Decreased meta-memory is associated with early tauopathy in cognitively unimpaired older adults

doi:10.1016/j.nicl.2019.102097

. 2019:24:102097.

doi: 10.1016/j.nicl.2019.102097. Epub 2019 Nov 18.

Decreased meta-memory is associated with early tauopathy in cognitively unimpaired older adults

Affiliations

¹ Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA 02114, USA; Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02115, USA; Center for Alzheimer Research and Treatment, Department of Neurology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA. Electronic address: patrizia@bwh.harvard.edu.
² Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02115, USA.
³ Department of Radiology, Division of Molecular Imaging and Nuclear Medicine, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA 02114, USA.
⁴ Department of Psychiatry, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA 02114, USA; Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02115, USA.
⁵ Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02115, USA; Center for Alzheimer Research and Treatment, Department of Neurology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA.
⁶ Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA 02114, USA; Department of Radiology, Division of Molecular Imaging and Nuclear Medicine, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA 02114, USA; Department of Neurology, Cliniques Universitaires Saint-Luc, Institute of Neurosciences, Université Catholique de Louvain, 10 Av. Hippocrate, 1200 Brussels, Belgium.
⁷ Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA 02114, USA; Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02115, USA.
⁸ Icahn School of Medicine at Mount Sinai, New York, USA.
⁹ Berenson-Allen Center for Noninvasive Brain Stimulation and Cognitive Neurology Unit, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA 02115, USA; Institut Guttmann, Universitat Autonoma, Barcelona, Spain.
¹⁰ Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02115, USA; Center for Alzheimer Research and Treatment, Department of Neurology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA; Department of Radiology, Division of Molecular Imaging and Nuclear Medicine, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA 02114, USA.
¹¹ Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA 02114, USA; Department of Psychiatry, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA 02114, USA; Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02115, USA; Center for Alzheimer Research and Treatment, Department of Neurology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA.

PMID: 31795044
PMCID: PMC6879982
DOI: 10.1016/j.nicl.2019.102097

Decreased meta-memory is associated with early tauopathy in cognitively unimpaired older adults

Patrizia Vannini et al. Neuroimage Clin. 2019.

. 2019:24:102097.

doi: 10.1016/j.nicl.2019.102097. Epub 2019 Nov 18.

Affiliations

¹ Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA 02114, USA; Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02115, USA; Center for Alzheimer Research and Treatment, Department of Neurology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA. Electronic address: patrizia@bwh.harvard.edu.
² Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02115, USA.
³ Department of Radiology, Division of Molecular Imaging and Nuclear Medicine, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA 02114, USA.
⁴ Department of Psychiatry, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA 02114, USA; Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02115, USA.
⁵ Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02115, USA; Center for Alzheimer Research and Treatment, Department of Neurology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA.
⁶ Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA 02114, USA; Department of Radiology, Division of Molecular Imaging and Nuclear Medicine, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA 02114, USA; Department of Neurology, Cliniques Universitaires Saint-Luc, Institute of Neurosciences, Université Catholique de Louvain, 10 Av. Hippocrate, 1200 Brussels, Belgium.
⁷ Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA 02114, USA; Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02115, USA.
⁸ Icahn School of Medicine at Mount Sinai, New York, USA.
⁹ Berenson-Allen Center for Noninvasive Brain Stimulation and Cognitive Neurology Unit, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA 02115, USA; Institut Guttmann, Universitat Autonoma, Barcelona, Spain.
¹⁰ Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02115, USA; Center for Alzheimer Research and Treatment, Department of Neurology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA; Department of Radiology, Division of Molecular Imaging and Nuclear Medicine, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA 02114, USA.
¹¹ Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA 02114, USA; Department of Psychiatry, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA 02114, USA; Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02115, USA; Center for Alzheimer Research and Treatment, Department of Neurology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA.

PMID: 31795044
PMCID: PMC6879982
DOI: 10.1016/j.nicl.2019.102097

Abstract

The ability to accurately judge memory efficiency (meta-memory monitoring) for newly learned (episodic) information, is decreased in older adults and even worse in Alzheimer's disease (AD), whereas no differences have been found for semantic meta-memory. The pathological substrates of this phenomenon are poorly understood. Here, we examine the association between meta-memory monitoring for episodic and semantic information to the two major proteinopathies in AD: amyloid (Aβ) and tau pathology in a group of cognitively unimpaired older adults. All participants underwent multi-tracer PET and meta-memory monitoring was assessed using a feeling-of-knowing (FOK) task for non-famous (episodic) and famous (semantic) face-name pairs. Whole brain voxel-wise correlations between meta-memory and PET data were conducted (controlling for memory), as well as confirmatory region-of-interest analyses. Participants had reduced episodic FOK compared to semantic FOK. Decreased episodic FOK was related to tauopathy in the medial temporal lobe regions, including the entorhinal cortex and temporal pole, whereas decreased semantic FOK was related to increased tau in regions associated with the semantic knowledge network. No association was found with Aβ-pathology. Alterations in the ability to accurately judge memory efficiency (in the absence of memory decline) may be a sensitive clinical indicator of AD pathophysiology in the pre-symptomatic phase.

Keywords: Alzheimer's disease; Amyloid; Feeling-of-knowing; Meta-memory; Tau.

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Conflict of interest statement

None.

Figures

**Fig. 1**
Relative accuracy of FOK judgements for episodic and semantic information

**Fig. 2**
The association between tau pathology and meta-memory accuracy.

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References

1. Allen-Burge R., Storandt M. Age equivalence in feeling-of-knowing experiences. J. Gerontol. B Psychol. Sci. Soc. Sci. 2000;55:214–223. - PubMed
1. Anderson J.W., Edgecomb S. Mild cognitive impairment and feeling-of-knowing in episodic memory. J. Clin. Exp. Neuropsychol. 2010;32:505–514. - PubMed
1. Babinski M.J. Contibution a l’etudedes troubles mantaux dans l’hemiplegie organique cerebrale (Anasognosie) Rev. Neurol. 1914;12:845–848.
1. Bäckman L., Karlsson T. The relation between level of general knowledge and feeling-of-knowing: an adult age study. Scand. J. Psychol. 1985;26:249–258. - PubMed
1. Backman L., Lipinska L. Monitoring of general knowledge: evidence for preservation in early Alzheimer's disease. Neuropsychologia. 1993;31:335–345. - PubMed

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[1] Allen-Burge R., Storandt M. Age equivalence in feeling-of-knowing experiences. J. Gerontol. B Psychol. Sci. Soc. Sci. 2000;55:214–223. - PubMed

[2] Allen-Burge R., Storandt M. Age equivalence in feeling-of-knowing experiences. J. Gerontol. B Psychol. Sci. Soc. Sci. 2000;55:214–223. - PubMed

[3] Anderson J.W., Edgecomb S. Mild cognitive impairment and feeling-of-knowing in episodic memory. J. Clin. Exp. Neuropsychol. 2010;32:505–514. - PubMed

[4] Anderson J.W., Edgecomb S. Mild cognitive impairment and feeling-of-knowing in episodic memory. J. Clin. Exp. Neuropsychol. 2010;32:505–514. - PubMed

[5] Babinski M.J. Contibution a l’etudedes troubles mantaux dans l’hemiplegie organique cerebrale (Anasognosie) Rev. Neurol. 1914;12:845–848.

[6] Babinski M.J. Contibution a l’etudedes troubles mantaux dans l’hemiplegie organique cerebrale (Anasognosie) Rev. Neurol. 1914;12:845–848.

[7] Bäckman L., Karlsson T. The relation between level of general knowledge and feeling-of-knowing: an adult age study. Scand. J. Psychol. 1985;26:249–258. - PubMed

[8] Bäckman L., Karlsson T. The relation between level of general knowledge and feeling-of-knowing: an adult age study. Scand. J. Psychol. 1985;26:249–258. - PubMed

[9] Backman L., Lipinska L. Monitoring of general knowledge: evidence for preservation in early Alzheimer's disease. Neuropsychologia. 1993;31:335–345. - PubMed

[10] Backman L., Lipinska L. Monitoring of general knowledge: evidence for preservation in early Alzheimer's disease. Neuropsychologia. 1993;31:335–345. - PubMed

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Decreased meta-memory is associated with early tauopathy in cognitively unimpaired older adults

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Decreased meta-memory is associated with early tauopathy in cognitively unimpaired older adults

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