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Memory-related eye movements challenge behavioral measures of pattern completion and pattern separation.

ABSTRACT: The hippocampus creates distinct episodes from highly similar events through a process called pattern separation and can retrieve memories from partial or degraded cues through a process called pattern completion. These processes have been studied in humans using tasks where participants must distinguish studied items from perceptually similar lure items. False alarms to lures (incorrectly reporting a perceptually similar item as previously studied) are thought to reflect pattern completion, a retrieval-based process. However, false alarms to lures could also result from insufficient encoding of studied items, leading to impoverished memory of item details and a failure to correctly reject lures. The current study investigated the source of lure false alarms by comparing eye movements during the initial presentation of items to eye movements made during the later presentation of item repetitions and similar lures in order to assess mnemonic processing at encoding and retrieval, respectively. Relative to other response types, lure false alarms were associated with fewer fixations to the initially studied items, suggesting that false alarms result from impoverished encoding. Additionally, lure correct rejections and lure false alarms garnered more fixations than hits, denoting additional retrieval-related processing. The results suggest that measures of pattern separation and completion in behavioral paradigms are not process-pure.

SUBMITTER: Molitor RJ

PROVIDER: S-EPMC4028360 | biostudies-literature | 2014 Jun

REPOSITORIES: biostudies-literature

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Memory-related eye movements challenge behavioral measures of pattern completion and pattern separation.

Molitor Robert J RJ Ko Philip C PC Hussey Erin P EP Ally Brandon A BA

Hippocampus 20140218 6

The hippocampus creates distinct episodes from highly similar events through a process called pattern separation and can retrieve memories from partial or degraded cues through a process called pattern completion. These processes have been studied in humans using tasks where participants must distinguish studied items from perceptually similar lure items. False alarms to lures (incorrectly reporting a perceptually similar item as previously studied) are thought to reflect pattern completion, a r ...[more]

PMID: 24493460

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Project description:Pattern separation and completion are fundamental hippocampal computations supporting memory encoding and retrieval. However, despite extensive exploration of these processes, it remains unclear whether and how top-down processes adaptively modulate the dynamics between these computations. Here we examine the role of expectation in shifting the hippocampus to perform pattern separation. In a behavioral task, 29 participants (7 males) learned a cue-object category contingency. Then, at encoding, one-third of the cues preceding the to-be-memorized objects, violated the studied rule. At test, participants performed a recognition task with old objects (targets) and a set of parametrically manipulated (very similar to dissimilar) foils for each object. Accuracy was found to be better for foils of high similarity to targets that were contextually unexpected at encoding compared with expected ones. Critically, there were no expectation-driven differences for targets and low similarity foils. To further explore these effects, we implemented a computational model of the hippocampus, performing the same task as the human participants. We used representational similarity analysis to examine how top-down expectation interacts with bottom-up perceptual input, in each layer. All subfields showed more dissimilar representations for unexpected items, with dentate gyrus (DG) and CA3 being more sensitive to expectation violation than CA1. Again, representational differences between expected and unexpected inputs were prominent for moderate to high levels of input similarity. This effect diminished when inputs from DG and CA3 into CA1 were lesioned. Overall, these novel findings strongly suggest that pattern separation in DG/CA3 underlies the effect that violation of expectation exerts on memory.SIGNIFICANCE STATEMENT What makes some events more memorable than others is a key question in cognitive neuroscience. Violation of expectation often leads to better memory performance, but the neural mechanism underlying this benefit remains elusive. In a behavioral study, we found that memory accuracy is enhanced selectively for unexpected highly similar foils, suggesting expectation violation does not enhance memory indiscriminately, but specifically aids the disambiguation of overlapping inputs. This is further supported by our subsequent investigation using a hippocampal computational model, revealing increased representational dissimilarity for unexpected highly similar foils in DG and CA3. These convergent results provide the first evidence that pattern separation plays an explicit role in supporting memory for unexpected information.

Dataset Information

Memory-related eye movements challenge behavioral measures of pattern completion and pattern separation.

Publications

Memory-related eye movements challenge behavioral measures of pattern completion and pattern separation.

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