the DA hypothesis of reward is no longer merely a testable scientific hypothesis, and instead has become a widely promoted dogma.
In the last few years, several papers have provided critical evaluations of the DA hypothesis of reinforcement [18], [93], [114], [128], [154], [155], [157], [160], [165], [193]. The present review is intended to have a different focus than most previous papers. The hypothesis that DA is involved in reinforcement presupposes that scientists understand or agree upon what the term ‘reinforcement’ actually means. In the present paper, we will argue that the particular model of reinforcement that one employs is of critical relevance for interpreting the literature on dopaminergic involvement in reinforcement. In summarizing various views of reinforcement, it will be suggested that learning and motivational processes are two critical aspects of reinforcement, and particular emphasis will be placed upon the fundamental importance of motivational factors for reinforcement processes involving natural stimuli such as food. Finally, this article will review the literature on aspects of motivation that are relatively preserved after interference with DA systems, and will discuss why such preserved functions render the DA hypothesis of reinforcement inadequate as a global theoretical framework.
Section snippets
DA Hypothesis of reinforcement
Several researchers are associated with the DA hypothesis of reinforcement, but the person most widely credited for the formal inception of this hypothesis is Wise (e.g. [215], [216], [218], [219], [223], [224] but see also [217], [222] for a more recent re-appraisal by this author). According to this hypothesis, DA systems mediate the reinforcing effects of several different classes of stimuli. The DA hypothesis of reinforcement was offered to explain the neural mechanisms underlying
What is reinforcement? The empirical law of effect described
The modern study of instrumental conditioning is built upon the seminal work of Thorndike and Skinner. It was Thorndike (e.g. [197]), who invented the term ‘The Law of Effect’ to describe the processes involved in instrumental conditioning. According to Thorndike, if a response occurred in the presence of a stimulus, and this led to a ‘satisfier’, then that response was likely to occur again in the presence of the same stimulus. Thorndike [197] maintained that responses ‘which are accompanied
What are the critical characteristics of reinforcing stimuli? Motivational and regulatory views of reinforcement
Typically, when a student first learns about reinforcement, it is in the context of a course in ‘learning’. When one wants to read about instrumental conditioning procedures, or schedules of reinforcement, one often looks in a book on ‘learning’. Moreover, anytime a scholar wishes to learn more about Thorndike, Skinner, Tolman, Hull, Spence, or various other researchers who have studied instrumental behavior, this information is typically discussed in terms of ‘Learning Theory’. Of course,
The empirical law of effect revisited: motivational corollary of the empirical law of effect
As noted above, Skinner did not invest a great deal of effort in discussing the critical characteristics of stimuli that allow them to act as reinforcers. Indeed, if one's goal is to develop a system of behavioral control using operant conditioning, the fact that a stimulus is reinforcing may be more important than why it is reinforcing. Nevertheless, it is useful to consider the relation between the motivational or regulatory views of reinforcement described above and Skinner's Empirical Law
The importance of motivational concepts for the dopamine hypothesis of reinforcement
In the prefatory remarks that began this article it was suggested that, for evaluating the DA hypothesis of reinforcement, it is important to identify the particular model or definition of reinforcement being employed. A careful examination of the literature shows that the motivational view of reinforcement has had a powerful influence over the DA/reinforcement hypothesis. Although some researchers have emphasized the effect of DA antagonists or depletions on response-reinforcement associative
Dissociable aspects of reinforcement and motivation: on the role of accumbens dopamine
In the pages above, evidence was reviewed indicating that motivation is seen by many investigators as a critical, even defining feature of the effects of reinforcing stimuli. Moreover, it is evident that most proponents of the DA hypothesis of reinforcement not only adhere to this view, but also actively employ it as an explanation of the impairments induced by DA antagonists. Thus, in evaluating the DA hypothesis of reinforcement, it is crucial to consider the effects of dopaminergic
Conclusions
Researchers who have attempted to identify the critical characteristics of reinforcing stimuli or reinforcing activities have generally arrived at an emphasis upon motivational factors. A thorough review of the behavioral literature indicates that, across several different investigators offering a multitude of theoretical approaches, motivation is seen by many as being fundamental to the process of reinforcement. The reinforcer has been described as a goal, a commodity, an incentive, or a
Acknowledgements
Much of the research by John D. Salamone cited in this manuscript was supported by grants from the National Science Foundation. Many thanks to Keri Nowend, Brian Carlson, Jennifer Trevitt, Susana Mingote and Suzanne Weber for their helpful comments.
References (228)
- et al.
Nucleus accumbens dopamine depletions make animals more sensitive to high ratio requirements but do not impair primary food reinforcement
Neuroscience
(1999) - et al.
Effects of dopamine antagonists and accumbens dopamine depletions on time-constrained progressive ratio performance
Pharmacol. Biochem. Behav.
(1998) - et al.
Reward and reinforcement produced by drinking sucrose: two processes that may depend on different neurotransmitters
Pharmacol. Biochem. Behav.
(1995) - et al.
Avoidance performance, cue and response–choice discrimination after neuroleptic treatment
Pharmacol. Biochem. Behav.
(1982) Short-term memory in the rhesus monkey: effects of dopamine blockade via acute haloperidol administration
Pharmacol. Biochem. Behav.
(1978)- et al.
Dopamine D1-like receptors and reward-related incentive learning
Neurosci. Biobehav. Rev.
(1998) - et al.
Microinjections of flupenthixol into the caudate-putamen but not the nucleus accumbens, amygdala or frontal cortex of rats produce intra-session declines in food-rewarded operant responding
Behav. Brain Res.
(1993) Measuring hedonic impact in animals and infants: microstructure of affective taste reactivity patterns
Neurosci. Biobehav. Rev.
(2000)- et al.
What is the role of dopamine in reward: hedonic impact, reward learning or incentive salience
Brain Res. Rev.
(1998) - et al.
Differential effects of pimozide on response-rate and choice accuracy in a self-stimulation paradigm in mice
Pharmacol. Biochem. Behav.
(1985)
High dose pimozide does not block amphetamine-induced euphoria in normal volunteers
Pharmacol. Biochem. Behav.
Schedule-dependent effects of haloperidol and amphetamine: multiple-schedule task shows within-subject effects
Pharmacol. Biochem. Behav.
A role for D2, but not D1, dopamine receptors in the response-reinstating effects of food reinforcement
Pharmacol. Biochem. Behav.
Intraacumbens raclopride attenuates amphetamine-induced locomotion, but fails to prevent the response-reinstating properties of food reinforcement
Pharmacol. Biochem. Behav.
Associative structures in instrumental learning
Effects of spiperone alone and in combination with anorectic agents on feeding parameters in the rat
Neuropharmacology
Nucleus accumbens dopamine depletions alter relative response allocation in a T-maze cost/benefit task
Behav. Brain Res.
Involvement of ventrolateral striatal dopamine in movement initiation and execution: a microdialysis and behavioral investigation
Neuroscience
Nucleus accumbens dopamine depletions in rats affect relative response allocation in a novel cost/benefit paradigm
Pharmacol. Biochem. Behav.
Different effects of nucleus accumbens and ventrolateral striatal dopamine depletions on instrumental response selection in the rat
Pharmacol. Biochem. Behav.
Different behavioral functions of dopamine in nucleus accumbens and ventrolateral striatum: a microdialysis and behavioral investigation
Neuroscience
Cocaine dependence: a disease of the brain's reward centers
J. Subst. Abuse Treat.
An update of Fowler and Das: anticholinergic reversal of haloperidol-induced, within-session decrements in rats’ lapping behavior
Pharmacol. Biochem. Behav.
Regulatory impairments following selective 6-OHDA lesions of the neostriatum
Behav. Brain Res.
Lack of an effect of 6-hydroxydopamine lesions of the nucleus accumbens on intravenous morphine self-administration
Pharmacol. Biochem. Behav.
Interactions between the amygdala and ventral striatum in stimulus-reward association: studies assessing a second-order schedule of sexual reinforcement
Neuroscience
The neuropsychological basis of addictive behavior
Brain Res. Rev.
Tremulous characteristics of the jaw movements induced by pilocarpine and ventrolateral striatal dopamine depletions
Pharmacol. Biochem. Behav.
Haloperidol-induced decrements in force and duration of rats tongue movements during licking are attenuated by concomitant anticholinergic treatment
Pharmacol. Biochem. Behav.
Effects of procurement cost on food consumption in rats
Physiol. Behav.
Some effects of pimozide on nondeprived rats licking sucrose solutions in an anhedonia paradigm
Pharmacol. Biochem. Behav.
Some effects of pimozide on nondeprived rats lever pressing maintained by a sucrose reward in an anhedonia paradigm
Pharmacol. Biochem. Behav.
Effects of neuroleptics on rate and duration of operant versus reflexive licking in rats
Pharmacol. Biochem. Behav.
Effects of pimozide on lever-pressing behavior maintained on an intermittent reinforcement schedule
Pharmacol. Biochem. Behav.
Dopamine receptor blockade and reductions in thirst produce different effects on drinking behavior
Pharmacol. Biochem. Behav.
Raclopride reduces sucrose preference in rats
Pharmacol. Biochem. Behav.
Dopamine receptors in the ventral tegmental area affect motor, but not motivational or reflexive, components of copulation in male rats
Brain Res.
The role of nucleus accumbens dopamine in motivated behavior: a unifying interpretation with special reference to reward-seeking
Brain Res. Rev.
NMDA-induced lesions of the nucleus accumbens or the ventral pallidum increase the rewarding efficacy of food deprived rats
Brain Res.
Oral motor performance following central dopamine receptor blockade
Eur. J. Pharmacol.
Foraging costs and meal patterns in ferrets
Physiol. Behav.
Palatability and foraging cost interact to control caloric intake
J. Exp. Psychol. Anim. Behav. Proc.
SCH 23390 blocks drug-conditioned place-preference and place aversion: anhedonia (lack of reward) or apathy (lack of motivation) after dopamine receptor blockade
Psychopharmacology
Response deprivation, reinforcement and economics
J. Exp. Anal. Behav.
Mechanisms of adaptive behavior: Clark L. Hull's theoretical papers, with commentary
Assessing haloperidol in rats with the barrier choice paradigm
Suma Psicologica
Dopaminergic regulation of feeding behavior: I. Differential effects of haloperidol microinjection in three striatal subregions
Psychobiology
Choice as time allocation
J. Exp. Anal. Behav.
Brain substrates of liking and wanting
Neurosci. Biobehav. Rev.
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Present address: Àrea de Psicobiologia, Campus de Riu Sec, Universitat Jaume I, 12079 Castelló, Spain.