Neural evidence of switch processes during semantic and phonetic foraging in human memory

Author:

Lundin Nancy B.123ORCID,Brown Joshua W.124,Johns Brendan T.5,Jones Michael N.14,Purcell John R.126ORCID,Hetrick William P.127ORCID,O’Donnell Brian F.127,Todd Peter M.14

Affiliation:

1. Department of Psychological and Brain Sciences, Indiana University, Bloomington, IN 47405

2. Program in Neuroscience, Indiana University, Bloomington, IN 47405

3. Department of Psychiatry and Behavioral Health, The Ohio State University, Columbus, OH 43210

4. Cognitive Science Program, Indiana University, Bloomington, IN 47405

5. Department of Psychology, McGill University, Montréal, QC H3A 1G1, Canada

6. Department of Psychiatry, Brain Health Institute, Rutgers University, Piscataway, NJ 08854

7. Department of Psychiatry, Indiana University School of Medicine, Indianapolis, IN 46202

Abstract

Humans may retrieve words from memory by exploring and exploiting in “semantic space” similar to how nonhuman animals forage for resources in physical space. This has been studied using the verbal fluency test (VFT), in which participants generate words belonging to a semantic or phonetic category in a limited time. People produce bursts of related items during VFT, referred to as “clustering” and “switching.” The strategic foraging model posits that cognitive search behavior is guided by a monitoring process which detects relevant declines in performance and then triggers the searcher to seek a new patch or cluster in memory after the current patch has been depleted. An alternative body of research proposes that this behavior can be explained by an undirected rather than strategic search process, such as random walks with or without random jumps to new parts of semantic space. This study contributes to this theoretical debate by testing for neural evidence of strategically timed switches during memory search. Thirty participants performed category and letter VFT during functional MRI. Responses were classified as cluster or switch events based on computational metrics of similarity and participant evaluations. Results showed greater hippocampal and posterior cerebellar activation during switching than clustering, even while controlling for interresponse times and linguistic distance. Furthermore, these regions exhibited ramping activity which increased during within-patch search leading up to switches. Findings support the strategic foraging model, clarifying how neural switch processes may guide memory search in a manner akin to foraging in patchy spatial environments.

Funder

HHS | NIH | National Institute of Mental Health

National Science Foundation

The Natural Science and Engineering Research Council of Canada Discovery Grant

Indiana Clinical and Translational Sciences Institute

John Templeton Foundation

Indiana University Imaging Research Facility Seed Funding

Publisher

Proceedings of the National Academy of Sciences

Subject

Multidisciplinary

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