Simple paradigm for investigating the learning of cost-benefit associations in monkeys

In most instances, before a reward can be consumed effort must be expended to acquire it. Converging behavioral data show that when subjects make cost-benefit decisions, they weigh the value of potential rewards against the perceived costs of their effort. Studies have linked dopaminergic (DA) signaling to these calculations. For instance, while response properties of primate DA neurons reflect the value of cues associated with reward (Schultz et al., 1997), these responses are reduced when the effort associated with a cue is increased (Varazanni et al., 2015). In addition to DA neurons themselves, their target sites like the striatum and prefrontal cortex, are also critical in cost-benefit processing (Friedman et. al., 2015). With the advent of techniques allowing for the reversible perturbation of specific pathways within primates (Kinoshita et al., 2011), it is now possible to causally investigate the role of specific neural circuits within the primate in cost-benefit processing. To help investigate this, we aimed to develop a simple behavioral task to examine cost-benefit behavior in primates, with the primary goals that the task: 1) was easy to learn, 2) demonstrated cost-benefit decision making, 3) exhibited learning of new cost-benefit associations, 4) was affected by manipulations in reward magnitude (a surrogate for DA signaling). Therefore we designed a paradigm in which, after fixating on a central point (500 ms), monkeys were given a choice between 2 visual cues. Cues were positioned randomly in 2 of 4 possible positions to avoid spatial response biases. To select a cue, monkeys had to saccade to this cue and maintain fixation for a period of time. The duration of fixation determined the effort level (cue A = 1 s; cue B = 5 s; cue C = 9 s) and juice amount determined the reward level. To manipulate reward magnitude, we ran one variant of this paradigm with lower reward values (cue A =0.11 ml; cue B = 0.54 ml; cue C = 0.98 ml) and the other with higher reward values (cue A = 0.16 ml; cue B = 0.81 ml; cue C = 1.46 ml). For each session 3 new visual cues were used and a randomized pair of cues were displayed on a given trial. We found that 1) animals were able to quickly learn this task, 2) during all sessions cue B became the preferred cue demonstrating a trade-off between the low effort cue (cue A) and the high reward cue (cue C) -possibly reflecting a preference for ‘middle options’ as seen in humans (Rodway et al., 2011), 3) preference for cue B increased during a session, 4) preference for cue B increased more quickly during higher reward sessions. These initial behavioral experiments pave the way for future studies investigating the causal role of specific pathways in cost-benefit processing.status: publishe