Insulin resistance and medial prefrontal gyrus metabolism in women receiving hormone therapy

Psychiatry Research - Neuroimaging

Volumn 223, Issue 1, 2014, Pages 28-36

  Rasgon, Natalie L ^a   Kenna, Heather A ^a   Wroolie, Tonita E ^a   Williams, Katherine E ^a   DeMuth, Bevin N ^a   Silverman, Daniel H S ^b  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Dementia; Hormone therapy; Insulin resistance; Medial prefrontal gyrus; Menopause

Indexed keywords

CONJUGATED ESTROGEN; ESTRADIOL; FLUORODEOXYGLUCOSE; GLUCOSE; INSULIN; PROGESTERONE;

ADULT; AGED; ARTICLE; BRAIN METABOLISM; BRAIN REGION; CLINICAL ARTICLE; COGNITIVE DEFECT; COHORT ANALYSIS; CONTROLLED STUDY; DEMENTIA; FEMALE; FOLLOW UP; GLUCOSE METABOLISM; HOMEOSTASIS; HOMEOSTATIC ASSESSMENT OF INSULIN RESISTANCE; HORMONAL THERAPY; HUMAN; INSULIN BLOOD LEVEL; INSULIN RESISTANCE; MEDIAL PREFRONTAL GYRUS; MENTAL PERFORMANCE; MIDDLE FRONTAL GYRUS; POSITRON EMISSION TOMOGRAPHY; POST HOC ANALYSIS; POSTMENOPAUSE; PRIORITY JOURNAL; RISK ASSESSMENT; WORKING MEMORY;

DEMENTIA; HORMONE THERAPY; INSULIN RESISTANCE; MEDIAL PREFRONTAL GYRUS; MENOPAUSE;

AGED; ESTROGEN REPLACEMENT THERAPY; ESTROGENS; FEMALE; FOLLOW-UP STUDIES; GYRUS CINGULI; HOMEOSTASIS; HUMANS; INSULIN RESISTANCE; MIDDLE AGED; MODELS, BIOLOGICAL; NEUROPSYCHOLOGICAL TESTS; POSITRON-EMISSION TOMOGRAPHY; POSTMENOPAUSE; PREFRONTAL CORTEX; PROGESTERONE; RISK FACTORS;

EID: 84902077160     PISSN: 09254927     EISSN: 18727506     Source Type: Journal    
DOI: 10.1016/j.pscychresns.2014.04.004     Document Type: Article

References (84)

1. Anderer P., Saletu B., Saletu-Zyhlarz G., Gruber D., Metka M., Huber J., Pascual-Marqui R.D. Brain regions activated during an auditory discrimination task in insomniac postmenopausal patients before and after hormone replacement therapy: low-resolution brain electromagnetic tomography applied to event-related potentials. Neuropsychobiology 2004, 49:134-153.
2. Alzheimer's disease facts and figures. Alzheimer's & Dementia 2009, 5:234-270. Alzheimer's Association.
3. Baker L.D., Cross D.J., Minoshima S., Belongia D., Watson G.S., Craft S. Insulin resistance and Alzheimer-like reductions in regional cerebral glucose metabolism for cognitively normal adults with prediabetes or early type 2 diabetes. Archives of Neurology 2011, 68:51-57.
4. Ballesteros S., Mayas J., Reales J.M. Cognitive function in normal aging and in older adults with mild cognitive impairment. Psicothema 2013, 25:18-24.
5. Berent-Spillson A., Persad C.C., Love T., Tkaczyk A., Wang H., Reame N.K., Frey K.A., Zubieta J.K., Smith Y.R. Early menopausal hormone use influences brain regions used for visual working memory. Menopause 2010, 17:692-699.
6. Birdsill A.C., Carlsson C.M., Willette A.A., Okonkwo O.C., Johnson S.C., Xu G., Oh J.M., Gallagher C.L., Koscik R.L., Jonaitis E.M., Hermann B.P., LaRue A., Rowley H.A., Asthana S., Sager M.A., Bendlin B.B. Low cerebral blood flow is associated with lower memory function in metabolic syndrome. Obesity 2013, 21:1313-1320.
7. Brann D., Dhandapani K., Wakade C., Mahesh V., Khan M. Neurotrophic and neuroprotective actions of estrogen: basic mechanisms and clinical implications. Steroids 2007, 72:381-405.
8. Bruehl H., Sweat V., Hassenstab J., Polyakov V., Convit A. Cognitive impairment in nondiabetic middle-aged and older adults is associated with insulin resistance. Journal of Clinical and Experimental Neuropsychology 2010, 32:487-493.
9. Buschke H., Fuld P. Evaluating storage, retention, and retrieval in disordered memory and learning. Neurology 1974, 24:1019-1025.
10. Caetano M.S., Horst N.K., Harenberg L., Liu B., Arnsten A.F., Laubach M. Lost in transition: aging-related changes in executive control by the medial prefrontal cortex. Journal of Neuroscience 2012, 32:3765-3777.
11. Chang Y.M., Rosene D.L., Killiany R.J., Mangiamele L.A., Luebke J.I. Increased action potential firing rates of layer 2/3 pyramidal cells in the prefrontal cortex are significantly related to cognitive performance in aged monkeys. Cerebral Cortex 2005, 15:409-418.
12. Chisholm N.C., Packard A.R., Koss W.A., Juraska J.M. The effects of long-term treatment with estradiol and medroxyprogesterone acetate on tyrosine hydroxylase fibers and neuron number in the medial prefrontal cortex of aged female rats. Endocrinology 2012, 153:4874-4882.
13. Craft S. Insulin resistance syndrome and Alzheimer disease: pathophysiologic mechanisms and therapeutic implications. Alzheimer Disease and Associated Disorders 2006, 20:298-301.
14. Craft S. The role of metabolic disorders in Alzheimer disease and vascular dementia: two roads converged. Archives of Neurology 2009, 66:300-305.
15. Craft S., Asthana S., Cook D., Baker L., Cherrier M., Purganan K., Wait C., Petrova A., Latendresse S., Watson G., Newcomer J., Schellenberg G., Krohn A. Insulin dose-response effects on memory and plasma amyloid precursor protein in Alzheimer's disease: interactions with apolipoprotein E genotype. Psychoneuroendocrinology 2003, 28:809-822.
16. Craft S., Asthana S., Schellenberg G., Baker L., Cherrier M., Boyt A., Martins R., Raskind M., Peskind E., Plymate S. Insulin effects on glucose metabolism, memory, and plasma amyloid precursor protein in Alzheimer's disease differ according to apolipoprotein-E genotype. Annals of the New York Academy of Sciences 2000, 903:222-228.
17. Craft S., Baker L.D., Montine T.J., Minoshima S., Watson G.S., Claxton A., Arbuckle M., Callaghan M., Tsai E., Plymate S.R., Green P.S., Leverenz J., Cross D., Gerton B. Intranasal insulin therapy for Alzheimer disease and amnestic mild cognitive impairment: a pilot clinical trial. Archives of Neurology 2012, 69:29-38.
18. Craft S., Dagogo-Jack S., Wiethop B., Murphy C., Nevins R., Fleischman S., Rice V., Newcomer J., Cryer P. Effects of hyperglycemia on memory and hormone levels in dementia of the Alzheimer type: a longitudinal study. Behavioral Neuroscience 1993, 107:926-940.
19. Craft S., Watson G. Insulin and neurodegenerative disease: shared and specific mechanisms. Lancet Neurology 2004, 3:169-178.
20. D'Elia L., Satz P. Color Trails 1 & 2 1993, Psychological Assessment Resources, Inc, Orlando, FL.
21. Delis D., Kaplan E., Kramer J. Delis-Kaplan Executive Function System (D-KEFS) 2001, Harcourt Assessment, Inc., San Antonio, TX.
22. Espeland M.A., Tindle H.A., Bushnell C.A., Jaramillo S.A., Kuller L.H., Margolis K.L., Mysiw W.J., Maldjian J.A., Melhem E.R., Resnick S.M. Brain volumes, cognitive impairment, and conjugated equine estrogens. Journals of Gerontology Series A: Biological Sciences and Medical Sciences 2009, 64:1243-1250.
23. Ferrannini E., Mari A. How to measure insulin sensitivity. Journal of Hypertension 1998, 16:895-906.
24. Folstein M., Folstein S., McHugh P. "Mini-mental state": a practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research 1975, 12:189-198.
25. Friston K., Holmes A., Worsley K., Poline J., Frith C., Frackowiak R. Statistical parametric maps in functional imaging: a general linear approach. Human Brain Mapping 1995, 2:189-210.
26. Golden S.H., Kim C., Barrett-Connor E., Nan B., Kong S., Goldberg R. The association of elective hormone therapy with changes in lipids among glucose intolerant postmenopausal women in the diabetes prevention program. Metabolism: Clinical and Experimental 2013, 62(9):1313-1322.
27. Goldstein B.J. Insulin resistance as the core defect in type 2 diabetes mellitus. The American Journal of Cardiology 2002, 90:3G-10G.
28. Hamilton M. A rating scale for depression. Journal of Neurology, Neurosurgery, and Psychiatry 1960, 23:56-62.
29. Hänninen T., Hallikainen M., Koivisto K., Helkala E., Reinikainen K., Soininen H., Mykkänen L., Laakso M., Pyörälä K., Riekkinen P.J. A follow-up study of age-associated memory impairment: neuropsychological predictors of dementia. Journal of the American Geriatric Society 1995, 43:1007-1015.
30. Hempel R., Onopa R., Convit A. Type 2 diabetes affects hippocampus volume differentially in men and women. Diabetes and Metabolism Research Reviews 2012, 28:76-83.
31. Henderson V.W., Popat R.A. Effects of endogenous and exogenous estrogen exposures in midlife and late-life women on episodic memory and executive functions. Neuroscience 2011, 191:129-138.
32. Hermans M.P., Levy J.C., Morris R.J., Turner R.C. Comparison of insulin sensitivity tests across a range of glucose tolerance from normal to diabetes. Diabetologia 1999, 42:678-687.
33. IBM Corp. Released 2013. IBM SPSS Statistics for Windows, Version 22.0. IBM Corporation, Armonk, NY.
34. Joffe H., Hall J., Gruber S., Sarmiento I., Cohen L., Yurgelun-Todd D., Martin K. Estrogen therapy selectively enhances prefrontal cognitive processes: a randomized, double-blind, placebo-controlled study with functional magnetic resonance imaging in perimenopausal and recently postmenopausal women. Menopause 2006, 13:411-422.
35. Kaczorowski C.C., Davis S.J., Moyer J.R. Aging redistributes medial prefrontal neuronal excitability and impedes extinction of trace fear conditioning. Neurobiology of Aging 2012, 33:1744-1757.
36. Karakelides H., Nair K.S. Sarcopenia of aging and its metabolic impact. Current Topics in Developmental Biology 2005, 68:123-148.
37. Kenna H., Hoeft F., Kelley R., Wroolie T., DeMuth B., Reiss A., Rasgon N. Fasting plasma insulin and the default mode network in women at risk for Alzheimer's disease. Neurobiology of Aging 2013, 34:641-649.
38. Kenna H.A., Rasgon N.L., Geist C., Small G., Silverman D. Thalamo-basal ganglia connectivity in postmenopausal women receiving estrogen therapy. Neurochemical Research 2009, 34:234-237.
39. Kugaya A., Epperson C., Zoghbi S., van Dyck C., Hou Y., Fujita M., Staley J., Garg P., Seibyl J., Innis R. Increase in prefrontal cortex serotonin 2 A receptors following estrogen treatment in postmenopausal women. American Journal of Psychiatry 2003, 160:1522-1524.
40. Liddell M., Williams J., Bayer A., Kaiser F., Owen M. Confirmation of association between the e4 allele of apolipoprotein E and Alzheimer's disease. Journal of Medical Genetics 1994, 31:197-200.
41. Liu M.1, Kelley M.H., Herson P.S., Hurn P.D. Neuroprotection of sex steroids. Minerva Endocrinol. 2010, 35(2):127-143.
42. Lord C., Engert V., Lupien S.J., Pruessner J.C. Effect of sex and estrogen therapy on the aging brain: a voxel-based morphometry study. Menopause 2010, 17:846-851.
43. Luine V., Frankfurt M. Interactions between estradiol, BDNF and dendritic spines in promoting memory. Neuroscience 2013, 239:34-45.
44. Maki P.M., Dennerstein L., Clark M., Guthrie J., LaMontagne P., Fornelli D., Little D., Henderson V.W., Resnick S.M. Perimenopausal use of hormone therapy is associated with enhanced memory and hippocampal function later in life. Brain Research 2011, 1379:232-243.
45. Malykhin N., Vahidy S., Michielse S., Coupland N., Camicioli R., Seres P., Carter R. Structural organization of the prefrontal white matter pathways in the adult and aging brain measured by diffusion tensor imaging. Brain Structure & Function 2011, 216:417-431.
46. Matthews D., Hosker J., Rudenski A., Naylor B., Treacher D., Turner R. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 1985, 28:412-419.
47. Milner B. Disorders of learning and memory after temporal lobe lesions in man. Clin. Neurosurg. 1972, 19:421-446.
48. Osterrieth P. Le test de copie d'une figure complex: contribution a l'etude de la perception et de la memoire. Archives de Psychologie 1944, 30:286-356.
49. 18F]2-Fluoro-2-deoxy-d-glucose positron emission tomography demonstration of estrogen negative and positive feedback on luteinizing hormone secretion in women. Journal of Clinical Endocrinology and Metabolism 2008, 93:3208-3214.
50. Polkowski K., Mazurek A. Biological properties of genistein. A review of in vitro and vivo data. Acta Poloniae Pharmaceutica 2000, 57:135-155.
51. Profenno L.A., Porsteinsson A.P., Faraone S.V. Meta-analysis of Alzheimer's disease risk with obesity, diabetes, and related disorders. Biological Psychiatry 2010, 67:505-512.
52. Rapoport S.I., Horwitz B., Grady C.L., Haxby J.V., DeCarli C., Schapiro M.B. Abnormal brain glucose metabolism in Alzheimer's disease, as measured by position emission tomography. Advances in Experimental Medicine and Biology 1991, 291:231-248.
53. Rasgon N., Small G., Giddarth P., Miller K., Ercoli L., Bookheimer S., Lavretsky H., Huang S., Barrio J., Phelps M. Estrogen use and brain metabolic change in older adults. A preliminary report. Psychiatry Research: Neuroimaging 2001, 107:11-18.
54. Rasgon N.L., Geist C.L., Kenna H.A., Wroolie T.E., Williams K.E., Silverman D.H.S. A prospective randomized trial to assess the effects of discontinuation of hormone therapy on cerebral function in postmenopausal women at risk for dementia. PLoS One 2014, 9(3):e89095.
55. Rasgon N.L., Kenna H.A., Wroolie T.E., Kelley R., Silverman D., Brooks J., Williams K.E., Powers B.N., Hallmayer J., Reiss A. Insulin resistance and hippocampal volume in women at risk for Alzheimer's disease. Neurobiology of Aging 2011, 32:1942-1948.
56. Rasgon N.L., Silverman D., Siddarth P., Miller K., Ercoli L.M., Elman S., Lavretsky H., Huang S.C., Phelps M.E., Small G.W. Estrogen use and brain metabolic change in postmenopausal women. Neurobiology of Aging 2005, 26:229-235.
57. Resnick S.M., Espeland M.A., Jaramillo S.A., Hirsch C., Stefanick M.L., Murray A.M., Ockene J., Davatzikos C. Postmenopausal hormone therapy and regional brain volumes: the WHIMS-MRI study. Neurology 2009, 72:135-142.
58. Saglam K. Insulin resistance and postmenopausal hormone replacement therapy. Metabolic Syndrome and Related Disorders 2004, 2:234-240.
59. Sakurai T., Iimuro S., Araki A., Umegaki H., Ohashi Y., Yokono K., Ito H. Age-associated increase in abdominal obesity and insulin resistance, and usefulness of AHA/NHLBI definition of metabolic syndrome for predicting cardiovascular disease in Japanese elderly with type 2 diabetes mellitus. Gerontology 2010, 56:141-149.
60. Salat D.H., Kaye J.A., Janowsky J.S. Prefrontal gray and white matter volumes in healthy aging and Alzheimer disease. Archives of Neurology 1999, 56:338-344.
61. Salat D.H., Tuch D.S., Greve D.N., van der Kouwe A.J., Hevelone N.D., Zaleta A.K., Rosen B.R., Fischl B., Corkin S., Rosas H.D., Dale A.M. Age-related alterations in white matter microstructure measured by diffusion tensor imaging. Neurobiology of Aging 2005, 26:1215-1227.
62. Schioth H.B., Craft S., Brooks S.J., Frey W.H., Benedict C. Brain insulin signaling and Alzheimer's disease: current evidence and future directions. Molecular Neurobiology 2012, 46:4-10.
63. Shaywitz S., Shaywitz B., Pugh K., Fulbright R., Skudlarski P., Mencl W., Constable R., Naftolin F., Palter S., Marchione K., Katz L., Shankweiler D., Fletcher J., Lacadie C., Keltz M., Gore J. Effect of estrogen on brain activation patterns in postmenopausal women during working memory tasks. Journal of the American Medical Association 1999, 281:1197-1202.
64. Shumaker S.A., Legault C., Rapp S.R., Thal L., Wallace R.B., Ockene J.K., Hendrix S.L., Jones B.N., Assaf A.R., Jackson R.D., Kotchen J.M., Wassertheil-Smoller S., Wactawski-Wende J. Estrogen plus progestin and the incidence of dementia and mild cognitive impairment in postmenopausal women: the Women's Health Initiative Memory Study: a randomized controlled trial. Journal of the American Medical Association 2003, 289:2651-2662.
65. Silverman D., Dy C., Castellon S., Lai J., Pio B., Abraham L., Waddell K., Petersen L., Phelps M., Ganz P. Altered frontocortical, cerebellar, and basal ganglia activity in adjuvant-treated breast cancer survivors 5-10 years after chemotherapy. Breast Cancer Research and Treatment 2007, 103:303-311.
66. Silverman D., Munakata J., Ennes H., Mandelkern M., Hoh C., Mayer E. Regional cerebral activity in normal and pathological perception of visceral pain. Gastroenterology 1997, 112:64-72.
67. Silverman D.H., Geist C.L., Kenna H.A., Williams K., Wroolie T., Powers B., Brooks J., Rasgon N.L. Differences in regional brain metabolism associated with specific formulations of hormone therapy in postmenopausal women at risk for AD. Psychoneuroendocrinology 2011, 36:502-513.
68. Small G., La Rue A., Komo S., Kaplan A., Mandelkern M. Predictors of cognitive change in middle-aged and older adults with memory loss. American Journal of Psychiatry 1995, 152:1757-1764.
69. Smith Y.R., Bowen L., Love T.M., Berent-Spillson A., Frey K.A., Persad C.C., Reame N.K., Koeppe R.A., Zubieta J.K. Early initiation of hormone therapy in menopausal women is associated with increased hippocampal and posterior cingulate cholinergic activity. Journal of Clinical Endocrinology and Metabolism 2011, 96:E1761-1770.
70. Strachan M.W., Reynolds R.M., Frier B.M., Mitchell R.J., Price J.F. The relationship between type 2 diabetes and dementia. British Medical Bulletin 2008, 88:131-146.
71. Sumino H., Ichikawa S., Itoh H., Utsugi T., Ohyama Y., Umeda M., Nakamura T., Kanda T., Mizunuma H., Tomono S., Murakami M., Kurabayashi M. Hormone replacement therapy decreases insulin resistance and lipid metabolism in Japanese postmenopausal women with impaired and normal glucose tolerance. Hormone Research 2003, 60:134-142.
72. Suzuki S., Brown C., Wise P. Mechanisms of neuroprotection by estrogen. Endocrine 2006, 29:209-215.
73. Benton Visual Retention Test-Fifth Edition 1992, The Psychological Corporation, Harcourt Brace and Company, San Antonio, TX.
74. Wechsler Abbreviated Scale of Intelligence 1997, The Psychological Corporation, Harcourt Brace & Company, San Antonio, TX.
75. Wechsler Adult Intelligence Scale-3rd Edition (WAIS-III) 1997, The Psychological Corporation, Harcourt Brace & Company, San Antonio, TX.
76. Wechsler Abbreivated Scale of Intelligence (WASI) 1999, The Psychological Corporation, Harcourt Brace & Company, San Antonio, TX.
77. Tai Y., Lin K.-P., Hoh C., Huang S., Hoffman E. Utilization of 3-D elastic transformation in registration of chest X-ray CT and whole body PET. IEEE Translational Nuclear Science 1997, 4.
78. Tchernof A., Calles-Escandon J., Sites C.K., Poehlman E.T. Menopause, central body fatness, and insulin resistance: effects of hormone-replacement therapy. Coronary Artery Disease 1998, 9:503-511.
79. Vanitallie T.B. Preclinical sporadic Alzheimer's disease: target for personalized diagnosis and preventive intervention. Metabolism: Clinical and Experimental 2013, 62(1):S30-33.
80. Vincent A., Fitzpatrick L. Soy isoflavones: are they useful in menopause?. Mayo Clinic Proceedings 2000, 75:1174-1184.
81. Wahrenberg H., Hertel K., Leijonhufvud B.M., Persson L.G., Toft E., Arner P. Use of waist circumference to predict insulin resistance: retrospective study. British Medical Journal 2005, 330:1363-1364.
82. Wellcome Trust Center for Neuroimaging. Released 2009. SPM2. London, United Kingdom.
83. Willette A.A., Xu G., Johnson S.C., Birdsill A.C., Jonaitis E.M., Sager M.A., Hermann B.P., La Rue A., Asthana S., Bendlin B.B. Insulin resistance, brain atrophy, and cognitive performance in late middle-aged adults. Diabetes Care 2013, 36:443-449.
84. Wroolie T.E., Kenna H.A., Williams K.E., Powers B.N., Holcomb M., Khaylis A., Rasgon NL. Differences in verbal memory performance in postmenopausal women receiving hormone therapy: 17β-estradiol versus conjugated equine estrogens. Am. J. Geriatr. Psychiatry. 2011, 19(9):792-802.