Walking Time Is Associated With Hippocampal Volume in Overweight and Obese Office Workers

Frida Bergman, Tove Matsson-Frost, Lars Jonasson, Elin Chorell, Ann Sörlin, Patrik Wennberg, Fredrik Öhberg, Mats Ryberg, James A Levine, Tommy Olsson, Carl-Johan Boraxbekk, Frida Bergman, Tove Matsson-Frost, Lars Jonasson, Elin Chorell, Ann Sörlin, Patrik Wennberg, Fredrik Öhberg, Mats Ryberg, James A Levine, Tommy Olsson, Carl-Johan Boraxbekk

Abstract

Objectives: To investigate the long-term effects on cognition and brain function after installing treadmill workstations in offices for 13 months. Methods: Eighty healthy overweight or obese office workers aged 40-67 years were individually randomized to an intervention group, receiving a treadmill workstation and encouraging emails, or to a control group, continuing to work as usual. Effects on cognitive function, hippocampal volume, prefrontal cortex (PFC) thickness, and circulating brain-derived neurotrophic factor (BDNF) were analyzed. Further, mediation analyses between changes in walking time and light-intensity physical activity (LPA) on changes in BDNF and hippocampal volume between baseline and 13 months, and multivariate analyses of the baseline data with percentage sitting time as the response variable, were performed. Results: No group by time interactions were observed for any of the outcomes. In the mediation analyses, positive associations between changes in walking time and LPA on changes in hippocampal volume were observed, although not mediated by changes in BDNF levels. In the multivariate analyses, a negative association between percentage sitting time and hippocampal volume was observed, however only among those older than 51 years of age. Conclusion: Although no group by time interactions were observed, our analyses suggest that increased walking and LPA may have positive effects on hippocampal volume and that sedentary behavior is associated with brain structures of importance for memory functions. Trial Registration: www.ClinicalTrials.gov as NCT01997970.

Keywords: brain function; cognition; office work; physical activity; randomized controlled trial; sedentary behavior.

Copyright © 2020 Bergman, Matsson-Frost, Jonasson, Chorell, Sörlin, Wennberg, Öhberg, Ryberg, Levine, Olsson and Boraxbekk.

Figures

Figure 1
Figure 1
Estimated means (SEM) of z-standardized scores for the different cognitive domains episodic memory (A), executive function (B), working memory (C), processing speed (D), and for the composite cognitive score (E). The cognitive score was derived from combining the different cognitive domains. **p < 0.01, ***p < 0.001 within-group difference from baseline.
Figure 2
Figure 2
Relationship between changes in walking time and Hippocampus (A) and changes in light-intensity physical activity (LPA) and Hippocampus (B) between baseline and 13 months, as mediated by changes in BDNF between baseline and 13 months. Beta-values along with standardized coefficients (z-values within parentheses) are reported, *p < 0.05, **p < 0.01.
Figure 3
Figure 3
(A) Two separate OPLS models describing baseline associations between measures of brain and cognitive functions and percentage sitting time in participants younger (y-axis) and older than 51 years (x-axis). A complete list of variables included in the OPLS-models is presented in the Supplementary Material. (B) Univariate linear regression analysis between hippocampal volume and percentage sitting time among participants younger than 51 years. (C) Univariate linear regression analysis between hippocampal volume and percentage sitting time among participants older than 51 years. OPLS, orthogonal partial least squares; pcorr = correlation scaled OPLS weights, i.e., multivariate association to percent sitting time. ACC, anterior cingulate cortex; dLPFC, dorsolateral prefrontal cortex; vLPFC, ventrolateral prefrontal cortex.

References

    1. Bergman F., Boraxbekk C. J., Wennberg P., Sorlin A., Olsson T. (2015). Increasing physical activity in office workers—the Inphact Treadmill study; a study protocol for a 13-month randomized controlled trial of treadmill workstations. BMC Public Health 15:632. 10.1186/s12889-015-2017-6
    1. Bergman F., Wahlström V., Stomby A., Otten J., Lanthén E., Renklint R., et al. . (2018). Treadmill workstations in office workers who are overweight or obese: a randomized controlled trial. Lancet Public Health 3, e523–e535. 10.1016/S2468-2667(18)30163-4
    1. Bobb J. F., Schwartz B. S., Davatzikos C., Caffo B. (2014). Cross-sectional and longitudinal association of body mass index and brain volume. Hum. Brain Mapp. 35, 75–88. 10.1002/hbm.22159
    1. Brooks S. J., Benedict C., Burgos J., Kempton M. J., Kullberg J., Nordenskjold R., et al. . (2013). Late-life obesity is associated with smaller global and regional gray matter volumes: a voxel-based morphometric study. Int. J. Obes. 37, 230–236. 10.1038/ijo.2012.13
    1. Burzynska A. Z., Chaddock-Heyman L., Voss M. W., Wong C. N., Gothe N. P., Olson E. A., et al. . (2014). Physical activity and cardiorespiratory fitness are beneficial for white matter in low-fit older adults. PLoS One 9:e107413. 10.1371/journal.pone.0107413
    1. Church T. S., Thomas D. M., Tudor-Locke C., Katzmarzyk P. T., Earnest C. P., Rodarte R. Q., et al. . (2011). Trends over 5 decades in U.S. occupation-related physical activity and their associations with obesity. PLoS One 6:e19657. 10.1371/journal.pone.0019657
    1. Colcombe S. J., Erickson K. I., Scalf P. E., Kim J. S., Prakash R., McAuley E., et al. . (2006). Aerobic exercise training increases brain volume in aging humans. J. Gerontol. A Biol. Sci. Med. Sci. 61, 1166–1170. 10.1093/gerona/61.11.1166
    1. Dahl A. K., Hassing L. B. (2013). Obesity and cognitive aging. Epidemiol. Rev. 35, 22–32. 10.1093/epirev/mxs002
    1. Delis D. C., Kaplan E., Kramer J. H. (2001). Delis-Kaplan Executive Function System. San Antonio, TX: The Psychological Corporation.
    1. Dempsey P. C., Blankenship J. M., Larsen R. N., Sacre J. W., Sethi P., Straznicky N. E., et al. . (2017). Interrupting prolonged sitting in type 2 diabetes: nocturnal persistence of improved glycaemic control. Diabetologia 60, 499–507. 10.1007/s00125-016-4169-z
    1. Duvivier B., Bolijn J. E., Koster A., Schalkwijk C. G., Savelberg H., Schaper N. C. (2018). Reducing sitting time versus adding exercise: differential effects on biomarkers of endothelial dysfunction and metabolic risk. Sci. Rep. 8:8657. 10.1038/s41598-018-26616-w
    1. Erickson K. I., Voss M. W., Prakash R. S., Basak C., Szabo A., Chaddock L., et al. . (2011). Exercise training increases size of hippocampus and improves memory. Proc. Natl. Acad. Sci. U S A 108, 3017–3022. 10.1073/pnas.1015950108
    1. Eriksen B. A., Eriksen C. W. (1974). Effects of noise letters upon the identification of a target letter in a nonsearch task. Percept. Psychophys. 16, 143–149. 10.3758/bf03203267
    1. Eriksson L., Trygg J., Wold S. (2008). CV-ANOVA for significance testing of PLS and OPLS (R) models. J. Chemomet. 22, 594–600. 10.1002/cem.1187
    1. Falck R. S., Davis J. C., Liu-Ambrose T. (2017). What is the association between sedentary behaviour and cognitive function? A systematic review. Br. J. Sports Med. 51, 800–811. 10.1136/bjsports-2015-095551
    1. Fanning J., Porter G., Awick E. A., Ehlers D. K., Roberts S. A., Cooke G., et al. . (2017). Replacing sedentary time with sleep, light, or moderate-to-vigorous physical activity: effects on self-regulation and executive functioning. J. Behav. Med. 40, 332–342. 10.1007/s10865-016-9788-9
    1. Fischl B., Salat D. H., Busa E., Albert M., Dieterich M., Haselgrove C., et al. . (2002). Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33, 341–355. 10.1016/s0896-6273(02)00569-x
    1. Greenwood P. M., Parasuraman R. (2016). The mechansisms of far transfer from cognitive training: review and hypothesis. Neuropsychology 30, 742–755. 10.1037/neu0000235
    1. Hamer M., Sharma N., Batty G. D. (2018). Association of objectively measured physical activity with brain structure: UK Biobank study. J. Intern. Med. 284, 439–443. 10.1111/joim.12772
    1. Hamer M., Stamatakis E. (2014). Prospective study of sedentary behavior, risk of depression, and cognitive impairment. Med. Sci. Sports Exerc. 46, 718–723. 10.1249/mss.0000000000000156
    1. Jonasson L. S., Nyberg L., Kramer A. F., Lundquist A., Riklund K., Boraxbekk C. J. (2017). Aerobic exercise intervention, cognitive performance, and brain structure: results from the physical influences on brain in aging (PHIBRA) study. Front. Aging Neurosci. 8:336. 10.3389/fnagi.2016.00336
    1. Kesse-Guyot E., Charreire H., Andreeva V. A., Touvier M., Hercberg S., Galan P., et al. . (2012). Cross-sectional and longitudinal associations of different sedentary behaviors with cognitive performance in older adults. PLoS One 7:e47831. 10.1371/journal.pone.0047831
    1. Kirchner W. K. (1958). Age differences in short-term retetion of rapidly changing information. J. Exp. Psychol. 55, 352–358. 10.1037/h0043688
    1. Loprinzi P. D., Frith E. (2018). Obesity and episodic memory function. J. Physiol. Sci. 68, 321–331. 10.1007/s12576-018-0612-x
    1. Maasakkers C. M., Claassen J. A. H. R., Gardiner P. A., Olde Rikkert M. G. M., Lipnicki D. M., Scarmeas N., et al. . (2020). The association of sedentary behaviour and cognitive function in people without dementia: a coordinated analysis across five cohort studies from COSMIC. Sports Med. 50, 403–413. 10.1007/s40279-019-01186-7
    1. Murdock B. B. J. (1962). The serial position effect of free recall. J. Exp. Psychol. 64, 482–488. 10.1037/h0045106
    1. Northey J. M., Cherbuin N., Pumpa K. L., Smee D. J., Rattray B. (2018). Exercise interventions for cognitive function in adults older than 50: a systematic review with meta-analysis. Br. J. Sports Med. 52, 154–160. 10.1136/bjsports-2016-096587
    1. Nyberg L., McIntosh A. R., Cabeza R., Habib R., Houle S., Tulving E. (1996). General and specific brain regions involved in encoding and retrieval of events: what, where, and when. Proc. Natl. Acad. Sci. U S A 93, 11280–11285. 10.1073/pnas.93.20.11280
    1. Physical Activity Guidelines Advisory Committee (2018). 2018 Physical Activity Guidelines Advisory Committee Scientific Report. Washington, DC: U.S. Department of Health and Human Services.
    1. Reuter M., Schmansky N. J., Rosas H. D., Fischl B. (2012). Within-subject template estimation for unbiased longitudinal image analysis. NeuroImage 61, 1402–1418. 10.1016/j.neuroimage.2012.02.084
    1. Rosseel Y. (2012). lavaan: an R package for structural equation modeling. J. Stat. Soft. 48:36 10.18637/jss.v048.i02
    1. Suwabe K., Byun K., Hyodo K., Reagh Z. M., Roberts J. M., Matsushita A., et al. . (2018). Rapid stimulation of human dentate gyrus function with acute mild exercise. Proc. Natl. Acad. Sci. U S A 115, 10487–10492. 10.1073/pnas.1805668115
    1. Torbeyns T., de Geus B., Bailey S., De Pauw K., Decroix L., Van Cutsem J., et al. . (2016). Bike desks in the office: physical health, cognitive function, work engagement, and work performance. J. Occup. Environ. Med. 58, 1257–1263. 10.1097/jom.0000000000000911
    1. Tremblay M. S., Aubert S., Barnes J. D., Saunders T. J., Carson V., Latimer-Cheung A. E., et al. . (2017). Sedentary behavior research network (SBRN)—terminology consensus project process and outcome. Int. J. Behav. Nutr. Phys. Act. 14:75. 10.1186/s12966-017-0525-8
    1. Walhovd K. B., Storsve A. B., Westlye L. T., Drevon C. A., Fjell A. M. (2014). Blood markers of fatty acids and vitamin D, cardiovascular measures, body mass index, and physical activity relate to longitudinal cortical thinning in normal aging. Neurobiol. Aging 35, 1055–1064. 10.1016/j.neurobiolaging.2013.11.011
    1. Wechsler D. (2010). WAIS IV: Wechsler Adult Intelligence Scale—Fourth Edition. Svensk Version. Sweden: Nyman, H. NCS Pearson Inc.
    1. Wheeler M. J., Dempsey P. C., Grace M. S., Ellis K. A., Gardiner P. A., Green D. J., et al. . (2017). Sedentary behavior as a risk factor for cognitive decline? A focus on the influence of glycemic control in brain health. Alzheimers Dement. 3, 291–300. 10.1016/j.trci.2017.04.001
    1. Vijayakumar N., Whittle S., Yücel M., Dennison M., Simmons J., Allen N. B. (2014). Thinning of the lateral prefrontal cortex during adolescence predicts emotion regulation in females. Soc. Cogn. Affect. Neurosci. 9, 1845–1854. 10.1093/scan/nst183
    1. Willette A. A., Kapogiannis D. (2015). Does the brain shrink as the waist expands? Ageing Res. Rev. 20, 86–97. 10.1016/j.arr.2014.03.007
    1. Voss M. W., Weng T. B., Burzynska A. Z., Wong C. N., Cooke G. E., Clark R., et al. . (2016). Fitness, but not physical activity, is related to functional integrity of brain networks associated with aging. NeuroImage 131, 113–125. 10.1016/j.neuroimage.2015.10.044
    1. Yang Y., Shields G. S., Guo C., Liu Y. (2018). Executive function performance in obesity and overweight individuals: a meta-analysis and review. Neurosci. Biobehav. Rev. 84, 225–244. 10.1016/j.neubiorev.2017.11.020

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