A differential role for human hippocampus in novelty and contextual processing: Implications for P300

Abstract

The role of the hippocampus in P300 has long been debated. Here, we present a theoretical framework that elucidates hippocampal contributions to scalp P300 based on intracranial and lesion research combined with emerging evidence on the role of the hippocampus in rapid statistical learning, memory, and novelty processing. The P300 has been divided in two subcomponents: a fronto‐central P3a related to novelty and distractor processing, and a parietal P3b related to target detection. Interest in a role for hippocampus in scalp P300 was sparked by P3‐like ERPs measured intracranially in human hippocampus. Subsequent medial temporal lobe lesion studies show intact scalp P3b, indicating that the hippocampus is not critical for P3b. This contrasts with the scalp P3a, which was significantly diminished in human patients with lesions in the posterior hippocampus. This suggests a differential role for hippocampus in P3a and P3b. Our framework purports that the hippocampus plays a central role in distractor processing that leads to P3a generation in cortical regions. We also propose that the hippocampus is involved at the end of the cognitive episode for both P3a and P3b implementing contextual updating. P3‐like ERPs measured in hippocampus may reflect input signals from cortical regions implementing updates based on the outcome of cognitive processes underlying scalp P3, enabling a model update of the environment facilitated by the hippocampus. Overall, this framework proposes an active role for the hippocampus in novelty processing leading up to P3a generation, followed by contextual updating of the outcome of both scalp P3a and P3b.

How predictability affects habituation to novelty?

“…Brain activity related to habituation to stimuli has been investigated in many studies, including a series of studies by Polich et al (15)(16)(17)(18)(19)(20)(22)(23)(24)(25). This present study clarified for the first time the influence of uncertainty and prediction error on brain activity related to habituation to novel stimuli based on mathematical models.…”

“…P300 for stimulus is known to predominantly appear from the frontal to the central and parietal brain parts and is considered to reflect attention to stimuli. In recent years, some studies have investigated habituation to stimuli using P300 (22)(23)(24)(25), but the effects of predictability (uncertainties and prediction errors) on brain activity related to novelty habituation remain unclear. In this study, we demonstrated an experimental evidence of the model prediction using P300.…”

Prediction errors indexed by the P3 track the updating of complex long-term memory schemas

“…The P300 potential has been strongly linked to context updating processes, for example in oddball and working memory tasks (Sutton, Braren, Zubin, & John, 1965)). The literature on the P300 has distinguished between a more frontally distributed P3a, which has been linked to mismatch and novelty processing, and shown to be dependent on the hippocampus, and the P3b, a parietally centred component, more strongly linked to target detection, and not as strongly linked to hippocampal processing (Fonken et al, 2019).…”

“…More generally, the P300 has been linked to updating of the (immediate) context in a number of tasks that require the comparison of a current stimulus with a recently preceding stimulus, and with the updating of information in working-memory tasks (Polich, 2012). It has been suggested to be divisible into two subcomponents the fronto-centrally distributed P3a, and the P3b, which has a centro-parietal topography (see Fonken, Kam, & Knight, 2019 for a review).…”

50+ years of P300: Where are we now?

“…Their methodology and findings solidify how the central and peripheral nervous system contribute to P300. Fonken, Kam, and Knight (2020) provide a highly informative revisit to the role of hippocampal functions that contribute to P3a and P3b generation. A theoretical framework was proposed of hippocampal contributions to P300, derived from intracranial and lesion research on the hippocampus linked to statistical learning, memory, and novelty processing.…”