Evidence for area CA1 as a match/mismatch detector: A high‐resolution fMRI study of the human hippocampus

Abstract

Summary The hippocampus is proposed to switch between memory encoding and retrieval by continually computing the overlap between what is expected and what is encountered. Central to this hypothesis is that area CA1 performs this calculation. However, empirical evidence for this is lacking. To test the theoretical role of area CA1 in match/mismatch detection, we had subjects study complex stimuli and then, during high-resolution fMRI scanning, make memory judgments about probes that either matched or mismatched expectations. More than any other hippocampal subfield, area CA1 displayed responses consistent with a match/mismatch detector. Specifically, the responses in area CA1 tracked the total number of changes present in the probe. Additionally, area CA1 was sensitive to both behaviorally relevant and irrelevant changes, a key feature of an automatic comparator. These results are consistent with, and provide the first evidence in humans for, the theoretically important role of area CA1 as a match/mismatch detector.

Associative retrieval processes in the human medial temporal lobe: Hippocampal retrieval success and CA1 mismatch detection

“…There were two main findings. First, activity during the decision probe was greater in CA 1 and PRc when the participant correctly recalled the learned associate and the recognition probe differed from (mismatched) this retrieved memory, a finding consistent with the hypothesis that CA 1 acts as a comparator, differentiating between perceptual inputs that are mnemonically unexpected vs. expected (e.g., Lisman and Grace 2005; for related hr-fMRI data, see Duncan et al 2011). In this framework, mismatches may constitute associative "prediction errors" between expected and actual events, analogous to those described in models of reinforcement learning (Rescorla and Wagner 1972).…”

“…Similarly, Duncan et al (2009) observed greater hippocampal activity when the probe matched an imagined display, but greater activation on mismatch trials when the probe contained unexpected perceptual novelty. The first pattern was interpreted as a goal-modulated match signal, and the second as an automatic mismatch signal (for related CA 1 data, see Duncan et al 2011). By contrast, Dudukovic et al (2011) proposed that match enhancement occurs when a previously encountered stimulus (e.g., a decision probe) triggers the retrieval of other event details that co-occurred with the stimulus's previous encounter.…”

“…In particular, although fMRI studies have revealed increased hippocampal activation during associative novelty (e.g., Kohler et al 2005;Maguire 2006, 2007b;Duncan et al 2009; see also, Shohamy and Wagner 2008), the acquired resolution in prior studies was insufficient to distinguish the BOLD response in distinct hippocampal subfields (Carr et al 2010; although complementary questions have been explored at high resolution, e.g., Bakker et al 2008;Duncan et al 2011;Lacy et al 2011). Accordingly, using high-resolution fMRI (hr-fMRI) ( Fig.…”

Attention promotes episodic encoding by stabilizing hippocampal representations

“…We did not find a significant link between the state of CA1 during encoding and memory, although there were theoretical reasons to expect CA1 modulation, including that CA1 activity is influenced by goal states during memory retrieval (28). Future studies will be needed to clarify how and when attention modulates mnemonic processes in different subfields.…”

“…Another candidate for the attentional modulation of memory is CA1. Activity in the CA1 subfield is modulated by goal states during memory retrieval (28), and this region serves as a "comparator" of expectations-which may be induced by attentional cues-and percepts (29,30).…”