That Old Devil Dopamine: Not the “Reward” N-transmitter?

…considerable research has demonstrated that there are empirical problems and conceptual limitations with the traditional DA hypothesis of “reward”…DA neuron activity and DA release occur in response to a variety of conditions, and span multiple timescales from very fast to relatively slow signals.

…the pattern of effects produced by DA antagonism and accumbens DA depletion on positively reinforced instrumental behavior differ substantially from extinction. Also, the processes most directly evoked by the use of the term reward (i.e., subjective pleasure, primary motivation) have been shown to be problematic in terms of demonstrating the involvement of DA systems. The idea that accumbens DA mediates the subjectively reported pleasure associated with primary positive reinforcers has been hotly debated and strongly challenged. DA antagonism or depletion does not generally impair appetitive taste reactivity for sucrose, which is a commonly used behavioral marker of hedonic reactivity in rodents. Administration of DA antagonists or nutritional depletion of DA generally has typically failed to blunt the subjectively rated euphoria produced by drugs of abuse in humans.

Neurochemical and physiological studies in animals clearly indicate that DA neuron activity is not simply tied to the delivery of primary positive reinforcers across a broad range of conditions:

  • Several studies have indicated that fast phasic DA neuron responses represent a reward prediction error, and it has been suggested that this could be related to the expected utility of rewards.
  • In addition, there also is evidence that prolonged DA signaling in response to cues that are distant from the reinforcer can provide a sustained motivational drive during maze learning that maintains instrumental behavior, (e.g.,)…phasic DA responses increased as animals progressed towards the increasing likelihood of reinforcement, …these DA signals were correlated with important features of behavioral output, such as response latencies. These responses increased as the animals progressed through the phases of the task even when reward was predicted, and thus did not represent a reward prediction error response. This led to the suggestion that mesolimbic DA helps to translate estimates of reinforcer availability into decisions to work for reward, and that mesolimbic DA release could being used as a motivational signal regulating behavioral activation and the decision of whether or not to engage in effortful activity,
  • Furthermore, the role of DA systems in instrumental learning is not limited to situations involving positive reinforcement. Striatal mechanisms in general, and accumbens DA in particular, also participate in aspects of aversive learning, punishment, and responsiveness to aversive stimuli.

[The Context]

The ability to interact with the environment in order to obtain access to significant stimuli such as food and water is critical for survival. In a complex environment, organisms usually have the option to pursue multiple reinforcers, which can vary in quality and magnitude. Furthermore, the instrumental actions that allow access to these reinforcers can be quite varied in terms of the kinetic requirements of the individual responses, as well as the overall work requirements across large units of time (e.g. ratio requirements, area of space to be covered). Thus, organisms must develop patterns of behavior that allocate behavioral resources across multiple response and reinforcer domains, which means that the animal must make choices between the various options available.

There are several research areas in behavioral science (e.g. response-reinforcement matching, optimal foraging theory, behavioral economics) that have emerged in order to characterize the choice behavior observed in these complex environments. This research has provided approaches for understanding how reinforcement value, as well as response requirements, influence the relative allocation of instrumental behavior across multiple options. Work-related response costs are an important factor influencing choice behavior, and considerable research has focused on the brain mechanisms that are involved in the exertion of effort and effort-related choice.

In assessing the possible role of DA in aspects of instrumental behavior, it is useful to consider the fundamental characteristics that allow some stimulus conditions to act as reinforcers.

  • The term reinforcement refers to behavioral contingencies that act to strengthen a particular behavior;
  • positive reinforcement refers to the process through which a response is followed by the presentation of stimulus that typically is contingent upon that response, and these events are followed by an increase in the probability of the occurrence of that response in the future…Skinner stated that reinforcement “brings behavior under the control of an appropriate deprivation…If there is a contingent relation between a response and a reinforcer, then it would also be true that there is an increase in reinforcer delivery that accompanies the increase in response probability…there is a motivational component to the action of reinforcers, which has been referred to as the “motivational corollary of the Empirical Law of Effect” … “responding is regarded as a secondary dependent variable that is important because it is instrumental in controlling consumption.”…For example, low doses of DA antagonists that suppress food reinforced lever pressing have little effect on food consumption …Nucleus accumbens DA depletion and antagonism have been shown repeatedly not to substantially impair food intake…

Thus, fundamental aspects of primary reinforcement and motivation to obtain access to the reinforcer remain intact after DA antagonism or accumbens DA depletions…In summary, the effects of interference with DA transmission can be selective and dissociative in nature, impairing some aspects of appetitive behavior while leaving others intact …these results are consistent with evidence demonstrating that some reinforced behaviors are relatively unaffected by DA antagonism, and that the effects of DA antagonists or depletion on instrumental behavior interact powerfully with the instrumental response requirement.

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