Top

Published in:

01-01-2014 | Original Article

Interleukin-1 beta C-511T polymorphism modulates functional connectivity of anterior midcingulate cortex in non-demented elderly Han males

Authors: Pei-Chi Tu, Tung-Ping Su, Chu-Chung Huang, Albert C. Yang, Heng-Liang Yeh, Chen-Jee Hong, Ying-Jay Liou, Mu-En Liu, Ching-Po Lin, Shih-Jen Tsai

Published in: Brain Structure and Function | Issue 1/2014

Abstract

Recent resting fMRI studies have suggested that the functional connectivity of the brain’s large-scale networks is associated with the cognitive decline of aging and is modulated by genetic factors. Our previous study found a significant association between interleukin-1 (IL-1 beta) C-511T polymorphism and working memory performance among elderly people. This study investigates the effects of IL-1 beta C-511T polymorphism on the functional connectivity of the cognitive division of the cingulate cortex [i.e., the anterior midcingulate (aMCC)] in non-demented Han elderly people and tests the hypothesis that T/T carriers are associated with lowered FC. Non-demented elderly males (n = 95) received resting MRI scanning, genotyping, and cognitive evaluation using the cognitive abilities screening instrument (CASI) and the Wechsler digit span task test. The functional connectivity map in each subject was derived based on positive correlations of low-frequency fMRI fluctuations with a seed in the aMCC according to structural definition. Between-group difference was compared by random effect analysis. Compared to the C/C or C/T carriers, the T/T carriers had a significantly worse CASI performance, especially in the abstraction scores. For the functional connectivity analysis, the T/T carriers exhibited significantly lower functional connectivity with several prefrontal areas and the left putamen. The cortico-striatal connection between the aMCC and left putamen was correlated with the CASI abstraction and attention scores. The results were consistent with our hypothesis and supported that the brains’ functional connectivity in elderly people may be modulated by genetic polymorphism associated with local inflammation processes.

Allen G, Barnard H, McColl R, Hester AL, Fields JA, Weiner MF, Ringe WK, Lipton AM, Brooker M, McDonald E, Rubin CD, Cullum CM (2007) Reduced hippocampal functional connectivity in Alzheimer disease. Arch Neurol 64:1482–1487PubMedCrossRef

Andrews-Hanna JR, Snyder AZ, Vincent JL, Lustig C, Head D, Raichle ME, Buckner RL (2007) Disruption of large-scale brain systems in advanced aging. Neuron 56:924–935PubMedCentralPubMedCrossRef

Biswal B, Yetkin FZ, Haughton VM, Hyde JS (1995) Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 34:537–541PubMedCrossRef

Braver TS, Cohen JD (1999) Dopamine, cognitive control, and schizophrenia: the gating model. Prog Brain Res 121:327–349PubMedCrossRef

Braver TS, Barch DM, Cohen JD (1999) Cognition and control in schizophrenia: a computational model of dopamine and prefrontal function. Biol Psychiatry 46:312–328PubMedCrossRef

Dennis NA, Browndyke JN, Stokes J, Need A, Burke JR, Welsh-Bohmer KA, Cabeza R (2010) Temporal lobe functional activity and connectivity in young adult APOE varepsilon4 carriers. Alzheimers Dement 6:303–311PubMedCentralPubMedCrossRef

Di Martino A, Scheres A, Margulies DS, Kelly AM, Uddin LQ, Shehzad Z, Biswal B, Walters JR, Castellanos FX, Milham MP (2008) Functional connectivity of human striatum: a resting state FMRI study. Cereb Cortex 18:2735–2747PubMedCrossRef

Dosenbach NU, Fair DA, Miezin FM, Cohen AL, Wenger KK, Dosenbach RA, Fox MD, Snyder AZ, Vincent JL, Raichle ME, Schlaggar BL, Petersen SE (2007) Distinct brain networks for adaptive and stable task control in humans. Proc Natl Acad Sci USA 104:11073–11078PubMedCrossRef

Dosenbach NU, Fair DA, Cohen AL, Schlaggar BL, Petersen SE (2008) A dual-networks architecture of top-down control. Trends Cogn Sci 12:99–105PubMedCentralPubMedCrossRef

Drzezga A, Becker JA, Van Dijk KR, Sreenivasan A, Talukdar T, Sullivan C, Schultz AP, Sepulcre J, Putcha D, Greve D, Johnson KA, Sperling RA (2011) Neuronal dysfunction and disconnection of cortical hubs in non-demented subjects with elevated amyloid burden. Brain 134:1635–1646PubMedCrossRef

Filippini N, Ebmeier KP, MacIntosh BJ, Trachtenberg AJ, Frisoni GB, Wilcock GK, Beckmann CF, Smith SM, Matthews PM, Mackay CE (2011) Differential effects of the APOE genotype on brain function across the lifespan. Neuroimage 54:602–610PubMedCrossRef

Glahn DC, Winkler AM, Kochunov P, Almasy L, Duggirala R, Carless MA, Curran JC, Olvera RL, Laird AR, Smith SM, Beckmann CF, Fox PT, Blangero J (2010) Genetic control over the resting brain. Proc Natl Acad Sci USA 107:1223–1228PubMedCrossRef

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

Greicius MD, Srivastava G, Reiss AL, Menon V (2004) Default-mode network activity distinguishes Alzheimer’s disease from healthy aging: evidence from functional MRI. Proc Natl Acad Sci USA 101:4637–4642PubMedCrossRef

Hall SK, Perregaux DG, Gabel CA, Woodworth T, Durham LK, Huizinga TW, Breedveld FC, Seymour AB (2004) Correlation of polymorphic variation in the promoter region of the interleukin-1 beta gene with secretion of interleukin-1 beta protein. Arthritis Rheum 50:1976–1983PubMedCrossRef

Han SD, Bondi MW (2008) Revision of the apolipoprotein E compensatory mechanism recruitment hypothesis. Alzheimers Dement 4:251–254PubMedCrossRef

Hedden T, Gabrieli JD (2004) Insights into the ageing mind: a view from cognitive neuroscience. Nat Rev Neurosci 5:87–96PubMedCrossRef

Hedden T, Van Dijk KR, Becker JA, Mehta A, Sperling RA, Johnson KA, Buckner RL (2009) Disruption of functional connectivity in clinically normal older adults harboring amyloid burden. J Neurosci 29:12686–12694PubMedCentralPubMedCrossRef

Helmich RC, Derikx LC, Bakker M, Scheeringa R, Bloem BR, Toni I (2010) Spatial remapping of cortico-striatal connectivity in Parkinson’s disease. Cereb Cortex 20:1175–1186PubMedCrossRef

Li Q, Cheung C, Wei R, Cheung V, Hui ES, You Y, Wong P, Chua SE, McAlonan GM, Wu EX (2010) Voxel-based analysis of postnatal white matter microstructure in mice exposed to immune challenge in early or late pregnancy. Neuroimage 52:1–8PubMedCrossRef

Liu HC, Chou P, Lin KN, Wang SJ, Fuh JL, Lin HC, Liu CY, Wu GS, Larson EB, White LR et al (1994) Assessing cognitive abilities and dementia in a predominantly illiterate population of older individuals in Kinmen. Psychol Med 24:763–770PubMedCrossRef

Liu B, Song M, Li J, Liu Y, Li K, Yu C, Jiang T (2010) Prefrontal-related functional connectivities within the default network are modulated by COMT val158met in healthy young adults. J Neurosci 30:64–69PubMedCrossRef

Machulda MM, Jones DT, Vemuri P, McDade E, Avula R, Przybelski S, Boeve BF, Knopman DS, Petersen RC, Jack CR Jr (2011) Effect of APOE ε4 status on intrinsic network connectivity in cognitively normal elderly subjects. Arch Neurol 68:1131–1136

Meisenzahl EM, Rujescu D, Kirner A, Giegling I, Kathmann N, Leinsinger G, Maag K, Hegerl U, Hahn K, Moller HJ (2001) Association of an interleukin-1beta genetic polymorphism with altered brain structure in patients with schizophrenia. Am J Psychiatry 158:1316–1319PubMedCrossRef

Mormino EC, Smiljic A, Hayenga AO, Onami SH, Greicius MD, Rabinovici GD, Janabi M, Baker SL, Yen IV, Madison CM, Miller BL, Jagust WJ (2011) Relationships between beta-amyloid and functional connectivity in different components of the default mode network in aging. Cereb Cortex 21:2399–2407

Murphy K, Birn RM, Handwerker DA, Jones TB, Bandettini PA (2009) The impact of global signal regression on resting state correlations: are anti-correlated networks introduced? Neuroimage 44:893–905PubMedCentralPubMedCrossRef

Murty VP, Sambataro F, Radulescu E, Altamura M, Iudicello J, Zoltick B, Weinberger DR, Goldberg TE, Mattay VS (2011) Selective updating of working memory content modulates meso-cortico-striatal activity. Neuroimage 57:1264–1272PubMedCrossRef

Onoda K, Ishihara M, Yamaguchi S (2012) Decreased functional connectivity by aging is associated with cognitive decline. J Cogn Neurosci 24:2186–2198PubMedCrossRef

Papiol S, Molina V, Rosa A, Sanz J, Palomo T, Fananas L (2007) Effect of interleukin-1beta gene functional polymorphism on dorsolateral prefrontal cortex activity in schizophrenic patients. Am J Med Genet B Neuropsychiatr Genet 144B:1090–1093PubMedCrossRef

Papiol S, Molina V, Desco M, Rosa A, Reig S, Sanz J, Palomo T, Fananas L (2008) Gray matter deficits in bipolar disorder are associated with genetic variability at interleukin-1 beta gene (2q13). Genes Brain Behav 7:796–801PubMedCrossRef

Parent A, Hazrati LN (1995) Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop. Brain Res Brain Res Rev 20:91–127PubMedCrossRef

Pociot F, Molvig J, Wogensen L, Worsaae H, Nerup J (1992) A TaqI polymorphism in the human interleukin-1 beta (IL-1 beta) gene correlates with IL-1 beta secretion in vitro. Eur J Clin Invest 22:396–402PubMedCrossRef

Postuma RB, Dagher A (2006) Basal ganglia functional connectivity based on a meta-analysis of 126 positron emission tomography and functional magnetic resonance imaging publications. Cereb Cortex 16:1508–1521PubMedCrossRef

Seeley WW, Menon V, Schatzberg AF, Keller J, Glover GH, Kenna H, Reiss AL, Greicius MD (2007) Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci 27:2349–2356PubMedCentralPubMedCrossRef

Sheehan DV, Lecrubier Y, Sheehan KH, Amorim P, Janavs J, Weiller E, Hergueta T, Baker R, Dunbar GC (1998) The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. J Clin Psychiatry 59(Suppl 20):22–33 (quiz 34–57)PubMed

Sheline YI, Morris JC, Snyder AZ, Price JL, Yan Z, D’Angelo G, Liu C, Dixit S, Benzinger T, Fagan A, Goate A, Mintun MA (2010a) APOE4 allele disrupts resting state fMRI connectivity in the absence of amyloid plaques or decreased CSF Abeta42. J Neurosci 30:17035–17040PubMedCentralPubMedCrossRef

Sheline YI, Raichle ME, Snyder AZ, Morris JC, Head D, Wang S, Mintun MA (2010b) Amyloid plaques disrupt resting state default mode network connectivity in cognitively normal elderly. Biol Psychiatry 67:584–587PubMedCentralPubMedCrossRef

Sun X, Zhang X, Chen X, Zhang P, Bao M, Zhang D, Chen J, He S, Hu X (2005) Age-dependent brain activation during forward and backward digit recall revealed by fMRI. Neuroimage 26:36–47PubMedCrossRef

Tanaka S, Kondo H, Kanda K, Ashino T, Nakamachi T, Sekikawa K, Iwakura Y, Shioda S, Numazawa S, Yoshida T (2011) Involvement of interleukin-1 in lipopolysaccharide-induced microglial activation and learning and memory deficits. J Neurosci Res 89:506–514PubMedCrossRef

Teng EL, Hasegawa K, Homma A, Imai Y, Larson E, Graves A, Sugimoto K, Yamaguchi T, Sasaki H, Chiu D et al (1994) The Cognitive Abilities Screening Instrument (CASI): a practical test for cross-cultural epidemiological studies of dementia. Int Psychogeriatr 6:45–58 (discussion 62)PubMedCrossRef

Thomason ME, Yoo DJ, Glover GH, Gotlib IH (2009) BDNF genotype modulates resting functional connectivity in children. Front Hum Neurosci 3:55PubMedCentralPubMedCrossRef

Trompet S, de Craen AJ, Slagboom P, Shepherd J, Blauw GJ, Murphy MB, Bollen EL, Buckley BM, Ford I, Gaw A, Macfarlane PW, Packard CJ, Stott DJ, Jukema JW, Westendorp RG (2008) Genetic variation in the interleukin-1 beta-converting enzyme associates with cognitive function. The PROSPER study. Brain 131:1069–1077PubMedCrossRef

Tsai SJ, Hong CJ, Liu ME, Hou SJ, Yen FC, Hsieh CH, Liou YJ (2010) Interleukin-1 beta (C-511T) genetic polymorphism is associated with cognitive performance in elderly males without dementia. Neurobiol Aging 31:1950–1955PubMedCrossRef

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 15:273–289PubMedCrossRef

Vincent JL, Snyder AZ, Fox MD, Shannon BJ, Andrews JR, Raichle ME, Buckner RL (2006) Coherent spontaneous activity identifies a hippocampal-parietal memory network. J Neurophysiol 96:3517–3531PubMedCrossRef

Vogt BA (2005) Pain and emotion interactions in subregions of the cingulate gyrus. Nat Rev Neurosci 6:533–544PubMedCentralPubMedCrossRef

Wang L, Zang Y, He Y, Liang M, Zhang X, Tian L, Wu T, Jiang T, Li K (2006) Changes in hippocampal connectivity in the early stages of Alzheimer’s disease: evidence from resting state fMRI. Neuroimage 31:496–504PubMedCrossRef

Ystad M, Hodneland E, Adolfsdottir S, Haasz J, Lundervold AJ, Eichele T, Lundervold A (2011) Cortico-striatal connectivity and cognition in normal aging: a combined DTI and resting state fMRI study. Neuroimage 55:24–31PubMedCrossRef

Yu C, Zhou Y, Liu Y, Jiang T, Dong H, Zhang Y, Walter M (2011) Functional segregation of the human cingulate cortex is confirmed by functional connectivity based neuroanatomical parcellation. Neuroimage 54:2571–2581PubMedCrossRef

Title: Interleukin-1 beta C-511T polymorphism modulates functional connectivity of anterior midcingulate cortex in non-demented elderly Han males
Authors: Pei-Chi Tu
Tung-Ping Su
Chu-Chung Huang
Albert C. Yang
Heng-Liang Yeh
Chen-Jee Hong
Ying-Jay Liou
Mu-En Liu
Ching-Po Lin
Shih-Jen Tsai
Publication date: 01-01-2014
Publisher: Springer Berlin Heidelberg
Published in: Brain Structure and Function / Issue 1/2014
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-012-0484-4

At a glance: The STEP trials

Springer Medicine

Interleukin-1 beta C-511T polymorphism modulates functional connectivity of anterior midcingulate cortex in non-demented elderly Han males

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 1/2014

Variations in midcingulate morphology are related to ERP indices of cognitive control

Erratum to: Comparative dynamics of MAPK/ERK signalling components and immediate early genes in the hippocampus and amygdala following contextual fear conditioning and retrieval

Immunohistochemical localization of two types of choline acetyltransferase in neurons and sensory cells of the octopus arm

Equations to describe brain size across the continuum of human lifespan

Perinatal and early postnatal reorganization of the subplate and related cellular compartments in the human cerebral wall as revealed by histological and MRI approaches

Differential expression of VGLUT1 or VGLUT2 in the trigeminothalamic or trigeminocerebellar projection neurons in the rat