Tracking neural correlates of successful learning over repeated sequence observations.

The neural correlates of memory formation in humans have long been investigated by exposing subjects to diverse material and comparing responses to items later remembered to those forgotten. Tasks requiring memorization of sensory sequences afford unique possibilities for linking neural memorization processes to behavior, because, rather than comparing across different items of varying content, each individual item can be examined across the successive learning states of being initially unknown, newly learned, and eventually, fully known. Sequence learning paradigms have not yet been exploited in this way, however. Here, we analyze the event-related potentials of subjects attempting to memorize sequences of visual locations over several blocks of repeated observation, with respect to pre- and post-block recall tests. Over centro-parietal regions, we observed a rapid P300 component superimposed on a broader positivity, which exhibited distinct modulations across learning states that were replicated in two separate experiments. Consistent with its well-known encoding of surprise, the P300 deflection monotonically decreased over blocks as locations became better learned and hence more expected. In contrast, the broader positivity was especially elevated at the point when a given item was newly learned, i.e., started being successfully recalled. These results implicate the Broad Positivity in endogenously-driven, intentional memory formation, whereas the P300, in processing the current stimulus to the degree that it was previously uncertain, indexes the cumulative knowledge thereby gained. The decreasing surprise/P300 effect significantly predicted learning success both across blocks and across subjects. This presents a new, neural-based means to evaluate learning capabilities independent of verbal reports, which could have considerable value in distinguishing genuine learning disabilities from difficulties to communicate the outcomes of learning, or perceptual impairments, in a range of clinical brain disorders.

Decisions are expedited through multiple neural adjustments spanning the sensorimotor hierarchy.

When decisions are made under speed pressure, "urgency" signals elevate neural activity toward action-triggering thresholds independent of the sensory evidence, thus incurring a cost to choice accuracy. While urgency signals have been observed in brain circuits involved in preparing actions, their influence at other levels of the sensorimotor pathway remains unknown. We used a novel contrast-comparison paradigm to simultaneously trace the dynamics of sensory evidence encoding, evidence accumulation, motor preparation, and muscle activation in humans. Results indicate speed pressure impacts multiple sensorimotor levels but in crucially distinct ways. Evidence-independent urgency was applied to cortical action-preparation signals and downstream muscle activation, but not directly to upstream levels. Instead, differential sensory evidence encoding was enhanced in a way that partially countered the negative impact of motor-level urgency on accuracy, and these opposing sensory-boost and motor-urgency effects had knock-on effects on the buildup and pre-response amplitude of a motor-independent representation of cumulative evidence.

Dynamic Interplay of Value and Sensory Information in High-Speed Decision Making.

In dynamic environments, split-second sensorimotor decisions must be prioritized according to potential payoffs to maximize overall rewards. The impact of relative value on deliberative perceptual judgments has been examined extensively [1-6], but relatively little is known about value-biasing mechanisms in the common situation where physical evidence is strong but the time to act is severely limited. In prominent decision models, a noisy but statistically stationary representation of sensory evidence is integrated over time to an action-triggering bound, and value-biases are affected by starting the integrator closer to the more valuable bound. Here, we show significant departures from this account for humans making rapid sensory-instructed action choices. Behavior was best explained by a simple model in which the evidence representation-and hence, rate of accumulation-is itself biased by value and is non-stationary, increasing over the short decision time frame. Because the value bias initially dominates, the model uniquely predicts a dynamic "turn-around" effect on low-value cues, where the accumulator first launches toward the incorrect action but is then re-routed to the correct one. This was clearly exhibited in electrophysiological signals reflecting motor preparation and evidence accumulation. Finally, we construct an extended model that implements this dynamic effect through plausible sensory neural response modulations and demonstrate the correspondence between decision signal dynamics simulated from a behavioral fit of that model and the empirical decision signals. Our findings suggest that value and sensory information can exert simultaneous and dynamically countervailing influences on the trajectory of the accumulation-to-bound process, driving rapid, sensory-guided actions.