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Awareness of what is learned as a characteristic of hippocampus-dependent memory

Christine N. Smith and Larry R. Squire
PNAS November 20, 2018 115 (47) 11947-11952; published ahead of print November 5, 2018 https://doi.org/10.1073/pnas.1814843115
Christine N. Smith
aVeterans Affairs San Diego Healthcare System, San Diego, CA 92161;bDepartment of Psychiatry, University of California, San Diego, La Jolla, CA 92093;
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  • For correspondence: cnsmith@ucsd.edulsquire@ucsd.edu
Larry R. Squire
aVeterans Affairs San Diego Healthcare System, San Diego, CA 92161;bDepartment of Psychiatry, University of California, San Diego, La Jolla, CA 92093;cDepartment of Neurosciences, University of California, San Diego, La Jolla, CA 92093;dDepartment of Psychology, University of California, San Diego, La Jolla, CA 92093
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  • For correspondence: cnsmith@ucsd.edulsquire@ucsd.edu
  1. Contributed by Larry R. Squire, October 10, 2018 (sent for review August 28, 2018; reviewed by Elizabeth Kensinger and Ken A. Paller)

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Significance

Knowledge (or awareness) of what has been learned has been described as a key feature of hippocampus-dependent memory or as unhelpful for understanding hippocampal function. We recorded eye movements while memory-impaired patients with hippocampal lesions and controls viewed familiar scenes or familiar scenes that had been altered. Controls preferentially looked at the altered regions of the scenes, but only when they knew what had changed and where the change occurred. Patients had difficulty distinguishing altered and unaltered scenes and, overall, did not direct their viewing toward the altered regions. Nonetheless, they did exhibit this effect on the few occasions when they were aware of the change. The results indicate the importance of conscious awareness for understanding hippocampal function.

Abstract

We explored the relationship between memory performance and conscious knowledge (or awareness) of what has been learned in memory-impaired patients with hippocampal lesions or larger medial temporal lesions. Participants viewed familiar scenes or familiar scenes where a change had been introduced. Patients identified many fewer of the changes than controls. Across all of the scenes, controls preferentially directed their gaze toward the regions that had been changed whenever they had what we term robust knowledge about the change: They could identify that a change occurred, report what had changed, and indicate where the change occurred. Preferential looking did not occur when they were unaware of the change or had only partial knowledge about it. The patients, overall, did not direct their gaze toward the regions that had been changed, but on the few occasions when they had robust knowledge about the change they (like controls) did exhibit this effect. Patients did not exhibit this effect when they were unaware of the change or had partial knowledge. The findings support the idea that awareness of what has been learned is a key feature of hippocampus-dependent memory.

  • declarative memory
  • medial temporal lobe
  • eye movements
  • amnesia

Footnotes

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

  • Reviewers: E.K., Boston College; and K.A.P., Northwestern University.

  • The authors declare no conflict of interest.

Published under the PNAS license.

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Awareness of what is learned as a characteristic of hippocampus-dependent memory
Christine N. Smith, Larry R. Squire
Proceedings of the National Academy of Sciences Nov 2018, 115 (47) 11947-11952; DOI: 10.1073/pnas.1814843115

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Awareness of what is learned as a characteristic of hippocampus-dependent memory
Christine N. Smith, Larry R. Squire
Proceedings of the National Academy of Sciences Nov 2018, 115 (47) 11947-11952; DOI: 10.1073/pnas.1814843115
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