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Research Article

Preserved capacity for learning statistical regularities and directing selective attention after hippocampal lesions

View ORCID ProfileNuttida Rungratsameetaweemana, Larry R. Squire, and John T. Serences
PNAS September 24, 2019 116 (39) 19705-19710; first published September 6, 2019 https://doi.org/10.1073/pnas.1904502116
Nuttida Rungratsameetaweemana
aNeurosciences Graduate Program, University of California San Diego, La Jolla, CA 92093;bUS Combat Capabilities Development Command Army Research Laboratory, Aberdeen Proving Ground, MD 21005;
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  • ORCID record for Nuttida Rungratsameetaweemana
  • For correspondence: nrungrat@ucsd.edu lsquire@ucsd.edu jserences@ucsd.edu
Larry R. Squire
aNeurosciences Graduate Program, University of California San Diego, La Jolla, CA 92093;cVeterans Affairs San Diego Healthcare System, San Diego, CA 92161;dDepartment of Psychiatry, University of California San Diego, La Jolla, CA 92093;eDepartment of Neurosciences, University of California San Diego, La Jolla, CA 92093;fDepartment of Psychology, University of California San Diego, La Jolla, CA 92093
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  • For correspondence: nrungrat@ucsd.edu lsquire@ucsd.edu jserences@ucsd.edu
John T. Serences
aNeurosciences Graduate Program, University of California San Diego, La Jolla, CA 92093;eDepartment of Neurosciences, University of California San Diego, La Jolla, CA 92093;fDepartment of Psychology, University of California San Diego, La Jolla, CA 92093
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  • For correspondence: nrungrat@ucsd.edu lsquire@ucsd.edu jserences@ucsd.edu
  1. Contributed by Larry R. Squire, August 6, 2019 (sent for review March 15, 2019; reviewed by Marlene Behrmann and Marvin M. Chun)

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Significance

The hippocampus is important for many kinds of learning and memory. We explored the role of the hippocampus in the learning of statistical regularities. We administered a motion discrimination task where expectation about stimulus regularities, the degree of attention afforded to the relevant stimulus, and the amount of available sensory information were manipulated. Although modestly slower overall, patients with bilateral damage to the hippocampus performed similar to controls, exhibiting a normal tendency to respond faster and more accurately when the motion direction was more probable, when the stimulus was better attended, and when more sensory evidence was present. These findings show that the ability to acquire expectations based on regularities of a sensory environment can be independent of the hippocampus.

Abstract

Prior knowledge about the probabilistic structure of visual environments is necessary to resolve ambiguous information about objects in the world. Expectations based on stimulus regularities exert a powerful influence on human perception and decision making by improving the efficiency of information processing. Another type of prior knowledge, termed top-down attention, can also improve perceptual performance by facilitating the selective processing of relevant over irrelevant information. While much is known about attention, the mechanisms that support expectations about statistical regularities are not well-understood. The hippocampus has been implicated as a key structure involved in or perhaps necessary for the learning of statistical regularities, consistent with its role in various kinds of learning and memory. Here, we tested this hypothesis using a motion discrimination task in which we manipulated the most likely direction of motion, the degree of attention afforded to the relevant stimulus, and the amount of available sensory evidence. We tested memory-impaired patients with bilateral damage to the hippocampus and compared their performance with controls. Despite a modest slowing in response initiation across all task conditions, patients performed similar to controls. Like controls, patients exhibited a tendency to respond faster and more accurately when the motion direction was more probable, the stimulus was better attended, and more sensory evidence was available. Together, these findings demonstrate a robust, hippocampus-independent capacity for learning statistical regularities in the sensory environment in order to improve information processing.

  • expectation
  • memory
  • hippocampus

Footnotes

  • ↵1To whom correspondence may be addressed. Email: nrungrat{at}ucsd.edu, lsquire{at}ucsd.edu, or jserences{at}ucsd.edu.
  • Author contributions: N.R. designed research; N.R. performed research; N.R. and J.T.S. analyzed data; and N.R., L.R.S., and J.T.S. wrote the paper.

  • Reviewers: M.B., Carnegie Mellon University; and M.M.C., Yale University.

  • The authors declare no conflict of interest.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1904502116/-/DCSupplemental.

Published under the PNAS license.

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Preserved capacity for learning statistical regularities and directing selective attention after hippocampal lesions
Nuttida Rungratsameetaweemana, Larry R. Squire, John T. Serences
Proceedings of the National Academy of Sciences Sep 2019, 116 (39) 19705-19710; DOI: 10.1073/pnas.1904502116

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Preserved capacity for learning statistical regularities and directing selective attention after hippocampal lesions
Nuttida Rungratsameetaweemana, Larry R. Squire, John T. Serences
Proceedings of the National Academy of Sciences Sep 2019, 116 (39) 19705-19710; DOI: 10.1073/pnas.1904502116
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Proceedings of the National Academy of Sciences: 116 (39)
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