Physiological and neurophysiological mechanisms for exploration and mistakes

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Why do we make mistakes? We have the capacity to identify the most rewarding course of action, yet we do not always choose it. Sometimes, "mistakes" are not really mistakes, but rather a form of exploration-meaning a drive to discover new opportunities and learn about the world. In an uncertain environment, some exploration is critical, even if it does not produce the most rewarding choice in the moment. However, my recent work suggests that the same exploratory mechanisms can cause mistakes when mistakes have no conceivable benefit. I believe that this happens, in part, because our brains evolved for a world that is always uncertain, where a little exploration was almost always advantageous. The long-term goal of this research program is to elucidate how endogenous, physiological processes alter how the brain responds in identical circumstances. This proposal will lay the foundation for this goal by investigating how endogenous, physiological processes influence exploration. The central hypothesis of this proposal is that exploratory mechanisms cause us to make mistakes both when they are useful and when they are not because exploration is driven by endogenous, arousal-linked fluctuations in the tuning of decision-making circuits. We will test different aspects of this hypothesis in two human behavioral aims and one primate electrophysiology aim. Our approach is unified by the observation that a physiological exploratory mechanisms would operate in real time, meaning it would vary over the seconds or minutes across which our bodies vary. In contrast, most current models of decision-making assume that behavior only varies in trial time-in units of discrete task events like trials and reward outcomes. Aim 1 will first determine whether exploration occurs in real time or trial time by manipulating the link between trial time and real time and asking whether this manipulation systematically changes the timing of exploration. Then, expanding on previous work by myself and others that links mistakes to autonomic arousal, Aim 2 will determine whether endogenous, real time cycles of arousal are sufficient to explain temporal variation in exploration. Finally, Aim 3 will harness our capacity for large scale recordings from populations of neurons to determine whether real-time fluctuations in arousal predict the disruptions in neuronal tuning that we find during periods of exploration. If my central hypothesis is correct, these studies will show that mistakes emerge from natural fluctuations in arousal and arousal-linked patterns of brain activity. Regardless of outcome, these studies will test an implicit assumption of many decision-making models and establish a research program at the intersection of cognitive neuroscience and physiology that my team and I will build on for decades as we elucidate how different aspects of cognition-including working memory, attention, and executive control-are changed by endogenous, real time physiological processes.