Abstract

In 1953, Olds and Milner discovered that rats would readily learn to work for electrical stimulation of certain brain sites. Their findings inspired a large body of research on the neural basis of reward, motivation, and learning. Unlike consummatory behaviors, which satiate as a result of ingestion of and contact with the goal object, performance for rewarding brain stimulation is remarkably stable and persistent. Pursuit of the stimulation is enhanced by different classes of dependence-inducing drugs, suggesting that common neural mechanisms underlie the rewarding effects of drugs and electrical brain stimulation. Indeed, dopamine-containing neurons in the midbrain are implicated in both phenomena. Major schools of thought that have addressed brain stimulation reward differ with regards to the roles played by hedonic experience and craving, although there is substantial overlap between the different viewpoints. A tradition that arose in the study of machine learning has been brought to bear on the role of dopamine neurons in reward-related learning in animals and on the phenomenon of intracranial self-stimulation. Neuroeconomic perspectives strive to integrate the processing of benefits, costs, and risks into an account of decision making grounded in brain circuitry. Adjudication of the differences between the various viewpoints and progress towards identifying the relevant neural circuitry has been hindered by the lack of specificity inherent in the use of electrical stimulation to study central nervous system function. Many neurons in addition to those targeted are likely activated by such stimulation. Recently developed optogenetic methods may overcome this obstacle, providing much more specific means for stimulating or silencing populations of nerve cells selected on the basis of their gene expression, cell-body location, and projections. Coupled with behavioral methods of increasing sophistication and specificity and with quantitative modeling of signal flow in the relevant neural circuitry, the new optogenetic methods promise to bring us much closer to fulfillment of the hopes engendered long ago by the discovery of brain stimulation reward.