On the neural computation of utility

Abstract

The rewarding effect produced by electrical stimulation of the lateral hypothalamus can compete and summate with gustatory rewards. However, physiological manipulations, such as sodium depletion and the accumulation of an energy-rich solution in the gut, can alter the rewarding impact of the gustatory stimuli without producing substantial changes in the rewarding effect of the electrical stimulation. On the basis of their competition and summation, it is argued that the artificial and natural rewards are evaluated in a common currency, represented in an aggregate firing-rate code. Such a code would make it possible for the synchronous, spatially contiguous pattern of neural firing induced by the electrode to simulate a signal normally produced by asynchronous, spatially distributed activity. It is suggested that a unidimensional code of this sort is employed to represent the utility of a goal object. In order for physiological feedback to alter the utility of one natural reward, such as sucrose, without changing the utility of a second natural reward, such as a salt solution, the physiological feedback signals must enter into the computation of utility at a stage of processing in which the representations of the two natural rewards are distinct. However, orderly choice between such rewards implies that their utilities are expressed ultimately in a common neural currency. That physiological feedback alters the rewarding effects of the gustatory stimuli suggests that the physiological feedback signals modulate the value of such natural stimuli at a stage of processing prior to their translation into a common currency. In contrast, physiological feedback would fail to alter the rewarding effect of the electrical stimulation if the electrically evoked signal is injected at a later stage processing, a stage in which different rewards are represented in a common currency. In this view, the signal injected by the electrical stimulation mimics the utility of a natural stimulus but not its sensory quality.