Changes in Neural Connectivity and Memory Following a Yoga Intervention for Older Adults: A Pilot Study

Journal of Alzheimer's Disease

Volumn 52, Issue 2, 2016, Pages 673-684

  Eyre, Harris A ^a,b   Acevedo, Bianca ^a   Yang, Hongyu ^a   Siddarth, Prabha ^a   Van Dyk, Kathleen ^a   Ercoli, Linda ^a   Leaver, Amber M ^c   Cyr, Natalie St ^a   Narr, Katherine ^c   Baune, Bernhard T ^b   Khalsa, Dharma S ^d   Lavretsky, Helen ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF ADELAIDE   (Australia)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d Alzheimer Research and Prevention Foundation   (United States)

Author keywords

Aging; cognitive decline; memory training; mild cognitive impairment; mind body; older adults; subjective memory complaints; yoga

Indexed keywords

ADULT; AGED; ANTERIOR CINGULATE; ARTICLE; CLINICAL ARTICLE; CONNECTOME; CONTROLLED STUDY; DEFAULT MODE NETWORK; DEPRESSION; FEMALE; FRONTAL CORTEX; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; INFERIOR FRONTAL GYRUS; LANGUAGE; LANGUAGE PROCESSING; MALE; MEDIAL FRONTAL CORTEX; MEMORY; MEMORY TEST; MILD COGNITIVE IMPAIRMENT; OCCIPITAL CORTEX; PARIETAL CORTEX; PERFORMANCE; PILOT STUDY; POSTERIOR CINGULATE; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; VERBAL MEMORY; YOGA; BRAIN; COGNITIVE DEFECT; DIAGNOSTIC IMAGING; FUNCTIONAL NEUROIMAGING; LEARNING; NERVE TRACT; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; PSYCHOLOGY;

BRAIN; COGNITIVE DYSFUNCTION; FUNCTIONAL NEUROIMAGING; HUMANS; LEARNING; MAGNETIC RESONANCE IMAGING; MEMORY; NEURAL PATHWAYS; NEUROPSYCHOLOGICAL TESTS; PILOT PROJECTS; YOGA;

EID: 84971280455     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-150653     Document Type: Article

References (68)

1. United Nations, Department of Economic and Social Affairs, Population Division (2013) World Population Ageing 2013. ST/ESA/SER.A/348.
2. PetersenRC(2011) Clinical practice. Mild cognitive impairment. N Engl J Med 364, 2227-2234.
3. Petersen RC, Smith GE, Waring SC, Ivnik RJ, Tangalos EG, Kokmen E (1999) Mild cognitive impairment: Clinical characterization and outcome. Arch Neurol 56, 303-308.
4. Norton S, Matthews FE, Barnes DE, Yaffe K, Brayne C (2014) Potential for primary prevention of Alzheimer's disease: An analysis of population-based data. Lancet Neurol 13, 788-794.
5. Dossett ML, Davis RB, Lembo AJ, Yeh GY (2014) Complementary and alternative medicine use by US adults with gastrointestinal conditions: Results from the 2012 National Health Interview Survey. Am J Gastroenterol 109, 1705-1711.
6. Abbott R, Lavretsky H (2013) Tai Chi and Qigong for the treatment and prevention of mental disorders. Psychiatr Clin North Am 36, 109-119.
7. Siddarth D, Siddarth P, LavretskyH(2014)Anobservational study of the health benefits of yoga or tai chi compared with aerobic exercise in community-dwelling middle-aged and older adults. Am J Geriatr Psychiatry 22, 272-273.
8. Lavretsky H (2009) Complementary and alternative medicine use for treatment and prevention of late-life mood and cognitive disorders. Aging Health 5, 61-78.
9. Gothe NP, Kramer AF, McAuley E (2014) The effects of an 8-week Hatha yoga intervention on executive function in older adults. J Gerontol A Biol Sci Med Sci 69, 1109-1116.
10. Hariprasad VR, Koparde V, Sivakumar PT, Varambally S, Thirthalli J, Varghese M, Basavaraddi IV, Gangadhar BN (2013) Randomized clinical trial of yoga-based intervention in residents from elderly homes: Effects on cognitive function. Indian J Psychiatry 55, S357-S363.
11. Marchand WR (2014) Neural mechanisms of mindfulness and meditation: Evidence from neuroimaging studies.World J Radiol 6, 471-479.
12. 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.
13. Wells RE, Yeh GY, Kerr CE, Wolkin J, Davis RB, Tan Y, Spaeth R,Wall RB,Walsh J, Kaptchuk TJ, Press D, Phillips RS, Kong J (2013) Meditation's impact on default mode network and hippocampus in mild cognitive impairment: A pilot study. Neurosci Lett 556, 15-19.
14. Ahdidan J, Raji CA, DeYoe EA, Mathis J, Noe KO, Rimestad J, Kjeldsen TK, Mosegaard J, Becker JT, LopezO(2015) Quantitative neuroimaging software for clinical assessment of hippocampal volumes on MR imaging. J Alzheimers Dis 49, 723-732.
15. Flak MM, Hernes SS, Skranes J, Lohaugen GC (2014) The Memory Aid study: Protocol for a randomized controlled clinical trial evaluating the effect of computer-based working memory training in elderly patients with mild cognitive impairment (MCI). Trials 15, 156.
16. Verhaeghen P, Marcoen A, Goossens L (1992) Improving memory performance in the aged through mnemonic training: A meta-analytic study. Psychol Aging 7, 242-251.
17. Olchik MR, Farina J, Steibel N, Teixeira AR, Yassuda MS (2013) Memory training (MT) in mild cognitive impairment (MCI) generates change in cognitive performance. Arch Gerontol Geriatr 56, 442-447.
18. Jean L, Bergeron ME, Thivierge S, Simard M (2010) Cognitive intervention programs for individuals with mild cognitive impairment: Systematic review of the literature. Am J Geriatr Psychiatry 18, 281-296.
19. Simon SS, Yokomizo JE, Bottino CM (2012) Cognitive intervention in amnestic Mild Cognitive Impairment:Asystematic review. Neurosci Biobehav Rev 36, 1163-1178.
20. Hughes CP, Berg L, Danziger WL, Coben LA, Martin RL (1982) A new clinical scale for the staging of dementia. Br J Psychiatry 140, 566-572.
21. Wilkinson GS, Robertson GJ (2006) Wide Range Achievement Test 4 professional manual, Psychological Assessment Resources, Lutz, FL.
22. Folstein MF, Folstein SE, McHugh PR (1975) Mini-mental state. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12, 189-198.
23. Fahn S, Elton R, et al., (1987) Unified Parkinson's Disease Rating Scale. In Recent Developments in Parkinson's Disease, Fahn S, Marsden C, Goldstein M, Calne D, eds. Macmillan Healthcare Information, Florham Park, NJ.
24. Fuld PA, Masur DM, Blau AD, Crystal H, Aronson MK (1990) Object-memory evaluation for prospective detection of dementia in normal functioning elderly: Predictive and normative data. J Clin Exp Neuropsychol 12, 520-528.
25. First MB, Gibbon M, Spitzer RL,Williams JBW, Benjamin L (1996) User's guide for the Structured Clinical Interview for DSM-IV Axis I Disorders-Research version-(SCID-I), Version 2.0. Biometrics Research Department, New York State Psychiatric Institute, New York.
26. Truelsen T, Lindenstrom E, Boysen G (1994) Comparison of probability of stroke between the Copenhagen City Heart Study and the Framingham Study. Stroke 25, 802-807.
27. American Heart Association (1990) Stroke Risk Factor Prediction Chart Dallas, TX.
28. Endicott J, Nee J, HarrisonW, Blumenthal R (1993) Quality of Life Enjoyment and Satisfaction Questionnaire: A new measure. Psychopharmacol Bull 29, 321-326.
29. Miller MD, Paradis CF, Houck PR, Mazumdar S, Stack JA, Rifai AH, Mulsant B, Reynolds CF (1992) Rating chronic medical illness burden in geropsychiatric practice and research: Application of the Cumulative Illness Rating Scale. Psychiatry Res 41, 237-248.
30. Ware JEJ,Kosinski M,KellerSD(1994) SF-36 physical and mental health summary scores: A user's manual, The Health Institute, New England Medical Center, Boston, MA.
31. Yesavage JA, Brink TL, Rose TL, Lum O, Huang V, Adey M, Leirer VO (1982) Development and validation of a geriatric depression screening scale: A preliminary report. J Psychiatr Res 17, 37-49.
32. Shapiro AM, Benedict RH, Schretlen D, Brandt J (1999) Construct and concurrent validity of the Hopkins Verbal Learning Test-revised. Clin Neuropsychol 13, 348-358.
33. Shin MS, Park SY, Park SR, Seol SH, Kwon JS (2006) Clinical and empirical applications of the Rey-Osterrieth Complex Figure Test. Nat Protoc 1, 892-899.
34. Newberg AB, Wintering N, Khalsa DS, Roggenkamp H, Waldman MR (2010) Meditation effects on cognitive function and cerebral blood flow in subjects with memory loss: A preliminary study. J Alzheimers Dis 20, 517-526.
35. ARPF, Alzheimer's Research & Prevention Foundation: ARPF Research: Kirtan Kriya, http://www.alzh eimersprevention.org/kirtan kriya.htm.
36. Lingjaerde O, Ahlfors UG, Bech P, Dencker SJ, Elgen K (1987) TheUKUside effect rating scale.Anewcomprehensive rating scale for psychotropic drugs and a cross-sectional study of side effects in neuroleptic-treated patients. Acta Psychiatr Scand Suppl 334, 1-100.
37. Gross AL, RebokGW(2011) Memory training and strategy use in older adults: Results from theACTIVE study. Psychol Aging 26, 503-517.
38. McCarty DL (1980) Investigation of a visual imagery mnemonic device for acquiring face-name associations. J Exp Psychol Hum Learn 6, 145-155.
39. Beckmann CF, Smith SM (2004) Probabilistic independent component analysis for functional magnetic resonance imaging. IEEE Trans Med Imaging 23, 137-152.
40. FMRIB, Dual Regression, http://fsl.fmrib.ox.ac.uk/fsl/ fslwiki/DualRegression, Accessed 05/08-15.
41. Koenigs M, Barbey AK, Postle BR, Grafman J (2009) Superior parietal cortex is critical for the manipulation of information in working memory. J Neurosci 29, 14980-14986.
42. Fox MD, Raichle ME (2007) Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 8, 700-711.
43. Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL (2001) A default mode of brain function. Proc Natl Acad Sci U S A 98, 676-682.
44. Yeo BT, Krienen FM, Sepulcre J, Sabuncu MR, Lashkari D, Hollinshead M, Roffman JL, SmollerJW, Zollei L, Polimeni JR, Fischl B, Liu H, Buckner RL (2011) The organization of the human cerebral cortex estimated by intrinsic functional connectivity. J Neurophysiol 106, 1125-1165.
45. Buckner RL, Andrews-Hanna JR, Schacter DL (2008) The brain's default network: Anatomy, function, and relevance to disease. Ann N Y Acad Sci 1124, 1-38.
46. Spreng RN, Mar RA, Kim AS (2009) The common neural basis of autobiographical memory, prospection, navigation, theory of mind, and the default mode: A quantitative metaanalysis. J Cogn Neurosci 21, 489-510.
47. Northoff G, Bermpohl F (2004) Cortical midline structures and the self. Trends Cogn Sci 8, 102-107.
48. Andrews-Hanna JR, Snyder AZ,Vincent JL, Lustig C, Head D, Raichle ME, Buckner RL (2007) Disruption of largescale brain systems in advanced aging. Neuron 56, 924-935.
49. Bluhm RL, Osuch EA, Lanius RA, Boksman K, Neufeld RW, Theberge J, Williamson P (2008) Default mode network connectivity: Effects of age, sex, and analytic approach. Neuroreport 19, 887-891.
50. Damoiseaux JS, Beckmann CF, Arigita EJ, Barkhof F, Scheltens P, Stam CJ, Smith SM, Rombouts SA (2008) Reduced resting-state brain activity in the default network in normal aging. Cereb Cortex 18, 1856-1864.
51. Razlighi QR, Habeck C, Steffener J, Gazes Y, Zahodne LB, Mackay-Brandt A, Stern Y (2014) Unilateral disruptions in the default network with aging in native space. Brain Behav 4, 143-157.
52. Biswal BB, Mennes M, Zuo XN, Gohel S, Kelly C, Smith SM, Beckmann CF, Adelstein JS, Buckner RL, Colcombe S, Dogonowski AM, Ernst M, Fair D, Hampson M, Hoptman MJ, Hyde JS, Kiviniemi VJ, Kotter R, Li SJ, Lin CP, Lowe MJ, Mackay C, Madden DJ, Madsen KH, Margulies DS, Mayberg HS, McMahon K, Monk CS, Mostofsky SH, Nagel BJ, Pekar JJ, Peltier SJ, Petersen SE, Riedl V, Rombouts SA, Rypma B, Schlaggar BL, Schmidt S, Seidler RD, Siegle GJ, Sorg C, Teng GJ, Veijola J, Villringer A, Walter M,Wang L,Weng XC, Whitfield-Gabrieli S,Williamson P, Windischberger C, Zang YF, Zhang HY, Castellanos FX, Milham MP (2010) Toward discovery science of human brain function. Proc Natl Acad Sci U S A 107, 4734-4739.
53. Campbell KL, Grigg O, Saverino C, Churchill N, Grady CL (2013) Age differences in the intrinsic functional connectivity of default network subsystems. Front Aging Neurosci 5, 73.
54. Mevel K, Landeau B, Fouquet M, La Joie R, Villain N, Mezenge F, Perrotin A, Eustache F, Desgranges B, Chetelat G (2013) Age effect on the default mode network, inner thoughts, and cognitive abilities. Neurobiol Aging 34, 1292-1301.
55. Vidal-Pineiro D, Valls-Pedret C, Fernandez-Cabello S, Arenaza-Urquijo EM, Sala-Llonch R, Solana E, Bargallo N, Junque C, Ros E, Bartres-Faz D (2014) Decreased default mode network connectivity correlates with age-associated structural and cognitive changes. Front Aging Neurosci 6, 256.
56. Ferreira LK, Busatto GF (2013) Resting-state functional connectivity in normal brain aging. Neurosci Biobehav Rev 37, 384-400.
57. Jones DT, Machulda MM, Vemuri P, McDade EM, Zeng G, Senjem ML, Gunter JL, Przybelski SA,AvulaRT, Knopman DS, Boeve BF, Petersen RC, Jack CR Jr (2011) Age-related changes in the default mode network are more advanced in Alzheimer disease. Neurology 77, 1524-1531.
58. Buckner RL, Snyder AZ, Shannon BJ, LaRossa G, Sachs R, Fotenos AF, Sheline YI, Klunk WE, Mathis CA, Morris JC, MintunMA(2005) Molecular, structural, and functional characterization of Alzheimer's disease: Evidence for a relationship between default activity, amyloid, and memory. J Neurosci 25, 7709-7717.
59. Greicius MD, Supekar K, Menon V, Dougherty RF (2009) Resting-state functional connectivity reflects structural connectivity in the default mode network. Cereb Cortex 19, 72-78.
60. Ornish D, Lin J, Chan JM, Epel E, Kemp C, Weidner G, Marlin R, Frenda SJ, Magbanua MJ, Daubenmier J, Estay I, Hills NK, Chainani-Wu N, Carroll PR, Blackburn EH (2013) Effect of comprehensive lifestyle changes on telomerase activity and telomere length in men with biopsy-proven low-risk prostate cancer: 5-year followup of a descriptive pilot study. Lancet Oncol 14, 1112-1120.
61. Eyre HA, Baune BT (2014) Assessing for unique immunomodulatory and neuroplastic profiles of physical activity subtypes: A focus on psychiatric disorders. Brain Behav Immun 39, 42-55.
62. Black DS, Cole SW, Irwin MR, Breen E, St Cyr NM, Nazarian N, Khalsa DS, Lavretsky H (2013) Yogic meditation reverses NF-kappaB and IRF-related transcriptome dynamics in leukocytes of family dementia caregivers in a randomized controlled trial. Psychoneuroendocrinology 38, 348-355.
63. Naveen GH, Thirthalli J, Rao MG, Varambally S, Christopher R, Gangadhar BN (2013) Positive therapeutic and neurotropic effects of yoga in depression: A comparative study. Indian J Psychiatry 55, S400-S404.
64. Sinha S, Singh SN, MongaYP, RayUS(2007) Improvement of glutathione and total antioxidant status with yoga. J Altern Complement Med 13, 1085-1090.
65. TaylorVA, DaneaultV, Grant J, Scavone G, Breton E, Roffe-Vidal S, Courtemanche J, Lavarenne AS, Marrelec G, Benali H, Beauregard M (2013) Impact of meditation training on the default mode network during a restful state. Soc Cogn Affect Neurosci 8, 4-14.
66. Brewer JA, Worhunsky PD, Gray JR, Tang YY, Weber J, Kober H (2011) Meditation experience is associated with differences in default mode network activity and connectivity. Proc Natl Acad Sci U S A 108, 20254-20259.
67. Vandenberghe R, Gitelman DR, Parrish TB, Mesulam MM (2001) Functional specificity of superior parietal mediation of spatial shifting. Neuroimage 14, 661-673.
68. Daselaar SM, Iyengar V, Davis SW, Eklund K, Hayes SM, Cabeza RE (2015) Less wiring, more firing: Lowperforming older adults compensate for impaired white matter with greater neural activity. Cereb Cortex 25, 983-990.