REVIEWS NEURAL BASIS OF DECIDING CHOOSING AND ACTING Jeffrey D Schall The ability and opportunity to make decisions and carry out effective actions in pursuit of goals is central to intelligent life Recent research has provided significant new insights into how the brain arrives at decisions makes choices and produces and evaluates the consequences of actions In fact by monitoring or manipulating specific neurons certain choices can now be predicted or manipulated Vanderbilt Vision Research Centre Department of Psychology Vanderbilt University Nashville Tennessee 37240 USA e mail jeffrey d schall vanderbilt edu Movements of physical bodies such as rocks are explained by external forces Such external factors are referred to as causes By contrast many human movements are distinguished from the movements of rocks by having explanations in terms of not just causes but reasons We describe human movements as actions directed towards a goal for a purpose and not just as events that happen through a more or less complex chain of causes Explaining my typing of these words entirely in terms of a pattern of neural activity in my spinal cord which produces muscle contractions in my fingers so that a keyboard is hit in a particular pattern seems incomplete A more satisfying explanation would include reasons desires and plans such as I want you to know this A fundamental goal of cognitive neuroscience is to understand how mental entities like reasons and desires derive from processes in the brain But as we come to understand the internal factors of human action in terms of brain function we must confront the fact that the brain comprises neurons and glia that fundamentally have no interests To paraphrase Wittgenstein what if anything is left if we subtract brain processes and associated body movements happening from the agent acting To answer this question we must understand the basic properties of decisions choices and actions and how they arise from brain processes We are beginning to reach such a level of understanding of how the brain makes decisions and generates actions This review will emphasize findings obtained in experiments in which the activity of individual neurons was monitored in specific parts of the NATURE REVIEWS NEUROSCIENCE brain of highly trained macaque monkeys performing certain tasks The tasks typically presented monkeys with a stimulus or set of stimuli that required some interpretation to determine which of two or more behavioural responses to produce to receive a juice reward Although these are rudimentary tasks compared with human decision making under more complex conditions of risks uncertainty and deadlines1 we can be optimistic that the information gained from these initial neurophysiological studies will provide a foundation for future experiments that investigate more complex decisions Choices decisions and actions The recent literature in cognitive neuroscience refers to human and nonhuman subjects as deciding attending intending and so on When a neurophysiologist uses these words does he mean the same thing as a philosopher a lawyer or the man on the street If we are to understand the neural mechanisms of decision choice and action then we must use precise and effective definitions that are consistent with both the casual and technical meanings I will discuss the operational definitions of these terms which are derived from philosophical sources2 4 Choice A choice is required when an organism is confronted with alternatives for which an action is necessary to acquire or avoid one or more of the alternatives because of a desire goal or preference An effective definition is that a choice at the most fundamental level is an overt action performed in the context of alternatives VOLUME 2 JANUARY 2001 3 3 REVIEWS Figure 1 Visual choice behaviour The pattern of gaze shifts made by a monkey searching for a randomly orientated T among randomly orientated Ls The visual array appeared after the monkey had fixated the central spot In this trial the monkey s first eye movement was to the left followed by a gaze shift to the element below the fixation spot followed by a sequence of eye movements around the perimeter of the array The T was fixated briefly before an eye movement to another L stimulus followed shortly by an eye movement back to the T This simple behaviour allows investigators to ask questions such as What processes in the brain led to the particular movements that were made How did the brain control when to move the eyes How did the brain identify and correct the errant eye movement past the T target Figure modified with permission from REF 9 taken from the Annual Review of Neuroscience Volume 22 1999 by Annual Reviews www AnnualReviews org for which explanations in terms of purposes can be given Ordering a meal at a restaurant is an example of a choice You may or may not need to deliberate about which meal you prefer but you must indicate your choice through some action like speaking or pointing at one of the options on the menu Movements of the eyes are another kind of action that can be made in the context of alternatives for a purpose FIG 1 Most visual images especially natural scenes present a multitude of alternative targets for fixation among which just one can be examined at a time Visually guided eye movements have been a very effective behaviour with which to address issues about perception cognition and choice behaviour5 Choices take time a choice process evolves from a state of more or less equipotentiality immediately after the alternatives are presented to a state of commitment before the overt action is performed With prior knowledge of the alternatives and preferences choices can be predicted FRONTAL EYE FIELD An area in the frontal lobe that receives visual inputs and produces movements of the eye 34 Decision We should start by distinguishing decide to from decide that this review is about decide to The fact that choices can be predicted means that it is possible to choose in advance I will have the Blue Plate special when we get to the restaurant This sense of choice approximates decision however important distinctions should be recognized between choice and JANUARY 2001 VOLUME 2 decision Foremost whereas choice refers to the final commitment to one alternative decision refers to the preceding deliberation about the alternatives The polarity of deciding and choosing can be highlighted by considering a visit to a new restaurant Everyone