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March 26, 2013; 80 (13) Article

Neural reserve, neuronal density in the locus ceruleus, and cognitive decline

Robert S. Wilson, Sukriti Nag, Patricia A. Boyle, Loren P. Hizel, Lei Yu, Aron S. Buchman, Julie A. Schneider, David A. Bennett
First published March 13, 2013, DOI: https://doi.org/10.1212/WNL.0b013e3182897103
Robert S. Wilson
From the Rush Alzheimer's Disease Center and Departments of Neurological Sciences (R.S.W., L.Y., A.S.B., J.A.S., D.A.B.), Behavioral Sciences (R.S.W., P.A.B.), and Pathology (S.N., J.A.S.), Rush University Medical Center (L.P.H.), Chicago, IL.
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Sukriti Nag
From the Rush Alzheimer's Disease Center and Departments of Neurological Sciences (R.S.W., L.Y., A.S.B., J.A.S., D.A.B.), Behavioral Sciences (R.S.W., P.A.B.), and Pathology (S.N., J.A.S.), Rush University Medical Center (L.P.H.), Chicago, IL.
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Patricia A. Boyle
From the Rush Alzheimer's Disease Center and Departments of Neurological Sciences (R.S.W., L.Y., A.S.B., J.A.S., D.A.B.), Behavioral Sciences (R.S.W., P.A.B.), and Pathology (S.N., J.A.S.), Rush University Medical Center (L.P.H.), Chicago, IL.
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Loren P. Hizel
From the Rush Alzheimer's Disease Center and Departments of Neurological Sciences (R.S.W., L.Y., A.S.B., J.A.S., D.A.B.), Behavioral Sciences (R.S.W., P.A.B.), and Pathology (S.N., J.A.S.), Rush University Medical Center (L.P.H.), Chicago, IL.
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Lei Yu
From the Rush Alzheimer's Disease Center and Departments of Neurological Sciences (R.S.W., L.Y., A.S.B., J.A.S., D.A.B.), Behavioral Sciences (R.S.W., P.A.B.), and Pathology (S.N., J.A.S.), Rush University Medical Center (L.P.H.), Chicago, IL.
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Aron S. Buchman
From the Rush Alzheimer's Disease Center and Departments of Neurological Sciences (R.S.W., L.Y., A.S.B., J.A.S., D.A.B.), Behavioral Sciences (R.S.W., P.A.B.), and Pathology (S.N., J.A.S.), Rush University Medical Center (L.P.H.), Chicago, IL.
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Julie A. Schneider
From the Rush Alzheimer's Disease Center and Departments of Neurological Sciences (R.S.W., L.Y., A.S.B., J.A.S., D.A.B.), Behavioral Sciences (R.S.W., P.A.B.), and Pathology (S.N., J.A.S.), Rush University Medical Center (L.P.H.), Chicago, IL.
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David A. Bennett
From the Rush Alzheimer's Disease Center and Departments of Neurological Sciences (R.S.W., L.Y., A.S.B., J.A.S., D.A.B.), Behavioral Sciences (R.S.W., P.A.B.), and Pathology (S.N., J.A.S.), Rush University Medical Center (L.P.H.), Chicago, IL.
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Citation
Neural reserve, neuronal density in the locus ceruleus, and cognitive decline
Robert S. Wilson, Sukriti Nag, Patricia A. Boyle, Loren P. Hizel, Lei Yu, Aron S. Buchman, Julie A. Schneider, David A. Bennett
Neurology Mar 2013, 80 (13) 1202-1208; DOI: 10.1212/WNL.0b013e3182897103

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Abstract

Objective: To test the hypothesis that higher neuronal density in brainstem aminergic nuclei contributes to neural reserve.

Methods: Participants are 165 individuals from the Rush Memory and Aging Project, a longitudinal clinical–pathologic cohort study. They completed a mean of 5.8 years of annual evaluations that included a battery of 19 cognitive tests from which a previously established composite measure of global cognition was derived. Upon death, they had a brain autopsy and uniform neuropathologic examination that provided estimates of the density of aminergic neurons in the locus ceruleus, dorsal raphe nucleus, substantia nigra, and ventral tegmental area plus summary measures of neuronal neurofibrillary tangles and Lewy bodies from these nuclei and medial temporal lobe and neocortex.

Results: Neuronal densities in each nucleus were approximately normally distributed. In separate analyses, higher neuronal density in each nucleus except the ventral tegmental area was associated with slower rate of cognitive decline, but when modeled together only locus ceruleus neuronal density was related to cognitive decline (estimate = 0.003, SE = 0.001, p < 0.001). Higher densities of tangles and Lewy bodies in these brainstem nuclei were associated with faster cognitive decline even after controlling for pathologic burden elsewhere in the brain. Locus ceruleus neuronal density, brainstem tangles, and brainstem Lewy bodies had independent associations with rate of cognitive decline. In addition, at higher levels of locus ceruleus neuronal density, the association of Lewy bodies with cognitive decline was diminished.

Conclusion: Density of noradrenergic neurons in the locus ceruleus may be a structural component of neural reserve.

GLOSSARY

AD=
Alzheimer disease

Footnotes

  • Go to Neurology.org for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • Editorial, page 1180

  • See page 1194

  • Received September 26, 2012.
  • Accepted November 26, 2012.
  • © 2013 American Academy of Neurology
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