A role for mesencephalic dopamine in activation: commentary on Berridge (2006)
Ideas about the functions of the central dopamine (DA) system may seem to have evolved quite considerably in the last decade. While the theoretical debate based on classic neuropsychopharmacological approaches has become much more sophisticated and refined, perhaps the major new concepts have derived from (1) electrophysiological observations that fast phasic firing of cells in the ventral tegmental area appear to model an error prediction signal relevant to Pavlovian or temporal difference learning models (Schultz 2002) and from (2) the relative contributions of such phasic responses with the tonic mode of action of the same DA systems (Goto and Grace 2005) Both of these empirical advances were also matched by theoretical refinement; for example, in the domain of human cognitive neuroscience, the study of the role of DA in reinforcement learning and "error prediction" learning has become highly fashionable (see, e.g. Montague et al. 2004; Frank and O'Reilly 2006) and the tonic phasic distinction has been a major new construct for modeling psychopathology, including genomic approaches (Bilder et al. 2004) One of the main thrusts of Berridge's article is a critical analysis of the role of DA in reinforcement learning, and we particularly appreciate his attempt to differentiate his account from a learning standpoint, for example, by his experiments with serial conditioned stimuli (CSs) We are graciously assigned one of the competing perspectives to Berridge's "incentive sensitization" hypothesis in terms of our speculations about the role of DA in habit learning. However, our position is a much more general one that in many ways is in harmony with that of Berridge, although on the basis of very different evidence. His discussion of a "motivational" role for the ascending DA system reminds us in many ways of notions that we have entertained in several previous articles (Robbins and Everitt 1982, 1987, 1992, 1995; Robbins et al. 1989) Thus, we suggested that functions of the central DA systems could be explained in terms of an "energetic" construct (i.e. one that accounts for the vigor and frequency of behavioral output) of "activation." This activational state, which is particularly important in the modulation of behavioral (and cognitive) output, has to be distinguished from concepts of arousal that affect the efficiency of cortical processing. As posited in our 1992 review of the considerable empirical data already then available, activation (sometimes confusingly called "behavioral arousal" is induced by many related states or stimuli, including food deprivation, "stress," psychomotor stimulant drugs, aversive stimuli such as tail pinch and foot shock, novelty, CSs, including predictors of appetitive events such as food, and also of aversive events (Robbins and Everitt 1992) The range of these stimuli and states, incidentally goes far beyond the hypothesis that the midbrain DA system responds simply to error prediction signals, especially as the class of activating stimuli also includes novel stimuli under certain conditions (c.f. Bardo et al. 1990) However, we acknowledge that there is controversy about the relative sensitivity of the midbrain DA neurons to different states and stimuli often arising from differences in the methods for indexing such changes, for example, electrophysiological, which are more sensitive to phasic Psychopharmacology (2007) 191:433 437 DOI 10.1007/s00213 006 0528 7
Psychopharmacology