Hippocampal neurochemicals are associated with exercise group and intensity, psychological health, and general cognition in older adults

GeroScience - Tập 45 Số 3 - Trang 1667-1685
Line Skarsem Reitlo1, Jelena Mihailovic2, Dorthe Stensvold3, Ulrik Wisløff3, Fahmeed Hyder2, Asta Håberg4
1Department of Neuromedicine and Movement Science, Faculty of Medicine and Health Sciences, Norwegian University of Science and Technology, Trondheim, Norway
2Department of Radiology and Biomedical Imaging, Yale University, New Haven, CT, USA
3Department of Circulation and Medical Imaging, Faculty of Medicine and Health Sciences, Norwegian University of Science and Technology, Trondheim, Norway
4Department of Radiology and Nuclear Medicine, St. Olavs hospital, Trondheim University Hospital, Trondheim, Norway

Tóm tắt

AbstractBased on the premise that physical activity/exercise impacts hippocampal structure and function, we investigated if hippocampal metabolites for neuronal viability and cell membrane density (i.e., N-acetyl aspartate (NAA), choline (Cho), creatine (Cr)) were higher in older adults performing supervised exercise compared to following national physical activity guidelines. Sixty-three participants (75.3 ± 1.9 years after 3 years of intervention) recruited from the Generation 100 study (NCT01666340_date:08.16.2012) were randomized into a supervised exercise group (SEG) performing twice weekly moderate- to high-intensity training, and a control group (CG) following national physical activity guidelines of ≥ 30-min moderate physical activity ≥ 5 days/week. Hippocampal body and head volumes and NAA, Cho, and Cr levels were acquired at 3T with magnetic resonance imaging and spectroscopic imaging. Sociodemographic data, peak oxygen uptake (VO2peak), exercise characteristics, psychological health, and cognition were recorded. General linear models were used to assess group differences and associations corrected for age, sex, education, and hippocampal volume. Both groups adhered to their training, where SEG trained at higher intensity. SEG had significantly lower NAA/Cr in hippocampal body than CG (p = 0.04). Across participants, higher training intensity was associated with lower Cho/Cr in hippocampal body (p < 0.001). Change in VO2peak, increasing VO2peak from baseline to 3 years, or VO2peak at 3 years were not associated with hippocampal neurochemicals. Lower NAA/Cr in hippocampal body was associated with poorer psychological health and slightly higher cognitive scores. Thus, following the national physical activity guidelines and not training at the highest intensity level were associated with the best neurochemical profile in the hippocampus at 3 years.

Từ khóa


Tài liệu tham khảo

Barnes DE, Yaffe K. The projected effect of risk factor reduction on Alzheimer’s disease prevalence. Lancet Neurol. 2011;10(9):819–28. https://doi.org/10.1016/S1474-4422(11)70072-2.

Laurin D, Verreault R, Lindsay J, et al. Physical activity and risk of cognitive impairment and dementia in elderly persons. Arch Neurol. 2001;58(3):498–504. https://doi.org/10.1001/archneur.58.3.498.

Livingston G, Huntley J, Sommerlad A, et al. Dementia prevention, intervention, and care: 2020 report of the Lancet Commission. Lancet. 2020;396(10248):413–46. https://doi.org/10.1016/S0140-6736(20)30367-6.

Norton S, Matthews FE, Barnes DE, et al. Potential for primary prevention of Alzheimer’s disease: an analysis of population-based data. Lancet Neurol. 2014;13(8):788–94. https://doi.org/10.1016/S1474-4422(14)70136-X.

Arba F, Quinn T, Hankey G, et al. Cerebral small vessel disease, medial temporal lobe atrophy and cognitive status in patients with ischaemic stroke and transient ischaemic attack. Eur J Neurol. 2017;24(2):276–82. https://doi.org/10.1111/ene.13191.

Domingos C, Pêgo J, Santos N. Effects of physical activity on brain function and structure in older adults: a systematic review. Behav Brain Res. 2021;402:113061. https://doi.org/10.1016/j.bbr.2020.113061.

Niemann C, Godde B, Voelcker-Rehage C. Not only cardiovascular, but also coordinative exercise increases hippocampal volume in older adults. Front Aging Neurosci. 2014;6:170. https://doi.org/10.3389/fnagi.2014.00170.

Wu A, Sharrett AR, Gottesman RF, et al. Association of brain magnetic resonance imaging signs with cognitive outcomes in persons with nonimpaired cognition and mild cognitive impairment. JAMA Netw Open. 2019;2(5):e193359–e193359. https://doi.org/10.1001/jamanetworkopen.2019.3359.

Bhattacharya TK, Pence BD, Ossyra JM, et al. Exercise but not (–)-epigallocatechin-3-gallate or β-alanine enhances physical fitness, brain plasticity, and behavioral performance in mice. Physiol Behav. 2015;145:29–37. https://doi.org/10.1016/j.physbeh.2015.03.023.

Brockett AT, LaMarca EA, Gould E. Physical exercise enhances cognitive flexibility as well as astrocytic and synaptic markers in the medial prefrontal cortex. PLoS ONE. 2015;10(5):e0124859. https://doi.org/10.1371/journal.pone.0124859.

Kim T-W, Choi H-H, Chung Y-R. Treadmill exercise alleviates impairment of cognitive function by enhancing hippocampal neuroplasticity in the high-fat diet-induced obese mice. J Exerc Rehabil. 2016;12(3):156. https://doi.org/10.12965/jer.1632644.322.

Vilela TC, Muller AP, Damiani AP, et al. Strength and aerobic exercises improve spatial memory in aging rats through stimulating distinct neuroplasticity mechanisms. Mol Neurobiol. 2017;54(10):7928–37. https://doi.org/10.1007/s12035-016-0272-x.

Park H-S, Kim C-J, Kwak H-B, et al. Physical exercise prevents cognitive impairment by enhancing hippocampal neuroplasticity and mitochondrial function in doxorubicin-induced chemobrain. Neuropharmacology. 2018;133:451–61. https://doi.org/10.1016/j.neuropharm.2018.02.013.

Erickson KI, Voss MW, Prakash RS, et al. Exercise training increases size of hippocampus and improves memory. Proc Natl Acad Sci U S A. 2011;108(7):3017–22. https://doi.org/10.1073/pnas.1015950108.

Maass A, Düzel S, Goerke M, et al. Vascular hippocampal plasticity after aerobic exercise in older adults. Mol Psychiatry. 2015;20(5):585–93. https://doi.org/10.1038/mp.2014.114.

Rosano C, Guralnik J, Pahor M, et al. Hippocampal response to a 24-month physical activity intervention in sedentary older adults. Am J Geriatr Psychiatry. 2017;25(3):209–17. https://doi.org/10.1016/j.jagp.2016.11.007.

Wilckens KA, Stillman CM, Waiwood AM, et al. Exercise interventions preserve hippocampal volume: A meta-analysis. Hippocampus. 2021;31(3):335–47. https://doi.org/10.1002/hipo.23292.

Jonasson LS, Nyberg L, Kramer AF, et al. Aerobic exercise intervention, cognitive performance, and brain structure: results from the Physical Influences on Brain in Aging (PHIBRA) study. Front Aging Neurosci. 2016;8:336. https://doi.org/10.3389/fnagi.2016.00336.

Matura S, Fleckenstein J, Deichmann R, et al. Effects of aerobic exercise on brain metabolism and grey matter volume in older adults: results of the randomised controlled SMART trial. Transl Psychiatry. 2017;7(7):e1172–e1172. https://doi.org/10.1038/tp.2017.135.

Pani J, Reitlo LS, Evensmoen HR, et al. Effect of 5 years of exercise intervention at different intensities on brain structure in older adults from the general population: a generation 100 substudy. Clin Interv Aging. 2021;16:1485. https://doi.org/10.2147/CIA.S318679.

Scheewe TW, van Haren NE, Sarkisyan G, et al. Exercise therapy, cardiorespiratory fitness and their effect on brain volumes: a randomised controlled trial in patients with schizophrenia and healthy controls. Eur Neuropsychopharmacol. 2013;23(7):675–85. https://doi.org/10.1016/j.euroneuro.2012.08.008.

Stephen R, Liu Y, Ngandu T, et al. Brain volumes and cortical thickness on MRI in the Finnish Geriatric Intervention Study to Prevent Cognitive Impairment and Disability (FINGER). Alzheimers Res Ther. 2019;11(1):1–10. https://doi.org/10.1186/s13195-019-0506-z.

Venkatraman VK, Sanderson A, Cox KL, et al. Effect of a 24-month physical activity program on brain changes in older adults at risk of Alzheimer’s disease: the AIBL active trial. Neurobiol Aging. 2020;89:132–41. https://doi.org/10.1016/j.neurobiolaging.2019.02.030.

Wagner G, Herbsleb M, Fdl Cruz, et al. Hippocampal structure, metabolism, and inflammatory response after a 6-week intense aerobic exercise in healthy young adults: a controlled trial. J Cereb Blood Flow Metab. 2015;35(10):1570–8. https://doi.org/10.1038/jcbfm.2015.125.

Colcombe S, Kramer AF. Fitness effects on the cognitive function of older adults: a meta-analytic study. Psychol Sci. 2003;14(2):125–30. https://doi.org/10.1111/1467-9280.t01-1-01430.

Smith PJ, Blumenthal JA, Hoffman BM, et al. Aerobic exercise and neurocognitive performance: a meta-analytic review of randomized controlled trials. Psychosom Med. 2010;72(3):239. https://doi.org/10.1097/PSY.0b013e3181d14633.

Young J, Angevaren M, Rusted J, et al. Aerobic exercise to improve cognitive function in older people without known cognitive impairment. Cochrane Database Syst Rev 2015;(4):CD005381. https://doi.org/10.1002/14651858.CD005381.pub4.

Sokołowski DR, Hansen TI, Rise HH, et al. 5 years of exercise intervention did not benefit cognition compared to the physical activity guidelines in older adults, but higher cardiorespiratory fitness did. A generation 100 substudy. Front. Aging Neurosci. 2021;13:742587. https://doi.org/10.3389/fnagi.2021.742587.

Block W, Jessen F, Träber F, et al. Regional N-acetylaspartate reduction in the hippocampus detected with fast proton magnetic resonance spectroscopic imaging in patients with Alzheimer disease. Arch Neurol. 2002;59(5):828–34. https://doi.org/10.1001/archneur.59.5.828.

Targosz-Gajniak MG, Siuda JS, Wicher MM, et al. Magnetic resonance spectroscopy as a predictor of conversion of mild cognitive impairment to dementia. J Neurol Sci. 2013;335(1–2):58–63. https://doi.org/10.1016/j.jns.2013.08.023.

Schuff N, Amend DL, Knowlton R, et al. Age-related metabolite changes and volume loss in the hippocampus by magnetic resonance spectroscopy and imaging☆. Neurobiol Aging. 1999;20(3):279–85. https://doi.org/10.1016/s0197-4580(99)00022-6.

Morrison JH, Hof PR. Life and death of neurons in the aging brain. Science. 1997;278(5337):412–9. https://doi.org/10.1126/science.278.5337.412.

Ross AJ, Sachdev PS. Magnetic resonance spectroscopy in cognitive research. Brain Res Rev. 2004;44(2–3):83–102. https://doi.org/10.1016/j.brainresrev.2003.11.001.

Gonzales MM, Tarumi T, Kaur S, et al. Aerobic fitness and the brain: increased N-acetyl-aspartate and choline concentrations in endurance-trained middle-aged adults. Brain Topogr. 2013;26(1):126–34. https://doi.org/10.1007/s10548-012-0248-8.

Stensvold, Viken H, Rognmo O, et al. A randomised controlled study of the long-term effects of exercise training on mortality in elderly people: study protocol for the Generation 100 study. BMJ Open. 2015;5(2):e007519. https://doi.org/10.1136/bmjopen-2014-007519.

Greene SJ, Killiany RJ, Initiative AsDN. Hippocampal subregions are differentially affected in the progression to Alzheimer’s disease. Anat Rec: Adv Integr Anat Evol Biol. 2012;295(1):132–40. https://doi.org/10.1002/ar.21493.

Scheenen TW, Klomp DW, Wijnen JP, et al. Short echo time 1H-MRSI of the human brain at 3T with minimal chemical shift displacement errors using adiabatic refocusing pulses. Magn Reson Med. 2008;59(1):1–6. https://doi.org/10.1002/mrm.21302.

Voss M. The chronic exercise-cognition interaction: fMRI research. In: T. McMorris. Editor. Exercise-cognition interaction. London: Elsevier Academic Press. 2016;187–209. https://doi.org/10.1016/B978-0-12-800778-5.00009-8.

Borg GA. Psychophysical bases of perceived exertion. Med Sci Sports Exerc. 1982;14(5):377–81.

Stensvold, Viken H, Steinshamn SL, et al. Effect of exercise training for five years on all cause mortality in older adults—the Generation 100 study: randomised controlled trial. BMJ. 2020;371:m3485. https://doi.org/10.1136/bmj.m3485.

Zigmond AS, Snaith RP. The hospital anxiety and depression scale. Acta Psychiatr Scand. 1983;67(6):361–70. https://doi.org/10.1111/j.1600-0447.1983.tb09716.x.

Mykletun A, Stordal E, Dahl AA. Hospital Anxiety and Depression (HAD) scale: factor structure, item analyses and internal consistency in a large population. Br J Psychiatry. 2001;179(6):540–4. https://doi.org/10.1192/bjp.179.6.540.

Haug TT, Mykletun A, Dahl AA. The association between anxiety, depression, and somatic symptoms in a large population: the HUNT-II study. Psychosom Med. 2004;66(6):845–51. https://doi.org/10.1097/01.psy.0000145823.85658.0c.

Bjerkeset O, Mykletun A, Dahl AA, et al. Mortality in relation to self-reported mixed anxiety and depression symptoms–The HUNT study. Nord J Psychiatry. 2007;61(1):6–11. https://doi.org/10.1080/08039480601121926.

Nasreddine ZS, Phillips NA, Bedirian V, et al. The Montreal cognitive assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc. 2005;53(4):695–9. https://doi.org/10.1111/j.1532-5415.2005.53221.x.

Stensvold D, Sandbakk SB, Viken H, et al. Cardiorespiratory Reference Data in Older Adults: The Generation 100 Study. Med Sci Sports Exerc. 2017;49(11):2206–15. https://doi.org/10.1249/mss.0000000000001343.

Gibbons RJ, Balady GJ, Beasley JW, et al. ACC/AHA guidelines for exercise testing. A report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines (Committee on Exercise Testing). J Am Coll Cardiol. 1997;30(1):260–311. https://doi.org/10.1016/s0735-1097(97)00150-2.

Fischl B. FreeSurfer. Neuroimage. 2012;62(2):774–81.

Cabanes E, Confort-Gouny S, Le Fur Y, et al. Optimization of residual water signal removal by HLSVD on simulated short echo time proton MR spectra of the human brain. J Magn Reson. 2001;150(2):116–25. https://doi.org/10.1006/jmre.2001.2318.

Provencher SW. Estimation of metabolite concentrations from localized in vivo proton NMR spectra. Magn Reson Med. 1993;30(6):672–9. https://doi.org/10.1002/mrm.1910300604.

Govindaraju V, Young K, Maudsley AA. Proton NMR chemical shifts and coupling constants for brain metabolites. NMR Biomed. 2000;13(3):129–53.

Wilson M, Davies NP, Sun Y, et al. A comparison between simulated and experimental basis sets for assessing short-TE in vivo 1H MRS data at 1.5 T. NMR Biomed. 2010;23(10):1117–26. https://doi.org/10.1002/nbm.1538.

Helms G. The principles of quantification applied to in vivo proton MR spectroscopy. Eur J Radiol. 2008;67(2):218–29. https://doi.org/10.1016/j.ejrad.2008.02.034.

Landheer K, Swanberg KM, Juchem C. Magnetic resonance Spectrum simulator (MARSS), a novel software package for fast and computationally efficient basis set simulation. NMR Biomed. 2021;34(5):e4129. https://doi.org/10.1002/nbm.4129.

Near J, Harris AD, Juchem C, et al. Preprocessing, analysis and quantification in single-voxel magnetic resonance spectroscopy: experts’ consensus recommendations. NMR Biomed. 2021;34(5):e4257. https://doi.org/10.1002/nbm.4257.

Hetherington H, Spencer D, Vaughan J, et al. Quantitative 31P spectroscopic imaging of human brain at 4 Tesla: assessment of gray and white matter differences of phosphocreatine and ATP. Magn Reson Med. 2001;45(1):46–52.

McLean MA, Woermann FG, Barker GJ, et al. Quantitative analysis of short echo time 1H-MRSI of cerebral gray and white matter. Magn Reson Med. 2000;44(3):401–11.

Träber F, Block W, Lamerichs R, et al. 1H metabolite relaxation times at 3.0 tesla: measurements of T1 and T2 values in normal brain and determination of regional differences in transverse relaxation. J Magn Reson Imaging. 2004;19(5):537–45. https://doi.org/10.1002/jmri.20053.

Kirov II, Fleysher L, Fleysher R, et al. Age dependence of regional proton metabolites T2 relaxation times in the human brain at 3 T. Magn Reson Med. 2008;60(4):790–5. https://doi.org/10.1002/mrm.21715.

Posse S, Otazo R, Caprihan A, et al. Proton echo-planar spectroscopic imaging of J-coupled resonances in human brain at 3 and 4 Tesla. Magn Reson Med. 2007;58(2):236–44. https://doi.org/10.1002/mrm.21287.

Mlynárik V, Gruber S, Moser E. Proton T 1 and T 2 relaxation times of human brain metabolites at 3 Tesla. NMR Biomed. 2001;14(5):325–31. https://doi.org/10.1002/nbm.713.

Cavassila S, Deval S, Huegen C, et al. Cramer-Rao bound expressions for parametric estimation of overlapping peaks: influence of prior knowledge. J Magn Reson. 2000;143(2):311–20. https://doi.org/10.1006/jmre.1999.2002.

Weston KS, Wisløff U, Coombes JS. High-intensity interval training in patients with lifestyle-induced cardiometabolic disease: a systematic review and meta-analysis. Br J Sports Med. 2014;48(16):1227–34. https://doi.org/10.1136/bjsports-2013-092576.

Murray ME, Przybelski SA, Lesnick TG, et al. Early Alzheimer’s disease neuropathology detected by proton MR spectroscopy. J Neurosci. 2014;34(49):16247–55. https://doi.org/10.1523/JNEUROSCI.2027-14.2014.

Frederiksen KS, Gjerum L, Waldemar G, et al. Effects of physical exercise on Alzheimer’s disease biomarkers: a systematic review of intervention studies. J Alzheimers Dis. 2018;61(1):359–72. https://doi.org/10.3233/JAD-170567.

Gogniat MA, Robinson TL, Miller LS. Exercise interventions do not impact brain volume change in older adults: a systematic review and meta-analysis. Neurobiol Aging. 2021;101:230–46. https://doi.org/10.1016/j.neurobiolaging.2021.01.025.

Firth J, Stubbs B, Vancampfort D, et al. Effect of aerobic exercise on hippocampal volume in humans: a systematic review and meta-analysis. Neuroimage. 2018;166:230–8. https://doi.org/10.1016/j.neuroimage.2017.11.007.

Loe H, Steinshamn S, Wisløff U. Cardio-respiratory reference data in 4631 healthy men and women 20–90 years: the HUNT 3 fitness study. PLoS ONE. 2014;9(11):e113884. https://doi.org/10.1371/journal.pone.0113884.

O’Keefe EL, Torres-Acosta N, O’Keefe JH, et al. Training for longevity: the reverse J-curve for exercise. Mo Med. 2020;117(4):355.

Storen O, Helgerud J, Saebo M, et al. The effect of age on the V O2max response to high-intensity interval training. Med Sci Sports Exerc. 2017;49(1):78–85. https://doi.org/10.1249/mss.0000000000001070.

Fock KM, Khoo J. Diet and exercise in management of obesity and overweight. J Gastroenterol Hepatol. 2013;28:59–63. https://doi.org/10.1111/jgh.12407.

Calverley TA, Ogoh S, Marley CJ, et al. HIITing the brain with exercise: mechanisms, consequences and practical recommendations. J Physiol. 2020;598(13):2513–30. https://doi.org/10.1113/JP275021.

Lucas SJ, Cotter JD, Brassard P, et al. High-intensity interval exercise and cerebrovascular health: curiosity, cause, and consequence. J Cereb Blood Flow Metab. 2015;35(6):902–11. https://doi.org/10.1038/jcbfm.2015.49.

Quistorff B, Secher NH, Van Lieshout JJ. Lactate fuels the human brain during exercise. FASEB J. 2008;22(10):3443–9. https://doi.org/10.1096/fj.08-106104.

Vestergaard MB, Jensen ML, Arngrim N, et al. Higher physiological vulnerability to hypoxic exposure with advancing age in the human brain. J Cereb Blood Flow Metab. 2020;40(2):341–53. https://doi.org/10.1177/0271678X18818291.

Inoue K, Okamoto M, Shibato J, et al. Long-term mild, rather than intense, exercise enhances adult hippocampal neurogenesis and greatly changes the transcriptomic profile of the hippocampus. PLoS ONE. 2015;10(6):e0128720. https://doi.org/10.1371/journal.pone.0128720.

Shih P-C, Yang Y-R, Wang R-Y. Effects of exercise intensity on spatial memory performance and hippocampal synaptic plasticity in transient brain ischemic rats. PLoS ONE. 2013;8(10):e78163. https://doi.org/10.1371/journal.pone.0078163.

Soya H, Mukai A, Deocaris CC, et al. Threshold-like pattern of neuronal activation in the hypothalamus during treadmill running: establishment of a minimum running stress (MRS) rat model. Neurosci Res. 2007;58(4):341–8. https://doi.org/10.1016/j.neures.2007.04.004.

Bjelland I, Dahl AA, Haug TT, et al. The validity of the Hospital Anxiety and Depression Scale: an updated literature review. J Psychosom Res. 2002;52(2):69–77. https://doi.org/10.1016/s0022-3999(01)00296-3.

Scherk H, Backens M, Schneider-Axmann T, et al. Neurochemical pathology in hippocampus in euthymic patients with bipolar I disorder. Acta Psychiatr Scand. 2008;117(4):283–8. https://doi.org/10.1111/j.1600-0447.2007.01142.x.

Ackl N, Ising M, Schreiber YA, et al. Hippocampal metabolic abnormalities in mild cognitive impairment and Alzheimer’s disease. Neurosci Lett. 2005;384(1–2):23–8. https://doi.org/10.1016/j.neulet.2005.04.035.

Liu Y, Cai Z-L, Xue S, et al. Proxies of cognitive reserve and their effects on neuropsychological performance in patients with mild cognitive impairment. J Clin Neurosci. 2013;20(4):548–53. https://doi.org/10.1016/j.jocn.2012.04.020.

Zotcheva E, Håberg AK, Wisløff U, et al. Effects of 5 years aerobic exercise on cognition in older adults: the Generation 100 study: a randomized controlled trial. Sports Med. 2022;52(7):1689–99. https://doi.org/10.1007/s40279-021-01608-5.

Borland E, Nägga K, Nilsson PM, et al. The Montreal cognitive assessment: normative data from a large Swedish population-based cohort. J Alzheimers Dis. 2017;59(3):893–901. https://doi.org/10.3233/JAD-170203.

Engedal K, Gjøra L, Bredholt T, et al. Sex differences on Montreal cognitive assessment and mini-mental state examination scores and the value of self-report of memory problems among community dwelling people 70 years and above: The HUNT Study. Dement Geriatr Cogn Disord. 2021;50(1):74–84. https://doi.org/10.1159/000516341.

Sun D, Zhang J, Fan Y, et al. Abnormal levels of brain metabolites may mediate cognitive impairment in stroke-free patients with cerebrovascular risk factors. Age Ageing. 2014;43(5):681–6. https://doi.org/10.1093/ageing/afu027.

Poppenk J, Evensmoen HR, Moscovitch M, et al. Long-axis specialization of the human hippocampus. Trends Cogn Sci. 2013;17(5):230–40. https://doi.org/10.1016/j.tics.2013.03.005.

Schuff N, Meyerhoff DJ, Mueller S, et al. N-acetylaspartate as a marker of neuronal injury in neurodegenerative disease. Adv Exp Med Biol. 2006;576:241–262; discussion 361–3. https://doi.org/10.1007/0-387-30172-0_17

Wang Z, Zhao C, Yu L, et al. Regional metabolic changes in the hippocampus and posterior cingulate area detected with 3-Tesla magnetic resonance spectroscopy in patients with mild cognitive impairment and Alzheimer disease. Acta Radiol. 2009;50(3):312–9. https://doi.org/10.1080/02841850802709219.

Modrego PJ, Fayed N. Longitudinal magnetic resonance spectroscopy as marker of cognitive deterioration in mild cognitive impairment. Am J Alzheimers Dis Other Demen. 2011;26(8):631–6. https://doi.org/10.1177/1533317511433809.

Kantarci K, Smith GE, Ivnik RJ, et al. 1H magnetic resonance spectroscopy, cognitive function, and apolipoprotein E genotype in normal aging, mild cognitive impairment and Alzheimer’s disease. J Int Neuropsychol Soc. 2002;8(7):934–42. https://doi.org/10.1017/s1355617702870084.

Griffith HR, Okonkwo OC, den Hollander JA, et al. Brain metabolic correlates of decision making in amnestic mild cognitive impairment. Aging Neuropsychol Cogn. 2010;17(4):492–504. https://doi.org/10.1080/13825581003646135.

Hansen BH, Anderssen SA, Steene-Johannessen J, et al. Fysisk aktivitet og sedat tid blant voksne og eldre i Norge—Nasjonal kartlegging 2014–2015. Helsedirektoratet. 2015. IS-2367. https://www.helsedirektoratet.no/rapporter/fysisk-aktivitet-kartleggingsrapporter/Fysisk%20aktivitet%20og%20sedat%20tid%20blant%20voksne%20og%20eldre%20i%20Norge.pdf/_/attachment/inline/7d460cdf-051a-4ecd-99d6-7ff8ee07cf06:eff5c93b46b28a3b1a4d2b548fc53b9f51498748/Fysisk%20aktivitet%20og%20sedat%20tid%20blant%20voksne%20og%20eldre%20i%20Norge.pdf

Walhovd KB, Fjell AM, Reinvang I, et al. Effects of age on volumes of cortex, white matter and subcortical structures. Neurobiol Aging. 2005;26(9):1261–70. https://doi.org/10.1016/j.neurobiolaging.2005.05.020.

Pintzka CW, Hansen TI, Evensmoen HR, et al. Marked effects of intracranial volume correction methods on sex differences in neuroanatomical structures: a HUNT MRI study. Front Neurosci. 2015;9:238. https://doi.org/10.3389/fnins.2015.00238.

Noble KG, Grieve SM, Korgaonkar MS, et al. Hippocampal volume varies with educational attainment across the life-span. Front Hum Neurosci. 2012;6:307. https://doi.org/10.3389/fnhum.2012.00307.

Geurts JJ, Barkhof F, Castelijns JA, et al. Quantitative 1H-MRS of healthy human cortex, hippocampus, and thalamus: metabolite concentrations, quantification precision, and reproducibility. J Magn Reson Imaging. 2004;20(3):366–71. https://doi.org/10.1002/jmri.20138.

Hammen T, Stadlbauer A, Tomandl B, et al. Short TE single-voxel 1H-MR spectroscopy of hippocampal structures in healthy adults at 1.5 Tesla—how reproducible are the results? NMR in Biomed. 2005;18(3):195–201. https://doi.org/10.1002/nbm.958.

Venkatraman TN, Hamer RM, Perkins DO, et al. Single-voxel 1H PRESS at 4.0 T: precision and variability of measurements in anterior cingulate and hippocampus. NMR Biomed. 2006;19(4):484–91. https://doi.org/10.1002/nbm.1055.

Kassem MN, Bartha R. Quantitative proton short-echo-time LASER spectroscopy of normal human white matter and hippocampus at 4 Tesla incorporating macromolecule subtraction. Magn Reson Med. 2003;49(5):918–27. https://doi.org/10.1002/mrm.10443.

Hsu Y-Y, Chen M-C, Lim K-E, et al. Reproducibility of hippocampal single-voxel proton MR spectroscopy and chemical shift imaging. Am J Roentgenol. 2001;176(2):529–36. https://doi.org/10.2214/ajr.176.2.1760529.

Griffith HR, den Hollander JA, Okonkwo O, et al. Executive function is associated with brain proton magnetic resonance spectroscopy in amnestic mild cognitive impairment. J Clin Exp Neuropsychol. 2007;29(6):599–609. https://doi.org/10.1080/13803390600826595.

Kantarci K, Petersen RC, Przybelski SA, et al. Hippocampal volumes, proton magnetic resonance spectroscopy metabolites, and cerebrovascular disease in mild cognitive impairment subtypes. Arch Neurol. 2008;65(12):1621–8. https://doi.org/10.1001/archneur.65.12.1621.

Koush Y, Rothman DL, Behar KL, et al. Human brain functional MRS reveals interplay of metabolites implicated in neurotransmission and neuroenergetics. J Cereb Blood Flow Metab. 2022;(6):911–934. https://doi.org/10.1177/0271678X221076570.

Arild A, Vangberg T, Nikkels H, et al. Five years of exercise intervention at different intensities and development of white matter hyperintensities in community dwelling older adults, a Generation 100 sub-study. Aging (Albany NY). 2022;14(2):596. https://doi.org/10.18632/aging.203843.

Thông tin
Thông tin xuất bản

GeroScience

Tập 45 Số 3

1667-1685

Thông tin tác giả