Abstract
Temporal discounting, the tendency to select a smaller reward offered sooner over a larger reward offered at a later time, has been associated with a number of real-world decision-making outcomes important for health and wellbeing. Neurobiological mechanisms supporting temporal discounting have been explored among younger participants, and these have considered white matter integrity. However, the white matter correlates of temporal discounting in older adults are unclear. We hypothesized that greater temporal discounting would be associated with poorer white matter integrity measures, more specifically lower fractional anisotropy and higher trace, in older adults. Participants were 302 older persons without dementia (mean age = 81.38, mean years of education = 15.75, 75.5% female, mean MMSE = 28.29) from the Rush Memory and Aging Project, a community-based longitudinal study of aging. Temporal discounting was assessed using standard elicitation questions. White matter integrity was assessed with diffusion tensor imaging (DTI). Regression models were adjusted for the effects of age, sex, education, and white matter lesions. Secondary models further adjusted for global cognition. Results revealed significant associations between temporal discounting and white matter integrity measures (FA and trace) in bilateral frontal, frontostriatal, and temporal–parietal lobe white matter tracts, and results remained significant after further accounting for global cognition. These results suggest that temporal discounting is inversely associated with white matter integrity in old age and that this association is independent of global cognition.
Similar content being viewed by others
References
Alexander AL, Lee JE, Lazar M, Field AS (2007) Diffusion tensor imaging of the brain. Neurotherapeutics 4:316–329
Bach M, Laun FB, Leemans A, Tax CMW, Biessels GJ, Stieltjes B et al (2014) Methodological considerations on tract-based spatial statistics (TBSS). NeuroImage 100:358–369
Ballard K, Knutson B (2009) Dissociable neural representations of future reward magnitude and delay during temporal discounting. NeuroImage 45:143–150
Basser PJ, Pierpaoli C (1996) Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J Magn Reson B 111:209–219
Bennett DA, Wilson RS, Schneider JA, Evans DA, Beckett LA, Aggarwal NT, Barnes LL, Fox JH, Bach J (2002) Natural history of mild cognitive impairment in older persons. Neurology 59:198–205
Bennett DA, Schneider JA, Aggarwal NT, Arvanitakis Z, Shah RC, Kelly JF, Fox JH, Cochran EJ, Arends D, Treinkman AD, Wilson RS (2006) Decision rules guiding the clinical diagnosis of Alzheimer’s disease in two community-based cohort studies compared to standard practice in a clinic-based cohort study. Neuroepidemiology 27:169–176
Bennett DA, Schneider JA, Buchman AS, Barnes LL, Boyle PA, Wilson RS (2012) Overview and findings from the Rush Memory and Aging Project. Curr Alzheimer Res 9(6):646–663
Boyle PA, Yu L, Segawa E, Wilson RS, Buchman AS, Laibson DI, Bennett DA (2012) Association of cognition with temporal discounting in community based older persons. BMC Geriatrics 12:48
Boyle PA, Yu L, Gamble KJ, Bennett DA (2013) Temporal discounting is associated with and increased risk of mortality among community-based older persons without dementia. PLoS One 8(6):e67376
Frost R, McNaughton N (2017) The neural basis of delay discounting: a review and preliminary model. Neurosci Biobehav Rev 79:48–65
Han SD, Boyle PA, Yu L, Fleischman DA, Arfanakis K, Bennett DA (2013) Ventromedial PFC, parahippocampal, and cerebellar connectivity are associated with temporal discounting in old age. Exp Gerontol 48:1489–1498
Han SD, Boyle PA, Yu L, Fleischman DA, Arfanakis K, Leurgans S, Bennett DA (2014) Financial literacy is associated with medial brain region functional connectivity in old age. Arch Gerontol Geriatr 59:429–438
Han SD, Boyle PA, Arfanakis K, Fleischman D, Yu L, James BD, Bennett DA (2016a) Financial literacy is associated with white matter integrity in old age. Neuroimage 130:223–229
Han SD, Boyle PA, Yu L, Arfanakis K, James BD, Fleischman DA, Bennett DA (2016b) Grey matter correlates of susceptibility to scams in community-dwelling older adults. Brain Imaging Behavior 10:524–532
Hanggi J, Lohrey C, Drobetz R, Baetschmann H, Forstmeier S, Maercker A, Jancke L (2016) Strength of structural and functional frontostriatal connectivity predicts self-control in the healthy elderly. Front Aging Neurosci 8:307
Herrmann ES, Johnson PS, Johnson MW (2015) Examining delay discounting of condom-protected sex among men who have sex with men using crowdsourcing technology. AIDS Behav 19:1655–1665
James BD, Boyle PA, Yu L, Han SD, Bennett DA (2015) Cognitive decline is associated with risk aversion and temporal discounting in older adults without dementia. PLoS One 10:e0121900
Laibson D (1997) Golden eggs and hyperbolic discounting. Q J Econ 112:443–478
LeBihan D, Mangin JF, Poupon C, Clark CA, Pappata S et al (2001) Diffusion tensor imaging: concepts and applications. J Magn Reson Imaging 13:534–546
Marks BL, Madden DJ, Bucur B, Provenzale JM, White LE, Cabeza R, Huettel SA (2007) Role of aerobic fitness and aging on cerebral white matter integrity. Ann NY Acad Sci 1097:111–171
Marks SM, Lockart SN, Baker SL, Jagust WJ (2017) Tau and beta-amyloid are associated with medial temporal lobe structure, function, and memory encoding in normal aging. J Neurosci 37:3192–3201
McClelland J, Dalton B, Kekic M, Bartholdy S, Campbell IC, Schmidt U (2016) A systematic review of temporal discounting in eating disorders and obesity: behavioral and neuroimaging findings. Neurosci Biobehav Rev 71:506–528
McKhann G, Drachman D, Folstein M, Katzman R, Price D, Standlan E (1984) Clinical diagnosis of Alzheimer’s disease: report of the NINCDS/ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer’s Disease. Neurology 34:939–944
Moody L, Franck C, Hatz L, Bickel WK (2016) Impulsivity and polysubstance use: a systematic comparison of delay discounting in mon, dual, and tri-substance use. Exp Clin Psychopharmacol 24:30–37
Mukherjee P, Berman JI, Chung SW, Hess CP, Henry RG (2008) Diffusion tensor MR imaging and fiber tractography: theoretical underpinnings. AJNR 29:632–641
Odom AL (2011) Delay discounting: trait variable? Behav Proces 87:1–9
Odom AL, Baumann AAL (2010) Delay discounting: state and trait variable. In: Madden GJ, Bickel WK (eds) Impulsivity: the behavioral and neurological science of discounting. APA Books, Washington, DC, pp 39–65
Olson EA, Collins PF, Hooper CJ, Muetzel R, Lim KO, Lucianna M (2008) White matter integrity predicts delay discounting behavior in 9- to 23-year-olds: a diffusion tensor imaging study. J Cogn Neurosci 21:1406–1421
Peper JS, Mandl RCW, Braams BR, Water ED, Heijboer AC, Koolschijn PCMP, Crone EA (2013) Delay discounting and frontostriatal fiber tracts: a combined DTI and MTR study on impulsive choices in healthy young adults. Cereb Cortex 23:1695–1702
Peters J, Buchel C (2011) The neural mechanisms of inter-temporal decision-making: understanding variability. Trends Cognit Sci 15:207–239
Pierpaoli C, Walker L, Irfanoglu MO, Barnett A, Basser PJ et al (2010) TORTOISE: an integrated software package for processing of diffusion MRI data. In: Proceedings of the 18th Annual Meeting ISMRM, Stockholm, Sweden. 1597
Reimers S, Maylor EA, Stewart N, Chater N (2009) Associations between a one-shot delay discounting measure and age, income, education and real-world impulsive behavior. Personal Individ Differ 47:973–978
Reynolds B, Schiffbauer R (2005) Delay of gratification and delay discounting: a unifying feedback model of delay-related impulsive behavior. Psychol Record 55:439–460
Schwarz CG, Reid RI, Gunter JL, Senjem ML, Przybelski SA, Zuk SM et al (2014) Improved DTI registration allows voxel-based analysis that outperforms tract-based spatial statistics. NeuroImage 94:65–78
Smith SM, Nichols TE (2009) Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localization in cluster inference. Neuroimage 44:83–98
Smith SM, Jenkinson M, Johansen-Berg H, Rueckert D, Nichols TE et al (2006) Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 31:1487–1505
Van den Bos W, Rodriguez CA, Schweitzer JB, McClure SM (2014) Connectivity strength of dissociable striatal tracts predict individual differences in temporal discounting. J Neurosci 34:10298–10310
Vanderveldt A, Oliveira L, Green L (2016) Delay discounting: pigeon, rat, human—does it matter? J Exp Psychol Anim Learn Cognit 42:141–162
Varentsova A, Zhang S, Arfanakis K (2014) Development of a high angular resolution diffusion imaging human brain template. Neuroimage 91:177–186
Voss MW, Heo S, Prakash RS, Erickson KI, Alves H, Chaddock L, Szabo AN, Mailey EL, Wojcicki TR, White SM, Gothe N, McAuley E, Sutton BP, Kramer AF (2013) The influence of aerobic fitness on cerebral white matter integrity and cognitive function in older adults: results of a one-year exercise intervention. Hum Brain Map 34:2972–2985
Wilson RS, Barnes LL, Bennett DA (2003) Assessment of lifetime participation in cognitively stimulating activities. J Clin Exp Psychol 25:634–642
Zacharaki EI, Kanterakis S, Bryan RN, Davatzikos C (2008) Measuring brain lesion progression with a supervised tissue classification system. Med Image Comput Comput Assist Interv 11:620–627
Acknowledgements
This work was supported by the National Institute on Aging at the National Institutes of Health Grants R01AG017917 to DAB, R01AG033678 to PAB, and R01AG055430 to SDH. The authors gratefully thank the Rush Memory and Aging Project staff and participants. The authors declare no competing financial interests.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical statement
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Han, S.D., Arfanakis, K., Fleischman, D.A. et al. White matter correlates of temporal discounting in older adults. Brain Struct Funct 223, 3653–3663 (2018). https://doi.org/10.1007/s00429-018-1712-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00429-018-1712-3