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PMID: 11425920 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Energy hypometabolism in posterior cingulate cortex of Alzheimer's patients: superficial laminar cytochrome oxidase associated with disease duration.

Valla J, Berndt JD, Gonzalez-Lima F

Abstract

Among brain regions affected in Alzheimer's disease (AD), the posterior cingulate shows the earliest and largest decrement in energy metabolism. Positron emission tomography (PET) studies have shown that these decrements appear before the onset of memory deficits or other symptoms in persons at genetic risk for AD. This study compares in vivo imaging results and in situ postmortem analyses by examining the posterior cingulate (area 23) in 15 AD patients and 13 age-matched nondemented controls using quantitative cytochrome oxidase histochemistry as an intracellular measure of oxidative energy metabolic capacity. Each of the six layers of the posterior cingulate demonstrated a decline in cytochrome oxidase activity in AD relative to controls, whereas adjacent motor cortex showed no significant differences. This decrement did not appear to be mainly secondary to nonspecific decrement in mitochondrial enzymes, oxidative stress, cell loss, or histopathology. The cytochrome oxidase decrement was most severe in the superficial layer I (-39%), which demonstrated a correlation to disease duration. Covariance analyses suggest that superficial laminas undergo a functional uncoupling from the deeper layers of posterior cingulate cortex in AD, whereas no such effects are found in motor cortex or controls. These findings expand on previous results from PET studies by illuminating the layer-specific cytochrome oxidase contributions to energy hypometabolism. The findings suggest a decrement of cytochrome oxidase in posterior cingulate cortex, with progressive reduction within the superficial laminas linked to disease duration. Such decrement could contribute to some of the behavioral symptoms displayed by AD patients. This decrement appeared greater in women.

MeSH Terms
Age Factors Aged Aged, 80 and over Alzheimer Disease/metabolism,pathology Cell Count Cytochrome-c Oxidase Deficiency Disease Progression Electron Transport Complex IV/metabolism Energy Metabolism Female Gyrus Cinguli/metabolism,pathology Heme Oxygenase (Decyclizing)/metabolism Heme Oxygenase-1 Histocytochemistry Humans Immunohistochemistry Male Membrane Proteins Motor Cortex/metabolism,pathology Sex Factors Succinate Dehydrogenase/metabolism
Chemicals
Membrane Proteins HMOX1 protein, human Heme Oxygenase (Decyclizing) Heme Oxygenase-1 Succinate Dehydrogenase Electron Transport Complex IV
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Valla J
Institute for Neuroscience and Department of Psychology, University of Texas at Austin, Austin, Texas 78712, USA.
Berndt J D
Gonzalez-Lima F
References (44)
44 references, click to expand
  1. Quantitative cytochemistry of cytochrome oxidase and cellular morphometry of the human inferior colliculus in control and Alzheimer's patients.
    Brain Res. 1997 Mar 28;752(1-2):117-26 PMID: 9106447
  2. Preclinical prediction of Alzheimer's disease using SPECT.
    Neurology. 1998 Jun;50(6):1563-71 PMID: 9633695
  3. The Consortium to Establish a Registry for Alzheimer's Disease (CERAD). Part II. Standardization of the neuropathologic assessment of Alzheimer's disease.
    Neurology. 1991 Apr;41(4):479-86 PMID: 2011243
  4. Distribution of cerebral degeneration in Alzheimer's disease. A clinico-pathological study.
    Arch Psychiatr Nervenkr (1970). 1976 Dec 31;223(1):15-33 PMID: 828039
  5. Age-related differences in neural activity during memory encoding and retrieval: a positron emission tomography study.
    J Neurosci. 1997 Jan 1;17(1):391-400 PMID: 8987764
  6. Neuronal activity and early neurofibrillary tangles in Alzheimer's disease.
    Ann Neurol. 1996 Sep;40(3):411-20 PMID: 8797530
  7. Regional brain effects of sodium azide treatment on cytochrome oxidase activity: a quantitative histochemical study.
    Metab Brain Dis. 1995 Dec;10(4):303-20 PMID: 8847994
  8. Longitudinal evaluation of early Alzheimer's disease using brain perfusion SPECT.
    J Nucl Med. 2000 Jul;41(7):1155-62 PMID: 10914904
  9. Evolution of neuronal changes in the course of Alzheimer's disease.
    J Neural Transm Suppl. 1998;53:127-40 PMID: 9700651
  10. Posterior cingulate cortex in Alzheimer's disease.
    Lancet. 1994 Sep 24;344(8926):895 PMID: 7916431
  11. Multivariate analysis of laminar patterns of neurodegeneration in posterior cingulate cortex in Alzheimer's disease.
    Exp Neurol. 1998 Sep;153(1):8-22 PMID: 9743563
  12. Noninvasive assessment of changes in cytochrome-c oxidase oxidation in human subjects during visual stimulation.
    J Cereb Blood Flow Metab. 1999 Jun;19(6):592-603 PMID: 10366189
  13. Cytochrome oxidase activity in the auditory system of the mouse: a qualitative and quantitative histochemical study.
    Neuroscience. 1994 Nov;63(2):559-78 PMID: 7891865
  14. Cytochrome oxidase deficiency in Alzheimer's disease.
    Neurology. 1990 Aug;40(8):1302-3 PMID: 2166249
  15. Preclinical evidence of Alzheimer's disease in persons homozygous for the epsilon 4 allele for apolipoprotein E.
    N Engl J Med. 1996 Mar 21;334(12):752-8 PMID: 8592548
  16. Rates and risk factors for dementia and Alzheimer's disease: results from EURODEM pooled analyses. EURODEM Incidence Research Group and Work Groups. European Studies of Dementia.
    Neurology. 1999 Jan 1;52(1):78-84 PMID: 9921852
  17. Cytochrome oxidase inhibition: a novel animal model of Alzheimer's disease.
    J Geriatr Psychiatry Neurol. 1992 Apr-Jun;5(2):93-101 PMID: 1317179
  18. Chronic sodium azide treatment impairs learning of the Morris water maze task.
    Behav Neural Biol. 1992 Jul;58(1):72-5 PMID: 1417674
  19. Marked and variable inhibition by chemical fixation of cytochrome oxidase and succinate dehydrogenase in single motoneurons.
    J Histochem Cytochem. 1989 Jun;37(6):899-901 PMID: 2542395
  20. No association between Alzheimer plaques and decreased levels of cytochrome oxidase subunit mRNA, a marker of neuronal energy metabolism.
    Brain Res Mol Brain Res. 1998 Aug 15;59(1):13-21 PMID: 9729244
  21. Reduced platelet cytochrome c oxidase activity in Alzheimer's disease.
    Neurology. 1994 Jun;44(6):1086-90 PMID: 8208406
  22. Oxidative phosphorylation diseases and mitochondrial DNA mutations: diagnosis and treatment.
    Annu Rev Nutr. 1994;14:535-68 PMID: 7946532
  23. Demonstration of decreased posterior cingulate perfusion in mild Alzheimer's disease by means of H215O positron emission tomography.
    Eur J Nucl Med. 1997 Jun;24(6):670-3 PMID: 9169576
  24. Regional pattern of degeneration in Alzheimer's disease: neuronal loss and histopathological grading.
    Histopathology. 1981 Sep;5(5):549-64 PMID: 7286917
  25. Network analysis of positron emission tomography regional cerebral blood flow data: ensemble inhibition during episodic memory retrieval.
    J Neurosci. 1996 Jun 1;16(11):3753-9 PMID: 8642418
  26. Decreased brain protein levels of cytochrome oxidase subunits in Alzheimer's disease and in hereditary spinocerebellar ataxia disorders: a nonspecific change?
    J Neurochem. 1999 Feb;72(2):700-7 PMID: 9930743
  27. Loss of neurons in the nucleus basalis of Meynert in Alzheimer's disease, paralysis agitans and Korsakoff's Disease.
    Acta Neuropathol. 1983;61(2):101-8 PMID: 6637393
  28. Metabolic reduction in the posterior cingulate cortex in very early Alzheimer's disease.
    Ann Neurol. 1997 Jul;42(1):85-94 PMID: 9225689
  29. Assessment of cerebral blood flow in Alzheimer's disease by spin-labeled magnetic resonance imaging.
    Ann Neurol. 2000 Jan;47(1):93-100 PMID: 10632106
  30. Heme oxygenase-1 is associated with the neurofibrillary pathology of Alzheimer's disease.
    Am J Pathol. 1994 Jul;145(1):42-7 PMID: 8030754
  31. Electron transport chain defects in Alzheimer's disease brain.
    Neurology. 1994 Jun;44(6):1090-6 PMID: 8208407
  32. Regional glucose metabolic abnormalities are not the result of atrophy in Alzheimer's disease.
    Neurology. 1998 Jun;50(6):1585-93 PMID: 9633698
  33. Quantitative analysis of a vulnerable subset of pyramidal neurons in Alzheimer's disease: I. Superior frontal and inferior temporal cortex.
    J Comp Neurol. 1990 Nov 1;301(1):44-54 PMID: 2127598
  34. Cytochrome oxidase: an endogenous metabolic marker for neuronal activity.
    Trends Neurosci. 1989 Mar;12(3):94-101 PMID: 2469224
  35. Quantitative mapping of cytochrome oxidase activity in the central auditory system of the gerbil: a study with calibrated activity standards and metal-intensified histochemistry.
    Brain Res. 1994 Oct 10;660(1):34-49 PMID: 7828000
  36. Neglect after cingulectomy.
    Neurology. 1973 Sep;23(9):1003-7 PMID: 4199186
  37. Impairment in mitochondrial cytochrome oxidase gene expression in Alzheimer disease.
    Brain Res Mol Brain Res. 1994 Jul;24(1-4):336-40 PMID: 7968373
  38. Hypofunction in the posterior cingulate gyrus correlates with disorientation for time and place in Alzheimer's disease.
    J Neurol Neurosurg Psychiatry. 1998 Apr;64(4):552-4 PMID: 9576555
  39. Are sex and educational level independent predictors of dementia and Alzheimer's disease? Incidence data from the PAQUID project.
    J Neurol Neurosurg Psychiatry. 1999 Feb;66(2):177-83 PMID: 10071096
  40. Functional alterations in Alzheimer's disease: diminution of cytochrome oxidase in the hippocampal formation.
    J Neuropathol Exp Neurol. 1993 Nov;52(6):580-5 PMID: 8229076
  41. The effects of aging on layer 1 in area 46 of prefrontal cortex in the rhesus monkey.
    Cereb Cortex. 1998 Dec;8(8):671-84 PMID: 9863695
  42. Induction of heme oxygenase-1 mRNA and protein in neocortex and cerebral vessels in Alzheimer's disease.
    J Neurochem. 1995 Sep;65(3):1399-402 PMID: 7543935
  43. Oxidative metabolism in cultured fibroblasts derived from sporadic Alzheimer's disease (AD) patients.
    Neurosci Lett. 1997 Oct 24;236(1):13-6 PMID: 9404940
  44. Cerebral metabolic and cognitive decline in persons at genetic risk for Alzheimer's disease.
    Proc Natl Acad Sci U S A. 2000 May 23;97(11):6037-42 PMID: 10811879
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2001-07-01
Pages
4923-30
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6762373
Subset
IM
Grants
NIMH NIH HHS · MH/NS 31862 · United States
NINDS NIH HHS · R01 NS37755 · United States
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