Intracranial EEG Correlates of Expectancy and Memory Formation in the Human Hippocampus and Nucleus Accumbens

Abstract

The human brain is adept at anticipating upcoming events, but in a rapidly changing world, it is essential to detect and encode events that violate these expectancies. Unexpected events are more likely to be remembered than predictable events, but the underlying neural mechanisms for these effects remain unclear. We report intracranial EEG recordings from the hippocampus of epilepsy patients, and from the nucleus accumbens of depression patients. We found that unexpected stimuli enhance an early (187 ms) and a late (482 ms) hippocampal potential, and that the late potential is associated with successful memory encoding for these stimuli. Recordings from the nucleus accumbens revealed a late potential (peak at 475 ms), which increases in magnitude during unexpected items, but no subsequent memory effect and no early component. These results are consistent with the hypothesis that activity in a loop involving the hippocampus and the nucleus accumbens promotes encoding of unexpected events.

Hippocampal Mismatch Signals Are Modulated by the Strength of Neural Predictions and Their Similarity to Outcomes

“…In either case, there may be a direct relationship between hippocampal mismatch detection and the disambiguation of similar stimuli. One caveat, however, in relating the present findings to prior evidence of hippocampal disambiguation of similar events (Bakker et al, 2008;Hulbert and Norman, 2015;Favila et al, 2016) is that our near condition only referred to stimuli from a common visual category, whereas prior studies have considered stimuli with much stronger perceptual overlap. Therefore, an informative follow-up to the present work would be to consider the relationship between prediction strength and hippocampal outcome responses across a wider range of similarities between predictions and outcomes (Lacy et al, 2011;Duncan et al, 2012).…”

“…However, for the comparison of near versus far trials, a cluster was observed in hippocampus, but not IFG or caudate. Likewise, the comparison of near versus far trials did not reveal clusters in the ventral striatum, midbrain, or insula, regions that have been associated previously with prediction error, mismatch, and/or expectancy violation signals (Berns et al, 2001;Lisman and Grace, 2005;D'Ardenne et al, 2008;Preuschoff et al, 2008;Axmacher et al, 2010).…”

“…From a prediction error perspective, mismatch signals may be greater when predictions are relatively farther from outcomes (Fiorillo et al, 2003). However, given the proposed role of the hippocampus in creating distinct representations of similar stimuli (Düzel et al, 2003;Leutgeb et al, 2007;Bakker et al, 2008;Yassa and Stark, 2011;Hulbert and Norman, 2015;Favila et al, 2016), hippocampal mismatch signals may increase when predictions are relatively closer to outcomes.…”

“…We hypothesized that hippocampal outcome responses would increase when predictions were strong but ultimately violated, consistent with a mismatch signal. Second, given the role of the hippocampus in discriminating similar events (Bakker et al, 2008;Yassa and Stark, 2011), we tested whether mismatch signals were stronger when predictions are near to outcomes compared to far from outcomes. Finally, we assessed whether hippocampal outcome responses were associated with subsequent behavioral expressions of successful memory updating.…”

The detection of transient directional couplings based on phase synchronization

“…The time interval ranging from 0 to 1000 ms after stimulus onset is sufficient to capture the main ERP components (hippocampus: a positive peak at around 200 ms and a negative peak at around 500 ms; rhinal cortex: a negative peak at around 400 ms) that have been described in previous studies [46,47]. We observe here similar ERP components, and the clear amplitude differences seen for the different conditions already indicate that the rhinal cortex and the hippocampus are involved in the memory processing steps investigated here.…”