Adaptive anterior hippocampal responses to oddball stimuli

Strange, Bryan A.; Dolan, Raymond J. · 2001 · Crossref

DOI: 10.1002/hipo.1084

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Summary

This study investigates the role of the anterior hippocampus in detecting "oddball" stimuli—items that deviate from a prevailing context—using event-related functional magnetic resonance imaging (fMRI). While previous electrophysiological studies suggested a hippocampal role in oddball detection, prior functional imaging experiments had failed to demonstrate such activation. The authors hypothesized that this discrepancy arose because previous studies did not account for rapid neural adaptation. They proposed that the hippocampus registers mismatches between expectation and experience, and that this response should diminish as oddball stimuli become predictable through repeated exposure. The experiment involved 11 subjects who viewed sequential lists of nouns during fMRI scanning. Each list contained 19 nouns belonging to a single semantic category, with one "oddball" inserted. Three types of oddballs were used: perceptual (novel font), semantic (different category), and emotional (aversive content). Subjects performed either a shallow encoding task (judging letter shape) or a deep encoding task (judging living/nonliving status) across four scanning sessions. The experimental design specifically modeled the hemodynamic response to the first versus subsequent presentations of oddballs to test for adaptation effects. Statistical analysis employed a random-effects model to identify regions where activation decreased from the first to the second session. The results demonstrated significant adaptive activation in the left anterior hippocampus for all three oddball types. This response was strongest during the first session and attenuated in subsequent sessions, confirming the hypothesis of rapid adaptation. Crucially, this adaptive response was not modulated by the depth of encoding, suggesting the process is automatic. However, a distinct region in the more lateral left anterior hippocampus showed an interaction with encoding depth for semantic oddballs, exhibiting enhanced adaptation only during deep processing. Other brain regions, such as the fusiform cortex and amygdala, showed non-adapting responses specific to perceptual and emotional oddballs, respectively. The findings resolve the conflict between electrophysiological and imaging data by showing that hippocampal responses to oddballs are transient and adapt quickly. The authors conclude that the anterior hippocampus functions as a comparator, registering mismatches between expectation and experience. This "novelty of novelty" effect supports a theory where the hippocampus detects violations of context regardless of task demands, facilitating the orienting response to salient stimuli. The study implies that failure to detect hippocampal activation in previous imaging studies was likely due to averaging responses across the entire experiment, thereby masking the rapid adaptive decline.

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• signal detection theory