Neuronal Correlates of Serial Decision-Making in the Supplementary Eye Field

Human behavior is influenced by serial decision-making: past decisions affect choices that set the context for selecting future options. A primate brain region that may be involved in linking decisions across time is the supplementary eye field (SEF), which, in addition to its well known visual responses and saccade-related activity, also signals the rules that govern flexible decisions and the outcomes of those decisions. Our hypotheses were that SEF neurons encode events during serial decision-making and link the sequential decisions with sustained activity. We recorded from neurons in the SEF of two rhesus monkeys (Macaca mulatta, one male, one female) that performed a serial decision-making task. The monkeys used saccades to select a rule that had to be applied later in the same trial to discriminate between visual stimuli. We found, first, that SEF neurons encoded the spatial parameters of saccades during rule selection but not during visual discrimination, suggesting a malleability to their movement-related tuning. Second, SEF activity linked the sequential decisions of rule selection and visual discrimination, but not continuously. Instead, rule-encoding activity appeared in a "just-in-time" manner before the visual discrimination. Third, SEF neurons encoded trial outcomes both prospectively, before decisions within a trial, and retrospectively, across multiple trials. The results thus identify neuronal correlates of rule selection and application in the SEF, including transient signals that link these sequential decisions. Its activity patterns suggest that the SEF participates in serial decision-making in a contextually dependent manner as part of a broader network.

SIGNIFICANCE STATEMENT Much research has gone into studying the neurobiological basis of single, isolated decisions. An important next step is to understand how the brain links multiple decisions to generate a coherent stream of thought and behavior. We studied neural activity related to serial decision-making in an area of frontal cortex known as the supplementary eye field (SEF). Neural recordings were conducted in monkeys that performed a serial decision-making task in which they selected and applied rules. We found that SEF neurons convey signals for serial decision-making, including transient encoding of one decision at the time it is needed for the next one and longer-term representations of trial outcomes, suggesting that the region plays a role in continuity of cognition and behavior.