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Open Access 01-01-2017 | Original Article

The association between stress and mood across the adult lifespan on default mode network

Authors: José Miguel Soares, Paulo Marques, Ricardo Magalhães, Nadine Correia Santos, Nuno Sousa

Published in: Brain Structure and Function | Issue 1/2017

Abstract

Aging of brain structure and function is a complex process characterized by high inter- and intra-individual variability. Such variability may arise from the interaction of multiple factors, including exposure to stressful experience and mood variation, across the lifespan. Using a multimodal neuroimaging and neurocognitive approach, we investigated the association of stress, mood and their interaction, in the structure and function of the default mode network (DMN), both during rest and task-induced deactivation, throughout the adult lifespan. Data confirmed a decreased functional connectivity (FC) and task-induced deactivation of the DMN during the aging process and in subjects with lower mood; on the contrary, an increased FC was observed in subjects with higher perceived stress. Surprisingly, the association of aging with DMN was altered by stress and mood in specific regions. An increased difficulty to deactivate the DMN was noted in older participants with lower mood, contrasting with an increased deactivation in individuals presenting high stress, independently of their mood levels, with aging. Interestingly, this constant interaction across aging was globally most significant in the combination of high stress levels with a more depressed mood state, both during resting state and task-induced deactivations. The present results contribute to characterize the spectrum of FC and deactivation patterns of the DMN, highlighting the crucial association of stress and mood levels, during the adult aging process. These combinatorial approaches may help to understand the heterogeneity of the aging process in brain structure and function and several states that may lead to neuropsychiatric disorders.

Aiken LS, West SG (1991) Multiple regression: testing and interpreting interactions. Sage, Newbury Park

Allen EA, Erhardt EB, Damaraju E, Gruner W, Segall JM, Silva RF, Havlicek M, Rachakonda S, Fries J, Kalyanam R, Michael AM, Caprihan A, Turner JA, Eichele T, Adelsheim S, Bryan AD, Bustillo J, Clark VP, Feldstein Ewing SW, Filbey F, Ford CC, Hutchison K, Jung RE, Kiehl KA, Kodituwakku P, Komesu YM, Mayer AR, Pearlson GD, Phillips JP, Sadek JR, Stevens M, Teuscher U, Thoma RJ, Calhoun VD (2011) A baseline for the multivariate comparison of resting-state networks. Front Syst Neurosci 5:2. doi:10.3389/fnsys.2011.00002 PubMedPubMedCentral

Andreescu C, Wu M, Butters MA, Figurski J, Reynolds CF 3rd, Aizenstein HJ (2011) The default mode network in late-life anxious depression. Am J Geriatr Psychiatry 19(11):980–983. doi:10.1097/JGP.0b013e318227f4f9 CrossRefPubMedPubMedCentral

Andrews-Hanna JR (2011) The brain’s default network and its adaptive role in internal mentation. Neuroscientist. doi:10.1177/1073858411403316 PubMedPubMedCentral

Andrews-Hanna JR, Reidler JS, Sepulcre J, Poulin R, Buckner RL (2010) Functional-anatomic fractionation of the brain’s default network. Neuron 65(4):550–562. doi:10.1016/j.neuron.2010.02.005 CrossRefPubMedPubMedCentral

Anticevic A, Cole MW, Murray JD, Corlett PR, Wang XJ, Krystal JH (2012) The role of default network deactivation in cognition and disease. Trends Cognit Sci 16(12):584–592. doi:10.1016/j.tics.2012.10.008 CrossRef

Arbabshirani MR, Havlicek M, Kiehl KA, Pearlson GD, Calhoun VD (2012) Functional network connectivity during rest and task conditions: a comparative study. Hum Brain Mapp. doi:10.1002/hbm.22118 PubMedPubMedCentral

Bartels A, Zeki S (2005) Brain dynamics during natural viewing conditions—a new guide for mapping connectivity in vivo. Neuroimage 24(2):339–349. doi:10.1016/j.neuroimage.2004.08.044 CrossRefPubMed

Beckmann CF, DeLuca M, Devlin JT, Smith SM (2005) Investigations into resting-state connectivity using independent component analysis. Philos Trans R Soc Lond B Biol Sci 360(1457):1001–1013. doi:10.1098/rstb.2005.1634 CrossRefPubMedPubMedCentral

Bian Y, Pan Z, Hou Z, Huang C, Li W, Zhao B (2012) Learning, memory, and glial cell changes following recovery from chronic unpredictable stress. Brain Res Bull 88(5):471–476. doi:10.1016/j.brainresbull.2012.04.008 CrossRefPubMed

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. doi:10.1196/annals.1440.011 CrossRefPubMed

Calabrese F, Molteni R, Racagni G, Riva MA (2009) Neuronal plasticity: a link between stress and mood disorders. Psychoneuroendocrinology 34(Suppl 1):S208–S216. doi:10.1016/j.psyneuen.2009.05.014 CrossRefPubMed

Calhoun VD, Adali T, Pearlson GD, Pekar JJ (2001) A method for making group inferences from functional MRI data using independent component analysis. Hum Brain Mapp 14(3):140–151CrossRefPubMed

Chou YH, Chen NK, Madden DJ (2013) Functional brain connectivity and cognition: effects of adult age and task demands. Neurobiol Aging 34(8):1925–1934. doi:10.1016/j.neurobiolaging.2013.02.012 CrossRefPubMedPubMedCentral

Cohen S, Kamarck T, Mermelstein R (1983) A global measure of perceived stress. J Health Soc Behav 24(4):385–396CrossRefPubMed

Correa N, Adali T, Li Y, Calhoun V (2005) Comparison of blind source separation algorithms for FMRI using a new Matlab toolbox: GIFT. Proc IEEE Int Conf Acoust Speech Signal Process 5:401–404

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(8):1856–1864. doi:10.1093/cercor/bhm207 CrossRefPubMed

De Vogelaere F, Santens P, Achten E, Boon P, Vingerhoets G (2012) Altered default-mode network activation in mild cognitive impairment compared with healthy aging. Neuroradiology 54(11):1195–1206. doi:10.1007/s00234-012-1036-6 CrossRefPubMed

Dennis AN, Cabeza R (2008) Neuroimaging of healthy cognitive aging. In: Salthouse FIMCTA (ed) Handbook of aging and cognition. Erlbaum, Mahwah

Dias-Ferreira E, Sousa JC, Melo I, Morgado P, Mesquita AR, Cerqueira JJ, Costa RM, Sousa N (2009) Chronic stress causes frontostriatal reorganization and affects decision-making. Science (New York, NY) 325(5940):621–625CrossRef

Ferreira LK, Busatto GF (2013) Resting-state functional connectivity in normal brain aging. Neurosci Biobehav Rev 37(3):384–400. doi:10.1016/j.neubiorev.2013.01.017 CrossRefPubMed

Fjell AM, McEvoy L, Holland D, Dale AM, Walhovd KB, Alzheimer’s Disease Neuroimaging I (2014) What is normal in normal aging? Effects of aging, amyloid and Alzheimer’s disease on the cerebral cortex and the hippocampus. Prog Neurobiol 117:20–40. doi:10.1016/j.pneurobio.2014.02.004 CrossRefPubMedPubMedCentral

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(3):189–198CrossRefPubMed

Fox MD, Snyder AZ, Vincent JL, Corbetta M, Van Essen DC, Raichle ME (2005) The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci USA 102(27):9673–9678. doi:10.1073/pnas.0504136102 CrossRefPubMedPubMedCentral

Frazier PA, Tix AP, Barron KE (2004) Testing moderator and mediator effects in counseling psychology research. J Couns Psychol 51(1):115–134. doi:10.1037/0022-0167.51.1.115 CrossRef

Giugni E, Vadala R, De Vincentiis C, Colica C, Bastianello S (2010) The brain’s default mode network: a mind “sentinel” role? Funct Neurol 25(4):189–190PubMed

Grady CL, Springer MV, Hongwanishkul D, McIntosh AR, Winocur G (2006) Age-related changes in brain activity across the adult lifespan. J Cogn Neurosci 18(2):227–241. doi:10.1162/089892906775783705 CrossRefPubMed

Grady CL, Protzner AB, Kovacevic N, Strother SC, Afshin-Pour B, Wojtowicz M, Anderson JA, Churchill N, McIntosh AR (2010) A multivariate analysis of age-related differences in default mode and task-positive networks across multiple cognitive domains. Cereb Cortex 20(6):1432–1447. doi:10.1093/cercor/bhp207 CrossRefPubMed

Greicius MD, Krasnow B, Reiss AL, Menon V (2003a) Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proc Natl Acad Sci USA 100(1):253–258. doi:10.1073/pnas.0135058100 CrossRefPubMed

Greicius MD, Krasnow B, Reiss AL, Menon V (2003b) Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proc Natl Acad Sci USA 98:4259–4264

Hafkemeijer A, van der Grond J, Rombouts SA (2012) Imaging the default mode network in aging and dementia. Biochim Biophys Acta 1822(3):431–441. doi:10.1016/j.bbadis.2011.07.008 CrossRefPubMed

Hansen NL, Lauritzen M, Mortensen EL, Osler M, Avlund K, Fagerlund B, Rostrup E (2014) Subclinical cognitive decline in middle-age is associated with reduced task-induced deactivation of the brain’s default mode network. Hum Brain Mapp 35(9):4488–4498. doi:10.1002/hbm.22489 CrossRefPubMed

Harrison BJ, Pujol J, Contreras-Rodriguez O, Soriano-Mas C, Lopez-Sola M, Deus J, Ortiz H, Blanco-Hinojo L, Alonso P, Hernandez-Ribas R, Cardoner N, Menchon JM (2011) Task-induced deactivation from rest extends beyond the default mode brain network. PLoS One 6(7):e22964. doi:10.1371/journal.pone.0022964 CrossRefPubMedPubMedCentral

Himberg J, Hyvarinen A, Esposito F (2004) Validating the independent components of neuroimaging time series via clustering and visualization. Neuroimage 22(3):1214–1222. doi:10.1016/j.neuroimage.2004.03.027 CrossRefPubMed

Huang CC, Hsieh WJ, Lee PL, Peng LN, Liu LK, Lee WJ, Huang JK, Chen LK, Lin CP (2015) Age-related changes in resting-state networks of a large sample size of healthy elderly. CNS Neurosci Ther. doi:10.1111/cns.12396

Kerestes R, Davey CG, Stephanou K, Whittle S, Harrison BJ (2013) Functional brain imaging studies of youth depression: a systematic review. Neuroimage Clin 4:209–231. doi:10.1016/j.nicl.2013.11.009 CrossRefPubMedPubMedCentral

Landin-Romero R, McKenna PJ, Salgado-Pineda P, Sarro S, Aguirre C, Sarri C, Compte A, Bosque C, Blanch J, Salvador R, Pomarol-Clotet E (2015) Failure of deactivation in the default mode network: a trait marker for schizophrenia? Psychol Med 45:1315–1325. doi:10.1017/S0033291714002426 CrossRefPubMed

Liao W, Chen H, Feng Y, Mantini D, Gentili C, Pan Z, Ding J, Duan X, Qiu C, Lui S, Gong Q, Zhang W (2010) Selective aberrant functional connectivity of resting state networks in social anxiety disorder. Neuroimage 52(4):1549–1558. doi:10.1016/j.neuroimage.2010.05.010 CrossRefPubMed

Marstaller L, Williams M, Rich A, Savage G, Burianova H (2015) Aging and large-scale functional networks: white matter integrity, gray matter volume, and functional connectivity in the resting state. Neuroscience 290:369–378. doi:10.1016/j.neuroscience.2015.01.049 CrossRefPubMed

Mason MF, Norton MI, Van Horn JD, Wegner DM, Grafton ST, Macrae CN (2007) Wandering minds: the default network and stimulus independent thought. Science (New York, NY) 315:393–395CrossRef

Meda SA, Gill A, Stevens MC, Lorenzoni RP, Glahn DC, Calhoun VD, Sweeney JA, Tamminga CA, Keshavan MS, Thaker G, Pearlson GD (2012) Differences in resting-state functional magnetic resonance imaging functional network connectivity between schizophrenia and psychotic bipolar probands and their unaffected first-degree relatives. Biol Psychiatry 71(10):881–889. doi:10.1016/j.biopsych.2012.01.025 CrossRefPubMedPubMedCentral

Meunier D, Stamatakis EA, Tyler LK (2014) Age-related functional reorganization, structural changes, and preserved cognition. Neurobiol Aging 35(1):42–54. doi:10.1016/j.neurobiolaging.2013.07.003 CrossRefPubMed

Mowinckel AM, Espeseth T, Westlye LT (2012) Network-specific effects of age and in-scanner subject motion: a resting-state fMRI study of 238 healthy adults. Neuroimage 63(3):1364–1373. doi:10.1016/j.neuroimage.2012.08.004 CrossRefPubMed

Owen AM, McMillan KM, Laird AR, Bullmore E (2005) N-back working memory paradigm: a meta-analysis of normative functional neuroimaging studies. Hum Brain Mapp 25(1):46–59. doi:10.1002/hbm.20131 CrossRefPubMed

Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL (2001) A default mode of brain function. Proc Natl Acad Sci 98:676–682CrossRefPubMedPubMedCentral

Sambataro F, Murty VP, Callicott JH, Tan HY, Das S, Weinberger DR, Mattay VS (2010) Age-related alterations in default mode network: impact on working memory performance. Neurobiol Aging 31(5):839–852. doi:10.1016/j.neurobiolaging.2008.05.022 CrossRefPubMed

Sampaio A, Soares JM, Coutinho J, Sousa N, Goncalves OF (2013) The big five default brain: functional evidence. Brain Struct Funct. doi:10.1007/s00429-013-0610-y

Santos NC, Costa PS, Cunha P, Cotter J, Sampaio A, Zihl J, Almeida OF, Cerqueira JJ, Palha JA, Sousa N (2013) Mood is a key determinant of cognitive performance in community-dwelling older adults: a cross-sectional analysis. Age 35(5):1983–1993. doi:10.1007/s11357-012-9482-y CrossRefPubMed

Sexton CE, Allan CL, Le Masurier M, McDermott LM, Kalu UG, Herrmann LL, Maurer M, Bradley KM, Mackay CE, Ebmeier KP (2012) Magnetic resonance imaging in late-life depression: multimodal examination of network disruption. Arch Gen Psychiatry 69(7):680–689. doi:10.1001/archgenpsychiatry.2011.1862 CrossRefPubMed

Sheline YI, Barch DM, Price JL, Rundle MM, Vaishnavi SN, Snyder AZ, Mintun MA, Wang S, Coalson RS, Raichle ME (2009) The default mode network and self-referential processes in depression. Proc Natl Acad Sci USA 106(6):1942–1947. doi:10.1073/pnas.0812686106 CrossRefPubMedPubMedCentral

Shirer WR, Ryali S, Rykhlevskaia E, Menon V, Greicius MD (2012) Decoding subject-driven cognitive states with whole-brain connectivity patterns. Cereb Cortex 22(1):158–165. doi:10.1093/cercor/bhr099 CrossRefPubMed

Soares JM, Sampaio A, Ferreira LM, Santos NC, Marques F, Palha JA, Cerqueira JJ, Sousa N (2012) Stress-induced changes in human decision-making are reversible. Transl Psychiatry 2:e131. doi:10.1038/tp.2012.59 CrossRefPubMedPubMedCentral

Soares JM, Sampaio A, Ferreira LM, Santos NC, Marques P, Marques F, Palha JA, Cerqueira JJ, Sousa N (2013a) Stress impact on resting state brain networks. PLoS One 8(6):e66500. doi:10.1371/journal.pone.0066500 CrossRefPubMedPubMedCentral

Soares JM, Sampaio A, Marques P, Ferreira LM, Santos NC, Marques F, Palha JA, Cerqueira JJ, Sousa N (2013b) Plasticity of resting state brain networks in recovery from stress. Front Hum Neurosci 7:919. doi:10.3389/fnhum.2013.00919 CrossRefPubMedPubMedCentral

Soares JM, Marques P, Magalhaes R, Santos NC, Sousa N (2014) Brain structure across the lifespan: the influence of stress and mood. Front Aging Neurosci 6:330. doi:10.3389/fnagi.2014.00330 CrossRefPubMedPubMedCentral

Sousa N, Lukoyanov NV, Madeira MD, Almeida OF, Paula-Barbosa MM (2000) Reorganization of the morphology of hippocampal neurites and synapses after stress-induced damage correlates with behavioral improvement. Neuroscience 97(2):253–266CrossRefPubMed

Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15(1):273–289. doi:10.1006/nimg.2001.0978 CrossRefPubMed

Vaisvaser S, Lin T, Admon R, Podlipsky I, Greenman Y, Stern N, Fruchter E, Wald I, Pine DS, Tarrasch R, Bar-Haim Y, Hendler T (2013) Neural traces of stress: cortisol related sustained enhancement of amygdala-hippocampal functional connectivity. Front Hum Neurosci 7:313. doi:10.3389/fnhum.2013.00313 CrossRefPubMedPubMedCentral

Veer IM, Beckmann CF, van Tol MJ, Ferrarini L, Milles J, Veltman DJ, Aleman A, van Buchem MA, van der Wee NJ, Rombouts SA (2010) Whole brain resting-state analysis reveals decreased functional connectivity in major depression. Front Syst Neurosci. doi:10.3389/fnsys.2010.00041 PubMedPubMedCentral

Wang L, Hermens DF, Hickie IB, Lagopoulos J (2012) A systematic review of resting-state functional-MRI studies in major depression. J Affect Disord 142(1–3):6–12. doi:10.1016/j.jad.2012.04.013 CrossRefPubMed

Wang Y, Chen K, Zhang J, Yao L, Li K, Jin Z, Ye Q, Guo X (2014) Aging influence on gray matter structural associations within the default mode network utilizing bayesian network modeling. Front Aging Neurosci 6:105. doi:10.3389/fnagi.2014.00105 PubMedPubMedCentral

Whitfield-Gabrieli S, Ford JM (2012) Default mode network activity and connectivity in psychopathology. Annu Rev Clin Psychol 8:49–76. doi:10.1146/annurev-clinpsy-032511-143049 CrossRefPubMed

Wu M, Andreescu C, Butters MA, Tamburo R, Reynolds CF 3rd, Aizenstein H (2011) Default-mode network connectivity and white matter burden in late-life depression. Psychiatry Res 194(1):39–46. doi:10.1016/j.pscychresns.2011.04.003 CrossRefPubMedPubMedCentral

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(1):37–49CrossRefPubMed

Yuen EY, Wei J, Liu W, Zhong P, Li X, Yan Z (2012) Repeated stress causes cognitive impairment by suppressing glutamate receptor expression and function in prefrontal cortex. Neuron 73(5):962–977. doi:10.1016/j.neuron.2011.12.033 CrossRefPubMedPubMedCentral

Zhu X, Wang X, Xiao J, Liao J, Zhong M, Wang W, Yao S (2012) Evidence of a dissociation pattern in resting-state default mode network connectivity in first-episode, treatment-naive major depression patients. Biol Psychiatry 71(7):611–617. doi:10.1016/j.biopsych.2011.10.035 CrossRefPubMed

Zuo XN, Kelly C, Adelstein JS, Klein DF, Castellanos FX, Milham MP (2010) Reliable intrinsic connectivity networks: test–retest evaluation using ICA and dual regression approach. Neuroimage 49(3):2163–2177. doi:10.1016/j.neuroimage.2009.10.080 CrossRefPubMed

Title: The association between stress and mood across the adult lifespan on default mode network
Authors: José Miguel Soares
Paulo Marques
Ricardo Magalhães
Nadine Correia Santos
Nuno Sousa
Publication date: 01-01-2017
Publisher: Springer Berlin Heidelberg
Published in: Brain Structure and Function / Issue 1/2017
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-016-1203-3

At a glance: The STEP trials

Springer Medicine

The association between stress and mood across the adult lifespan on default mode network

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

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