Functional consequences of neurite orientation dispersion and density in humans across the adult lifespan

Journal of Neuroscience

Volumn 35, Issue 4, 2015, Pages 1753-1762

  Nazeri, Arash ^a,b   Chakravart, Mallar ^d   Rotenberg, David J ^a   Rajji, Tarek K ^a,b,e   Rathi, Xyogesh ^f   Michailovich, Oleg V ^g   Voineskos, Aristotle N ^a,b,e  

^a CENTRE FOR ADDICTION AND MENTAL HEALTH   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c DOUGLAS MENTAL HEALTH UNIVERSITY INSTITUTE   (Canada)

^d MCGILL UNIVERSITY   (Canada)

^e UNIVERSITY OF TORONTO   (Canada)

^f HARVARD MEDICAL SCHOOL   (United States)

^g UNIVERSITY OF WATERLOO   (Canada)

Author keywords

Cognitive aging; Diffusion weighted MRI; GBSS; Gray matter; Neurite orientation dispersion; Structure function relationship

Indexed keywords

ADULT; AGE; AGED; AGING; ARTICLE; BEHAVIOR; CEREBELLUM; COGNITION; CONNECTOME; CORTICAL THICKNESS (BRAIN); DENDRITE; DIFFUSION WEIGHTED IMAGING; DSM-IV; EXPERIMENTAL COGNITIVE TEST; FEMALE; FRACTIONAL ANISOTROPY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GRAY MATTER; HIPPOCAMPUS; HUMAN; HUMAN EXPERIMENT; INTRANEURITE VOLUME FRACTION; LIFESPAN; MALE; MINI MENTAL STATE EXAMINATION; NERVOUS SYSTEM PARAMETERS; NEURITE ORIENTATION DISPERSION AND DENSITY IMAGING; NEURITE ORIENTATION DISPERSION INDEX; NEUROIMAGING; NORMAL HUMAN; PRIORITY JOURNAL; RESTING STATE NETWORK; SPATIAL ANALYSIS; STRUCTURE ACTIVITY RELATION; STRUCTURED INTERVIEW; TASK PERFORMANCE; URINALYSIS; WHITE MATTER; WORKING MEMORY; ANATOMY AND HISTOLOGY; ANISOTROPY; BLOOD; BRAIN; BRAIN MAPPING; CELL COUNT; CYTOLOGY; DIFFUSION TENSOR IMAGING; IMAGE PROCESSING; MIDDLE AGED; NERVE CELL; NEURITE; NONPARAMETRIC TEST; PHYSIOLOGY; REST; VASCULARIZATION; VERY ELDERLY; YOUNG ADULT;

OXYGEN;

ADULT; AGED; AGED, 80 AND OVER; AGING; ANISOTROPY; BRAIN; BRAIN MAPPING; CELL COUNT; DIFFUSION TENSOR IMAGING; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MALE; MIDDLE AGED; NEURITES; NEURONS; OXYGEN; REST; STATISTICS, NONPARAMETRIC; YOUNG ADULT;

EID: 84921923580     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3979-14.2015     Document Type: Article

References (68)

1. Anderson B, Rutledge V (1996) Age and hemisphere effects on dendritic structure. Brain 119:1983–1990. CrossRef Medline
2. Assaf Y, Alexander DC, Jones DK, Bizzi A, Behrens TE, Clark CA, Cohen Y, Dyrby TB, Huppi PS, Knoesche TR, Lebihan D, Parker GJ, Poupon C, Poupon C, Anaby D, Anwander A, Bar L, Barazany D, Blumenfeld-Katzir T, De-Santis S, Duclap D, Figini M, Fischi E, Guevara P, Hubbard P, Hofstetter S, Jbabdi S, Kunz N, Lazeyras F, Lebois A, Liptrot MG, Lundell H, Mangin JF, Dominguez DM, Morozov D, Schreiber J, Seunarine K, Nava S, Poupon C, Riffert T, Sasson E, Schmitt B, Shemesh N, Sotiropoulos SN, Tavor I, Zhang HG, Zhou FL (2013) The CONNECT project: combining macro-and micro-structure. Neuroimage 80:273-282. CrossRef Medline
3. Avants BB, Tustison NJ, Wu J, Cook PA, Gee JC (2011) An open source multivariate framework for n-tissue segmentation with evaluation on public data. Neuroinformatics 9:381– 400.CrossRef Medline
4. Avants BB, Tustison NJ, Song G, Cook PA, Klein A, Gee JC (2011) A reproducible evaluation of ANTs similarity metric performance in brain image registration. Neuroimage 54:2033-2044.CrossRef Medline
5. Ball G, Srinivasan L, Aljabar P, Counsell SJ, Durighel G, Hajnal JV, Rutherford MA, Edwards AD (2013) Development of cortical microstructure in the preterm human brain. Proc Natl Acad Sci U S A 110:9541-9546.CrossRef Medline
6. Beckmann CF, Smith SM (2004) Probabilistic independent component analysis for functional magnetic resonance imaging. IEEE Trans Med Imaging 23:137-152.CrossRef Medline
7. 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 360:1001-1013.CrossRef Medline
8. Buell SJ, Coleman PD (1979) Dendritic growth in the aged human brain and failure of growth in senile dementia. Science 206:854-856.CrossRef Medline
9. Bullmore ET, Bassett DS (2011) Brain graphs: graphical models of the human brain connectome. Annu Rev Clin Psychol 7:113-140.CrossRef Medline
10. Chen S, Hillman DE (1999) Dying-back of Purkinje cell dendrites with synapse loss in aging rats. J Neurocytol 28:187-196.CrossRef Medline
11. Dale AM, Fischl B, Sereno MI (1999) Cortical surface-based analysis: I. Segmentation and surface reconstruction. Neuroimage 9:179 –194. CrossRef Medline
12. de Brabander JM, Kramers RJ, Uylings HB (1998) Layer-specific dendritic regression of pyramidal cells with ageing in the human prefrontal cortex. Eur J Neurosci 10:1261-1269.CrossRef Medline
13. Dickstein DL, Weaver CM, Luebke JI, Hof PR (2013) Dendritic spine changes associated with normal aging. Neuroscience 251:21-32.CrossRef Medline
14. Duan H, Wearne SL, Rocher AB, Macedo A, Morrison JH, Hof PR (2003) Age-related dendritic and spine changes in corticocortically projecting neurons in macaque monkeys. Cereb Cortex 13:950 –961.CrossRef Medline
15. Ferreira LK, Busatto GF (2013) Resting-state functional connectivity in normal brain aging. Neurosci Biobehav Rev 37:384-400.CrossRef Medline
16. Filippini N, MacIntosh BJ, Hough MG, Goodwin GM, Frisoni GB, Smith SM, Matthews PM, Beckmann CF, Mackay CE (2009) Distinct patterns of brain activity in young carriers of the APOE-_4 allele. Proc Natl Acad Sci U S A 106:7209 –7214. CrossRef Medline
17. Fischl B (2012) FreeSurfer. Neuroimage 62:774 –781. CrossRef Medline
18. Fischl B, Dale AM (2000) Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci U S A 97: 11050-11055.
19. CrossRef Medline Flood DG, Buell SJ, Defiore CH, Horwitz GJ, Coleman PD (1985) Agerelated dendritic growth in dentate gyrus of human brain is followed by regression in the ‘oldest old’. Brain Res 345:366 –368. CrossRef Medline
20. Friston KJ, Harrison L, Penny W (2003) Dynamic causal modelling. Neuroimage 19:1273-1302.
21. CrossRef Medline Glasser MF, Van Essen DC (2011) Mapping human cortical areas in vivo based on myelin content as revealed by T1-and T2-weighted MRI. J Neurosci 31:11597-11616.CrossRef Medline
22. Griffanti L, Salimi-Khorshidi G, Beckmann CF, Auerbach EJ, Douaud G, Sexton CE, Zsoldos E, Ebmeier KP, Filippini N, Mackay CE, Moeller S, Xu J, Yacoub E, Baselli G, Ugurbil K, Miller KL, Smith SM (2014) ICAbased artefact removal and accelerated fMRI acquisition for improved resting state network imaging. Neuroimage 95:232-247.CrossRef Medline
23. Grydeland H, Walhovd KB, Tamnes CK, Westlye LT, Fjell AM (2013) Intracortical myelin links with performance variability across the human lifespan: results from T1-and T2-weighted MRI myelin mapping and diffusion tensor imaging. J Neurosci 33:18618 –18630. CrossRef Medline
24. Jacobs B, Scheibel AB (1993) A quantitative dendritic analysis of Wernicke’s area in humans. I. Lifespan changes. J Comp Neurol 327:83-96.CrossRef Medline
25. Jacobs B, Driscoll L, Schalln M (1997) Life-span dendritic and spine changes in areas 10 and 18 of human cortex: A quantitative Golgi study. J Comp Neurol 386:661– 680. CrossRef Medline
26. Jenkinson M, Beckmann CF, Behrens TE, Woolrich MW, Smith SM (2012) Neuroimage 62:782-790.CrossRef Medline
27. Jespersen SN, Kroenke CD, Ostergaard L, Ackerman JJ, Yablonskiy DA (2007) Modeling dendrite density from magnetic resonance diffusion measurements. Neuroimage 34:1473-1486.CrossRef Medline
28. Kim SY, Chung K, Deisseroth K (2013) Light microscopy mapping of connections in the intact brain. Trends Cogn Sci 17:596 –599. CrossRef Medline
29. Koo BB, Hua N, Choi CH, Ronen I, Lee JM, Kim DS (2009) A framework to analyze partial volume effect on gray matter mean diffusivity measurements. Neuroimage 44:136 –144. CrossRef Medline
30. Kumazawa S, Yoshiura T, Honda H, Toyofuku F, Higashida Y (2010) Partial volume estimation and segmentation of brain tissue based on diffusion tensor MRI. Med Phys 37:1482-1490.CrossRef Medline
31. Liu T, Li H, Wong K, Tarokh A, Guo L, Wong ST (2007) Brain tissue segmentation based on DTI data
32. 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._zbap__: pdfs%3B12%3Bhttp://dx.doi.org/10.1016/01651781%3B/Border_http://dx.doi.org/10.1016/0165-1781_: pdfe%3B12__zbapx_(92)90005-N Medline
33. 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 63:1364 –1373. CrossRef Medline
34. Nakamura S, Akiguchi I, Kameyama M, Mizuno N (1985) Age-related changes of pyramidal cell basal dendrites in layers III and V of human motor cortex: a quantitative Golgi study. Acta Neuropathol 65:281-284.CrossRef Medline
35. Nichols TE, Holmes AP (2002) Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp 15:1-25.CrossRef Medline
36. Nyberg L, Salami A, Andersson M, Eriksson J, Kalpouzos G, Kauppi K, Lind J, Pudas S, Persson J, Nilsson LG (2010) Longitudinal evidence for diminished frontal cortex function in aging. Proc Natl Acad Sci U S A 107: 22682-22686.CrossRef Medline
37. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97-113.CrossRef Medline
38. Pasternak O, Sochen N, Gur Y, Intrator N, Assaf Y (2009) Free water elimination and mapping from diffusion MRI. Magn Reson Med 62:717-730.CrossRef Medline
39. Pasternak O, Westin CF, Bouix S, Seidman LJ, Goldstein JM, Woo TU, Petryshen TL, Mesholam-Gately RI, McCarley RW, Kikinis R, Shenton ME, Kubicki M (2012) Excessive extracellular volume reveals a neurodegenerative pattern in schizophrenia onset. J Neurosci 32:17365-17372.CrossRef Medline
40. Penzes P, Cahill ME, Jones KA, VanLeeuwen JE, Woolfrey KM (2011) Dendritic spine pathology in neuropsychiatric disorders. Nat Neurosci 14: 285-293.CrossRef Medline
41. Pereira JB, Valls-Pedret C, Ros E, Palacios E, Falcon C, Bargallo N, Bartres- Faz D, Wahlund LO, Westman E, Junque C (2014) Regional vulnerability of hippocampal subfields to aging measured by structural and diffusion MRI. Hippocampus 24:403– 414. CrossRef Medline
42. Preacher KJ, Hayes AF (2008) Asymptotic and resampling strategies for assessing and comparing indirect effects in multiple mediator models. Behav Res Methods 40:879-891.CrossRef Medline
43. Pyapali GK, Turner DA (1996) Increased dendritic extent in hippocampal CA1 neurons from aged F344 rats. Neurobiol Aging 17:601– 611. CrossRef Medline
44. Rathi Y, Pasternak O, Savadjiev P, Michailovich O, Bouix S, Kubicki M, Westin CF, Makris N, Shenton ME (2014) Gray matter alterations in early aging: A diffusion magnetic resonance imaging study. Hum Brain Mapp 35:3841-3856.CrossRef Medline
45. Raz N, Lindenberger U, Rodrigue KM, Kennedy KM, Head D, Williamson A, Dahle C, Gerstorf D, Acker JD (2005) Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. Cereb Cortex 15:1676 –1689. CrossRef Medline
46. Reisberg B, Franssen EH, Hasan SM, Monteiro I, Boksay I, Souren LEM, Kenowsky S, Auer SR, Elahi S, Kluger A (1999) Retrogenesis: clinical, physiologic, and pathologic mechanisms in brain aging, Alzheimer’s and other dementing processes. Eur Arch Psychiatry Clin Neurosci 249:28– 36. CrossRef Medline
47. Reitan RM, Wolfson D (1985) The Halstead-Reitan neuropsychological test battery: theory and clinical interpretation: Neuropsychology Tucson, AZ.
48. Rogers J, Zornetzer SF, Bloom FE, Mervis RE (1984) Senescent microstructural changes in rat cerebellum. Brain Res 292:23-32.CrossRef Medline
49. Roostaei T, Nazeri A, Sahraian MA, Minagar A (2014) The human cerebellum: a review of physiologic neuroanatomy. Neurol Clin 32:859-869.CrossRef Medline
50. Salimi-Khorshidi G, Douaud G, Beckmann CF, Glasser MF, Griffanti L, Smith SM (2014) Automatic denoising of functional MRI data: combining independent component analysis and hierarchical fusion of classifiers. Neuroimage 90:449-468.CrossRef Medline
51. Schmahmann JD, Pandya DN (1997) The cerebrocerebellar system. Int Rev Neurobiol 41:31– 60. CrossRef Medline
52. Schwarz CG, Reid RI, Gunter JL, Senjem ML, Przybelski SA, Zuk SM, Whitwell JL, Vemuri P, Josephs KA, Kantarci K, Thompson PM, Petersen RC, Jack CR Jr; Alzheimer’s Disease Neuroimaging Initiative (2014) Improved DTI registration allows voxel-based analysis that outperforms Tract-Based Spatial Statistics. Neuroimage 94:65-78.CrossRef Medline
53. Shepherd GM (2011) The microcircuit concept applied to cortical evolution: from three-layer to six-layer cortex. Front Neuroanat 5.
54. Smith SM (2002) Fast robust automated brain extraction.HumBrain Mapp 17:143-155.CrossRef Medline
55. Smith SM, Nichols TE (2009) Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage 44:83-98.CrossRef Medline
56. Smith SM, Jenkinson M, Johansen-Berg H, Rueckert D, Nichols TE, Mackay CE, Watkins KE, Ciccarelli O, Cader MZ, Matthews PM, Behrens TE (2006) Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 31:1487-1505.CrossRef Medline
57. Smith SM, Fox PT, Miller KL, Glahn DC, Fox PM, Mackay CE, Filippini N, Watkins KE, Toro R, Laird AR, Beckmann CF (2009) Correspondence of the brain’s functional architecture during activation and rest. Proc Natl Acad Sci U S A 106:13040 –13045. CrossRef Medline
58. Smith SM, Vidaurre D, Beckmann CF, Glasser MF, Jenkinson M, Miller KL, Nichols TE, Robinson EC, Salimi-Khorshidi G, Woolrich MW, Barch DM, Ugurbil K, Van Essen DC (2013) Functional connectomics from resting-state fMRI. Trends Cogn Sci 17:666-682.CrossRef Medline
59. Sotiropoulos SN, Behrens TE, Jbabdi S (2012) Ball and rackets: inferring fiber fanning from diffusion-weighted MRI. Neuroimage 60:1412-1425.CrossRef Medline
60. Sotiropoulos SN, Jbabdi S, Xu J, Andersson JL, Moeller S, Auerbach EJ, Glasser MF, Hernandez M, Sapiro G, Jenkinson M, Yacoub E, Lenglet C, Van Essen DC, Ugurbil K, Behrens TE, Behrens TE (2013) Advances in diffusion MRI acquisition and processing in the Human Connectome Project. Neuroimage 80:125-143.CrossRef Medline
61. Spruston N (2008) Pyramidal neurons: dendritic structure and synaptic integration. Nat Rev Neurosci 9:206 –221. CrossRef Medline
62. Trenerry MR, Crosson B, DeBoe J, Leber WR (1989) Stroop neuropsychological screening test manual. Odessa, FL: Psychological Assessment Resources.
63. Viswanathan A, Freeman RD (2007) Neurometabolic coupling in cerebral cortex reflects synaptic more than spiking activity. Nat Neurosci 10:1308– 1312. CrossRef Medline
64. Voets NL, Beckmann CF, Cole DM, Hong S, Bernasconi A, Bernasconi N (2012) Structural substrates for resting network disruption in temporal lobe epilepsy. Brain 135:2350 –2357. CrossRef Medline
65. Wechsler D (1997) The Wechsler Memory Scale. San Antonio, TX: Psychological Corporation, Harcourt Brace Jovanovich.
66. Winston GP, Micallef C, Symms MR, Alexander DC, Duncan JS, Zhang H (2014) Advanced diffusion imaging sequences could aid assessing patients with focal cortical dysplasia and epilepsy. Epilepsy Res 108:336– 339. CrossRef Medline
67. Young ME, Ohm DT, Dumitriu D, Rapp PR, Morrison JH (2014) Differential effects of aging on dendritic spines in visual cortex and prefrontal cortex of the rhesus monkey. Neuroscience 274:33– 43. CrossRef Medline
68. Zhang H, Schneider T, Wheeler-Kingshott CA, Alexander DC (2012) NODDI: practical in vivo neurite orientation dispersion and density imaging of the human brain. Neuroimage 61:1000 –1016. CrossRef Medline