Weighing up the benefits of work: Behavioral and neural analyses of effort-related decision making

Abstract

How we decide whether a course of action is worth undertaking is largely unknown. Recently, neuroscientists have been turning to ecological approaches to address this issue, examining how animals evaluate the costs and benefits of different options. We present here evidence from rodents and monkeys that demonstrate the degree to which they take into account work and energetic requirements when deciding what responses to make. These calculations appear to be critically mediated by the anterior cingulate cortex (ACC) and mesolimbic dopamine (DA) pathways, with damage to either causing a bias towards options that are easily obtained but yield relatively smaller reward rather than alternatives that require more work but result in greater reward. The evaluation of such decisions appears to be carried out in systems independent of those involved in delay-discounting. We suggest that top-down signals from ACC to nucleus accumbens (NAc) and/or midbrain DA cells may be vital for overcoming effort-related response costs.

Introduction

One of the central questions in the behavioral sciences is how animals decide what is worth doing. Importantly, the behavior that is most advantageous is seldom constant, but instead dependent on a number of situational variables and the internal state of the animal (Stephens & Krebs, 1986). Up until recently, however, neuroscientists have tended to investigate the selection of behavior in situations which have limited possibilities of response and a single well-defined outcome. Frequently, there is no place for considering whether or not current motivation might play a part in performance, rendering one course of action appropriate under one state, another under a different one. While this kind of research has allowed scientists to make important progress in determining the neural mechanisms of selection and evaluation of goal-oriented actions (Miller and Cohen, 2001, Schall and Thompson, 1999), such an approach may not model faithfully the typical scenario faced by animals in real-world circumstances where there are multiple potential courses of action to choose between, each of which with a set of possible costs to achieve particular consequences.

On the vast majority of occasions, our survival is not critically dependent on the decisions we make. On a day-by-day basis, while our choices may have far-reaching consequences, for most people in rich countries, they tend to be confined to issues of immediate concern, of what we should eat today rather than what we need do in order to gather sufficient sustenance to last through the night. It is therefore perhaps unsurprising that psychology and neuroscience have tended to concentrate on characterizing how behavioral acts relate to proximal rewards, trying to delineate the neural mechanisms linking sensory processes with responses and the selection of voluntary actions, with little consideration for what long-term goals an animal might possess. Nevertheless, if we start from the relatively uncontroversial position that the brain is the result of its evolutionary history and this history has been driven by natural selection, then it seems likely that many aspects of overt behavior are too the products of selective, evolutionary processes (Kacelnik, 1997). This notion, of analyzing the behavior in terms of its costs and benefits to an individual’s overall fitness, has been one pioneered by behavioral ecologists for the past fifty years, building on the principles of Niko Tinbergen (Stephens and Krebs, 1986, Tinbergen, 1951). Their approach has generally been focused purely at a behavioral level, even actively avoiding issues of mechanisms (with the exception of Tinbergen himself). Nonetheless, this methodology is being increasingly courted by neuroscientists as a novel way of approaching the link between brain and behavior (Glimcher, 2002, Platt, 2002).

In this paper, we will focus in particular on one type of cost-benefit decision making: choosing whether or not it is worth it for an animal to apply additional work to receive a larger reward. In the first section, we will consider evidence that animals do weigh up the amount of effort or persistent responding required by the available options to decide which course of action to take. We will then discuss the findings from a cost-benefit T-maze paradigm which indicates a vital role for the anterior cingulate cortex (ACC) and the mesolimbic dopamine (DA) systems in allowing animals, when conditions are favorable, to overcome effort-related response costs to obtain greater rewards (Salamone et al., 1994, Walton et al., 2002).