BDNF Responses in Healthy Older Persons to 35 Minutes of Physical Exercise, Cognitive Training, and Mindfulness: Associations with Working Memory Function

Journal of Alzheimer's Disease

Volumn 55, Issue 2, 2017, Pages 645-657

  Håkansson, Krister ^a,b,c   Ledreux, Aurélie ^d   Daffner, Kirk ^f   Terjestam, Yvonne ^a   Bergman, Patrick ^a   Carlsson, Roger ^a   Kivipelto, Miia ^b,c   Winblad, Bengt ^b   Granholm, Ann Charlotte ^d,e   Mohammed, Abdul Kadir H ^a,b  

^a LINNAEUS UNIVERSITY   (Sweden)

^b KAROLINSKA INSTITUTE   (Sweden)

^c STOCKHOLM UNIVERSITY   (Sweden)

^d MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^e UNIVERSITY OF DENVER   (United States)

^f MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Aging; brain derived neurotrophic factor; cognitive function; cognitive training; crossover design; exercise; geriatrics; intervention study; mindfulness; neuroplasticity

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR;

AGED; ARTICLE; COGNITION; CONTROLLED STUDY; EXERCISE; FEMALE; HUMAN; MALE; MINDFULNESS; NORMAL HUMAN; PHYSICAL ACTIVITY; PRIORITY JOURNAL; TRAINING; WORKING MEMORY; ANALYSIS OF VARIANCE; BLOOD; BRAIN; CROSSOVER PROCEDURE; HEALTHY AGING; METABOLISM; PHYSIOLOGY; PROCEDURES; SHORT TERM MEMORY; TEACHING; VERY ELDERLY;

AGED; AGED, 80 AND OVER; ANALYSIS OF VARIANCE; BRAIN; BRAIN-DERIVED NEUROTROPHIC FACTOR; COGNITION; CROSS-OVER STUDIES; EXERCISE; FEMALE; HEALTHY AGING; HUMANS; MALE; MEMORY, SHORT-TERM; MINDFULNESS; TEACHING;

EID: 84999114779     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-160593     Document Type: Article

References (78)

1. NybergL,Lövdén M, Riklund K, Lindenberger U,Bäckman L (2012) Memory aging and brain maintenance. Trends Cogn Sci 16, 292-305.
2. Cummings J (2004) Alzheimer's disease. N Engl J Med 351, 56-67.
3. Wimo A, Winblad B, Jonsson L (2010) The worldwide societal costs of dementia: Estimates for 2009. Alzheimers Dement 6, 98-103.
4. Deckers K, van Boxtel MPJ, Schiepers OJG, de Vugt M, Munoz Sanchez JL, Anstey KJ, Brayne C, Dartigues J-F, Engedal K, Kivipelto M, Ritchie K, Starr JM, Yaffe K, Irving K, Verhey FRJ, Köhler S (2015) Target risk factors for dementia prevention: A systematic review and Delphi consensus study on the evidence from observational studies. Int J Geriatr Psychiatry 30, 234-246.
5. Colcombe S, KramerAF(2003) Fitness effects on the cognitive function of older adults: A meta-analytic study. Psychol Sci 14, 125-130.
6. Hindin SB, Zelinski EM (2012) Extended practice and aerobic exercise interventions benefit untrained cognitive outcomes in older adults: A meta-analysis. J Am Geriatr Soc 60, 136-141.
7. Lampit A, Hallock H, Valenzuela M (2014) Computerized cognitive training in cognitively healthy older adults: A systematic review and meta-analysis of effect modifiers. PLoS Med 11, e1001756.
8. Rebok GW, Ball K, Guey LT, Jones RN, Kim H-Y, King JW, Marsiske M, Morris JN, Tennstedt SL, Unverzagt FW, Willis SL, ACTIVE Study Group (2014) Ten-year effects of the advanced cognitive training for independent and vital elderly cognitive training trial on cognition and everyday functioning in older adults. J Am Geriatr Soc 62, 16-24.
9. Daffner KR (2009) Promoting successful cognitive aging: A comprehensive review. J Alzheimers Dis 19, 1101-1122.
10. NganduT, Lehtisalo J, Solomon A, Levälahti E, Ahtiluoto S, Antikainen R, Bäckman L, Hänninen T, Jula A, Laatikainen T, Lindström J, Mangialasche F, Paajanen T, Pajala S, Peltonen M, Rauramaa R, Stigsdotter-Neely A, Strandberg T, Tuomilehto J, Soininen H, Kivipelto M (2015) A 2 year multidomain intervention of diet, exercise, cognitive training, and vascular risk monitoring versus control to prevent cognitive decline in at-risk elderly people (FINGER): A randomised controlled trial. Lancet 385, 2255-2263.
11. Rosenzweig MR (1966) Environmental complexity, cerebral change, and behavior. Am Psychol 21, 321-332.
12. Xu X, Ye L, Ruan Q (2009) Environmental enrichment induces synaptic structural modification after transient focal cerebral ischemia in rats. Exp Biol Med (Maywood) 234, 296-305.
13. Mohammed A, Zhu S, Darmopil S, Hjerling-Leffler J, Ernfors P, Winblad B, Diamond M, Eriksson P, Bogdanovic N (2002) Environmental enrichment and the brain. Prog Brain Res 138, 109-133.
14. Park DC, Bischof GN (2013) The aging mind: Neuroplasticity in response to cognitive training. Dialogues Clin Neurosci 15, 109-119.
15. Ickes BR, Pham TM, Sanders LA, Albeck DS, Mohammed AH, GranholmAC(2000) Long-term environmental enrichment leads to regional increases in neurotrophin levels in rat brain. Exp Neurol 164, 45-52.
16. Cotman CW, Berchtold NC (2002) Exercise: A behavioral intervention to enhance brain health and plasticity. Trends Neurosci 25, 295-301.
17. Branchi I, D'Andrea I, Sietzema J, Fiore M, Di Fausto V, Aloe L, Alleva E (2006) Early social enrichment augments adult hippocampal BDNF levels and survival of BrdUpositive cells while increasing anxiety-and "depression-" like behavior. J Neurosci Res 83, 965-973.
18. Agranoff BW, Cotman CW, Uhler MD (1999) Synaptic Plasticity as a Model for Learning and Memory Research, Lippincott-Raven, Philadelphia.
19. Neeper SA, Gomez-Pinilla F, Choi J, Cotman C (1995) Exercise and brain neurotrophins. Nature 373, 109-109.
20. Ieraci A, Mallei A, Musazzi L, Popoli M (2015) Physical exercise and acute restraint stress differentially modulate hippocampal brain-derived neurotrophic factor transcripts and epigenetic mechanisms in mice. Hippocampus 25, 1380-1392.
21. TokuyamaW, Okuno H, Hashimoto T, Xin Li Y, Miyashita Y (2000) BDNF upregulation during declarative memory formation in monkey inferior temporal cortex. Nat Neurosci 3, 1134-1142.
22. Yamada K, Mizuno M, Nabeshima T (2002) Role for brainderived neurotrophic factor in learning and memory. Life Sci 70, 735-744.
23. Rossi C, Angelucci A, Costantin L, Braschi C, Mazzantini M, Babbini F, Fabbri ME, Tessarollo L, Maffei L, Berardi N, Caleo M (2006) Brain-derived neurotrophic factor (BDNF) is required for the enhancement of hippocampal neurogenesis following environmental enrichment. Eur J Neurosci 24, 1850-1856.
24. Griesbach GS, Hovda DA, Gomez-Pinilla F (2009) Exercise-induced improvement in cognitive performance after traumatic brain injury in rats is dependent on BDNF activation. Brain Res 1288, 105-115.
25. Mu JS, Li WP, Yao ZB, Zhou XF (1999) Deprivation of endogenous brain-derived neurotrophic factor results in impairment of spatial learning and memory in adult rats. Brain Res 835, 259-265.
26. Lu B, Chow A (1999) Neurotrophins and hippocampal synaptic transmission and plasticity. J Neurosci Res 58, 76-87.
27. Zagrebelsky M, Korte M (2014) Form follows function: BDNF and its involvement in sculpting the function and structure of synapses. Neuropharmacology 76(Pt C), 628-638.
28. Waterhouse EG, An JJ, Orefice LL, Baydyuk M, Liao G-Y, Zheng K, Lu B,XuB(2012)BDNFpromotes differentiation and maturation of adult-born neurons through GABAergic transmission. J Neurosci 32, 14318-14330.
29. Lee J, Duan W, Mattson MP (2002) Evidence that brain-derived neurotrophic factor is required for basal neurogenesis and mediates, in part, the enhancement of neurogenesis by dietary restriction in the hippocampus of adult mice. J Neurochem 82, 1367-1375.
30. Scharfman H, Goodman J, Macleod A, Phani S, Antonelli C, Croll S (2005) Increased neurogenesis and the ectopic granule cells after intrahippocampalBDNFinfusion in adult rats. Exp Neurol 192, 348-356.
31. Taliaz D, Stall N, Dar DE, Zangen A (2009) Knockdown of brain-derived neurotrophic factor in specific brain sites precipitates behaviors associated with depression and reduces neurogenesis. Mol Psychiatry 15, 80-92.
32. Szuhany KL, Bugatti M, Otto MW (2015) A meta-analytic review of the effects of exercise on brain-derived neurotrophic factor. J Psychiatric Res 60, 56-64.
33. de Melo FG Coelho FG, Gobbi SS, Andreatto CAAC, Corazza DID, Pedroso RVR, Santos-Galduroz RFR (2012) Physical exercise modulates peripheral levels of brainderived neurotrophic factor (BDNF): A systematic review of experimental studies in the elderly. Arch Gerontol Geriatr 56, 10-15.
34. Laske C, Banschbach S, Stransky E, Bosch S, Straten G, Machann J, Fritsche A, Hipp A, Niess A, Eschweiler GW (2010) Exercise-induced normalization of decreased BDNF serum concentration in elderly women with remitted major depression. Int J Neuropsychopharmacol 13, 595-602.
35. Rasmussen P, Brassard P, Adser H, Pedersen MV, Leick L, Hart E, Secher NH, Pedersen BK, Pilegaard H (2009) Evidence for a release of brain-derived neurotrophic factor from the brain during exercise. Exp Physiol 94, 1062-1069.
36. Tsai C-L, Chen F-C, Pan C-Y,Wang C-H, Huang T-H, Chen T-C (2014) Impact of acute aerobic exercise and cardiorespiratory fitness on visuospatial attention performance and serum BDNF levels. Psychoneuroendocrinology 41, 121-131.
37. Lavretsky H, Epel ES, Siddarth P, Nazarian N, Cyr NS, Khalsa DS, Lin J, Blackburn E, Irwin MR (2013) A pilot study of yogic meditation for family dementia caregivers with depressive symptoms: Effects on mental health, cognition, and telomerase activity. Int J Geriatr Psychiatry 28, 57-65.
38. Fox KCR, Nijeboer S, Dixon ML, Floman JL, Ellamil M, Rumak SP, Sedlmeier P, Christoff K (2014) Is meditation associated with altered brain structure? A systematic review and meta-analysis of morphometric neuroimaging in meditation practitioners. Neurosci Biobehav Rev 43, 48-73.
39. Leckie RL, Oberlin LE,VossMW, Prakash RS, Szabo-Reed A, Chaddock-Heyman L, Phillips SM, Gothe NP, Mailey E, Vieira-Potter VJ, Martin SA, Pence BD, Lin M, Parasuraman R, Greenwood PM, Fryxell KJ,Woods JA,McAuley E, Kramer AF, Erickson KI (2014) BDNF mediates improvements in executive function following a 1-year exercise intervention. Front Hum Neurosci 8, 985.
40. Eyre HA, Acevedo B, Yang H, Siddarth P, Van Dyk K, Ercoli L, Leaver AM, Cyr NS, Narr K, Baune BT, Khalsa DS, Lavretsky H (2016) Changes in neural connectivity and memory following a yoga intervention for older adults: A pilot study. J Alzheimers Dis 52, 673-684.
41. O'Leary K, O'Neill S, Dockray S (2016) A systematic review of the effects of mindfulness interventions on cortisol. J Health Psychol 21, 2108-2121.
42. Lakshminarasimhan H, Chattarji S (2012) Stress leads to contrasting effects on the levels of brain derived neurotrophic factor in the hippocampus and amygdala. PLoS One 7, e30481.
43. Nettiksimmons J, Simonsick EM, Harris T, Satterfield S, Rosano C, Yaffe K, for the Health ABC Study (2014) The associations between serum brain-derived neurotrophic factor, potential confounders, and cognitive decline: A longitudinal study. PLoS One 9, e91339.
44. Komulainen P, Pedersen M, Hänninen T, Bruunsgaard H, Lakka TA, Kivipelto M, Hassinen M, Rauramaa TH, Pedersen BK, Rauramaa R (2008) BDNF is a novel marker of cognitive function in ageing women: The DR's EXTRA Study. Neurobiol Learn Mem 90, 596-603.
45. Angelucci F, Spalletta G, di Iulio F, Ciaramella A, Salani F, Colantoni L, Varsi AE, Gianni W, Sancesario G, Caltagirone C, Bossu P (2010) Alzheimer's disease (AD) and Mild Cognitive Impairment (MCI) patients are characterized by increased BDNF serum levels. Curr Alzheimer Res 7, 15-20.
46. Ziegenhorn AA, Schulte-Herbrüggen O, Danker-Hopfe H, Malbranc M, Hartung H-D, Anders D, Lang UE, Steinhagen-Thiessen E, Schaub RT, Hellweg R (2007) Serum neurotrophins-A study on the time course and influencing factors in a large old age sample. Neurobiol Aging 28, 1436-1445.
47. LaskeC, StranskyE,LeyheT, EschweilerGW(2006) Stagedependent BDNF serum concentrations in Alzheimer's disease. J Neural Transm 113, 1217-1224.
48. AronowWS (2015) Blood pressure goals and targets in the elderly. Curr Treat Options Cardiovasc Med 17, 394.
49. Qiu C, Strauss von E, Fastbom J, Winblad B, Fratiglioni L (2003) Lowblood pressure and risk of dementia in theKungsholmen project: A 6-year follow-up study. Arch Neurol 60, 223-228.
50. Folstein M, Folstein S, McHugh P (1975) "Mini-mental state." A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12, 189-198.
51. Borg G (1970) Perceived exertion as an indicator of somatic stress. Scand J Rehabil Med 2, 92-98.
52. Shinaver CS, Entwistle PC, Söderqvist S (2014) Cogmed WM training: Reviewing the reviews. Appl Neuropsychol Child 3, 163-172.
53. Kabat-Zinn J (2011) Some reflections on the origins of MBSR, skillful means, and the trouble with maps. Contemporary Buddhism 12, 281-306.
54. Giese M, Beck J, Brand S, Muheim F, Hemmeter U, Hatzinger M, Holsboer-Trachsler E, Eckert A (2014) Fast BDNF serum level increase and diurnal BDNF oscillations are associated with therapeutic response after partial sleep deprivation. J Psychiatric Res 59, 1-7.
55. Polacchini A, Metelli G, Francavilla R, Baj G, Florean M, Mascaretti LG, Tongiorgi E (2015) A method for reproducible measurements of serum BDNF: Comparison of the performance of six commercial assays. Sci Rep 5, 17989.
56. Lim Y, Zhong JH, Zhou XF (2015) Development of mature BDNF-specific sandwich ELISA. J Neurochem 134, 75-85.
57. Klein AB, Williamson R, Santini MA, Clemmensen C, Ettrup A, Rios M, Knudsen GM, Aznar S (2011) Blood BDNF concentrations reflect brain-tissue BDNF levels across species. The Int J Neuropsychopharmacol 14, 347-353.
58. Erickson KI, Voss MW, Prakash RS, Basak C, Szabo A, Chaddock L, Kim JS, Heo S, Alves H, White SM,Wojcicki TR, Mailey E, Vieira VJ, Martin SA, Pence BD,Woods JA, McAuley E, Kramer AF (2011) Exercise training increases size of hippocampus and improves memory. Proc Natl Acad Sci U S A 108, 3017-3022.
59. Cohen J (1988) Statistical Power Analysis for the Behavioral Sciences. 2nd edn., Lawrence Erlbaum Associates, Hillsdale, NJ.
60. Schuch FB, da Silveira LE, de Zeni TC, da Silva DP, Wollenhaupt-Aguiar B, Ferrari P, Reischak-Oliveira A, Kapczinski F (2015) Effects of a single bout of maximal aerobic exercise on BDNF in bipolar disorder: A gender-based response. Psychiat Res 229, 57-62.
61. Lommatzsch M, Zingler D, Schuhbaeck K, Schloetcke K, Zingler C, Schuff-Werner P, Virchow JC (2005) The impact of age, weight and gender on BDNF levels in human platelets and plasma. Neurobiol Aging 26, 115-123.
62. Trajkovska V, Marcussen AB, VinbergM, Hartvig P, Aznar S, Knudsen GM (2007) Measurements of brain-derived neurotrophic factor: Methodological aspects and demographical data. Brain Res Bull 73, 143-149.
63. Laske C, Stransky E, Leyhe T (2006) Decreased brain-derived neurotrophic factor (BDNF)-and betathromboglobulin (beta-TG)-blood levels in Alzheimer's disease. Thromb Haemost 96, 102-103.
64. Cho H-C, Kim J, Kim S, Son YH, Lee N, Jung SH (2012) The concentrations of serum, plasma and platelet BDNF are all increased by treadmill VO2max performance in healthy college men. Neurosci Lett 519, 78-83.
65. Heyman E, Gamelin FX, Goekint M, Piscitelli F, Roelands B, Leclair E, Di Marzo V, Meeusen R (2012) Intense exercise increases circulating endocannabinoid and BDNF levels in humans-Possible implications for reward and depression. Psychoneuroendocrinology 37, 844-851.
66. Rojas Vega S, HollmannW, VeraWahrmann B, Strüder HK (2012) pH buffering does not influence BDNF responses to exercise. Int J Sports Med 33, 8-12.
67. Winblad B, Amouyel P, Andrieu S, Ballard C, Brayne C, Brodaty H, Cedazo-Minguez A, Dubois B, Edvardsson D, Feldman H, Fratiglioni L, Frisoni GB, Gauthier S, Georges J, Graff C, Iqbal K, Jessen F, Johansson G, Jonsson L, Kivipelto M, Knapp M, Mangialasche F, Melis R, Nordberg A, Rikkert MO, Qiu C, Sakmar TP, Scheltens P, Schneider LS, Sperling R, Tjernberg LO, Waldemar G, Wimo A, Zetterberg H (2016) Defeating Alzheimer's disease and other dementias: A priority for European science and society. Lancet Neurol 15, 455-532.
68. Hall J, Thomas KL, Everitt BJ (2000) Rapid and selective induction of BDNF expression in the hippocampus during contextual learning. Nat Neurosci 3, 533-535.
69. Pressler SJ, Titler M, Koelling TM, Riley PL, Jung M, Hoyland-Domenico L, Ronis DL, Smith DG, Bleske BE, Dorsey SG, Giordani B (2015) Nurse-enhanced computerized cognitive training increases serum brain-derived neurotropic factor levels and improves working memory in heart failure. J Card Fail 21, 630-641.
70. Vinogradov S, Fisher M, Holland C, Shelly W, Wolkowitz O, Mellon SH (2009) Is serum brain-derived neurotrophic factor a biomarker for cognitive enhancement in schizophrenia? Biol Psychiatry 66, 549-553.
71. Angelucci F, Peppe A, Carlesimo GA, Serafini F, Zabberoni S, Barban F, Shofany J, Caltagirone C, Costa A (2015) A pilot study on the effect of cognitive training on BDNF serum levels in individuals with Parkinson's disease. Front Hum Neurosci 9, 130.
72. Phillips C, Baktir MA, Srivatsan M, Salehi A (2014) Neuroprotective effects of physical activity on the brain: A closer look at trophic factor signaling. Front Cell Neurosci 8, 170.
73. Brunelli A, Dimauro I, Sgro P, Emerenziani GP, Magi F, Baldari C, Guidetti L, Di Luigi L, Parisi P, Caporossi D (2012) Acute exercise modulates BDNF and pro-BDNF protein content in immune cells. Med Sci Sports Exerc 44, 1871-1880.
74. Smith PA (2014) BDNF: No gain without pain? Neuroscience 283, 107-123.
75. Lanz TA, Bove SE, Pilsmaker CD, Mariga A, Drummond EM, CadelinaGW, AdamowiczWO, Swetter BJ, Carmel S, Dumin JA, Kleiman RJ (2012) Robust changes in expression of brain-derived neurotrophic factor (BDNF) mRNA and protein across the brain do not translate to detectable changes in BDNF levels in CSF or plasma. Biomarkers 17, 524-531.
76. Pan W, Banks WA, Fasold MB, Bluth J, Kastin AJ (1998) Transport of brain-derived neurotrophic factor across the blood-brain barrier. Neuropharmacology 37, 1553-1561.
77. Pardridge WM (2007) Blood-brain barrier delivery. Drug Discov Today 12, 54-61.
78. Buchman AS, Yu L, Boyle PA, Schneider JA, De Jager PL, Bennett DA (2016) Higher brain BDNF gene expression is associated with slower cognitive decline in older adults. Neurology 86, 735-741.