ABSTRACT
Value-based decision making involves choosing from multiple options with different values. Despite extensive studies on value representation in various brain regions, the neural mechanism for how multiple value options are converted to motor actions remains unclear. To study this, we developed a multi-value foraging task with varying menu of items in non-human primates using eye movements that dissociates value and choice, and conducted electrophysiological recording in the midbrain superior colliculus (SC). SC neurons encoded "absolute" value, independent of available options, during late fixation. In addition, SC neurons also represent value threshold, modulated by available options, different from conventional motor threshold. Electrical stimulation of SC neurons biased choices in a manner predicted by the difference between the value representation and the value threshold. These results reveal a neural mechanism directly transforming absolute values to categorical choices within SC, supporting highly efficient value-based decision making critical for real-world economic behaviors.
Subject(s)
Choice Behavior/physiology , Reward , Superior Colliculi/physiology , Animals , Electric Stimulation/instrumentation , Eye Movement Measurements , Macaca mulatta , Male , Microelectrodes , Models, Animal , Neurons/physiology , Photic Stimulation , Saccades/physiology , Single-Cell Analysis , Superior Colliculi/cytologyABSTRACT
Microsaccades are small-amplitude (typically <1°), ballistic eye movements that occur when attempting to fixate gaze. Initially thought to be generated randomly, it has recently been established that microsaccades are influenced by sensory stimuli, attentional processes, and certain cognitive states. Whether decision processes influence microsaccades, however, is unknown. Here, we adapted two classic economic tasks to examine whether microsaccades reflect evolving saccade decisions. Volitional saccade choices of monkey and human subjects provided a measure of the subjective value of targets. Importantly, analyses occurred during a period of complete darkness to minimize the known influence of sensory and attentional processes on microsaccades. As the time of saccadic choice approached, microsaccade direction became the following: 1) biased toward targets as a function of their subjective value and 2) predictive of upcoming, voluntary choice. Our results indicate that microsaccade direction is influenced by and is a reliable tell of evolving saccade decisions. Our results are consistent with dynamic decision processes within the midbrain superior colliculus; that is, microsaccade direction is influenced by the transition of activity toward caudal saccade regions associated with high saccade value and/or future saccade choice.
