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Atlasing the frontal lobe connections and their variability due to age and education: a spherical deconvolution tractography study

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Abstract

In neuroscience, there is a growing consensus that higher cognitive functions may be supported by distributed networks involving different cerebral regions, rather than by single brain areas. Communication within these networks is mediated by white matter tracts and is particularly prominent in the frontal lobes for the control and integration of information. However, the detailed mapping of frontal connections remains incomplete, albeit crucial to an increased understanding of these cognitive functions. Based on 47 high-resolution diffusion-weighted imaging datasets (age range 22–71 years), we built a statistical normative atlas of the frontal lobe connections in stereotaxic space, using state-of-the-art spherical deconvolution tractography. We dissected 55 tracts including U-shaped fibers. We further characterized these tracts by measuring their correlation with age and education level. We reported age-related differences in the microstructural organization of several, specific frontal fiber tracts, but found no correlation with education level. Future voxel-based analyses, such as voxel-based morphometry or tract-based spatial statistics studies, may benefit from our atlas by identifying the tracts and networks involved in frontal functions. Our atlas will also build the capacity of clinicians to further understand the mechanisms involved in brain recovery and plasticity, as well as assist clinicians in the diagnosis of disconnection or abnormality within specific tracts of individual patients with various brain diseases.

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References

  • Aggleton JP, O’Mara SM, Vann SD, Wright NF, Tsanov M, Erichsen JT (2010) Hippocampal-anterior thalamic pathways for memory: uncovering a network of direct and indirect actions. Eur J Neurosci 31(12):2292–2307

    Article  PubMed  PubMed Central  Google Scholar 

  • Azuar C, Reyes P, Slachevsky A, Volle E, Kinkingnehun S, Kouneiher F, Bravo E, Dubois B, Koechlin E, Levy R (2014) Testing the model of caudo-rostral organization of cognitive control in the human with frontal lesions. Neuroimage 84:1053–1060

    Article  CAS  PubMed  Google Scholar 

  • Badre D (2008) Cognitive control, hierarchy, and the rostro-caudal organization of the frontal lobes. Trends Cogn Sci 12(5):193–200

    Article  PubMed  Google Scholar 

  • Badre D, D’Esposito M (2007) Functional magnetic resonance imaging evidence for a hierarchical organization of the prefrontal cortex. J Cogn Neurosci 19(12):2082–2099

    Article  PubMed  Google Scholar 

  • Barbas H, Mesulam MM (1981) Organization of afferent input to subdivisions of area 8 in the rhesus monkey. J Comp Neurol 200(3):407–431

  • Barrick TR, Lawes IN, Mackay CE, Clark CA (2007) White matter pathway asymmetry underlies functional lateralization. Cereb Cortex 17(3):591–598

    Article  PubMed  Google Scholar 

  • Barrick TR, Charlton RA, Clark CA, Markus HS (2010) White matter structural decline in normal ageing: a prospective longitudinal study using tract-based spatial statistics. Neuroimage 51(2):565–577

    Article  PubMed  Google Scholar 

  • Bastin ME, Piatkowski JP, Storkey AJ, Brown LJ, Maclullich AM, Clayden JD (2008) Tract shape modelling provides evidence of topological change in corpus callosum genu during normal ageing. Neuroimage 43(1):20–28

    Article  PubMed  Google Scholar 

  • Bastin C, Yakushev I, Bahri MA, Fellgiebel A, Eustache F, Landeau B, Scheurich A, Feyers D, Collette F, Chetelat G, Salmon E (2012) Cognitive reserve impacts on inter-individual variability in resting-state cerebral metabolism in normal aging. Neuroimage 63(2):713–722

    Article  PubMed  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Royal Statistical Soc Series B (Methodological) 289–300

  • Bishop NA, Lu T, Yankner BA (2010) Neural mechanisms of ageing and cognitive decline. Nature 464(7288):529–535

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brayne C, Ince PG, Keage HA, McKeith IG, Matthews FE, Polvikoski T, Sulkava R (2010) Education, the brain and dementia: neuroprotection or compensation? Brain 133(Pt 8):2210–2216

    Article  PubMed  Google Scholar 

  • Brett M, Leff AP, Rorden C, Ashburner J (2001) Spatial normalization of brain images with focal lesions using cost function masking. Neuroimage 14(2):486–500

    Article  CAS  PubMed  Google Scholar 

  • Brickman AM, Stern Y (2009) Aging and memory in humans. In: S LR (ed) Encyclopedia of neuroscience. Academic Press, Oxford, pp 175–180

    Chapter  Google Scholar 

  • Burgess PW, Alderman N, Volle E, Benoit RG, Gilbert SJ (2009) Mesulam’s frontal lobe mystery re-examined. Restor Neurol Neurosci 27:493–506

    PubMed  Google Scholar 

  • Cabeza R, Dennis N (2012) Frontal lobes and aging: deterioration and compensation. In: Stuss D, Knight R (eds) Principles of frontal lobe function, 2nd edn., pp 628–652

    Google Scholar 

  • Cabeza R, Anderson ND, Locantore JK, McIntosh AR (2002) Aging gracefully: compensatory brain activity in high-performing older adults. Neuroimage 17(3):1394–1402

    Article  PubMed  Google Scholar 

  • Catani M (2006) Diffusion tensor magnetic resonance imaging tractography in cognitive disorders. Curr Opin Neurol 19(6):599–606

    Article  PubMed  Google Scholar 

  • Catani M, Thiebaut de Schotten M (2008) A diffusion tensor imaging tractography atlas for virtual in vivo dissections. Cortex 44(8):1105–1132

    Article  PubMed  Google Scholar 

  • Catani M, Howard RJ, Pajevic S, Jones DK (2002) Virtual in vivo interactive dissection of white matter fasciculi in the human brain. NeuroImage 17(1):77–94

    Article  PubMed  Google Scholar 

  • Catani M, Jones DK, ffytche DH (2005) Perisylvian language networks of the human brain. Ann Neurol 57(1):8–16

    Article  PubMed  Google Scholar 

  • Catani M, Allin MP, Husain M, Pugliese L, Mesulam MM, Murray RM, Jones DK (2007) Symmetries in human brain language pathways correlate with verbal recall. Proc Natl Acad Sci USA 104(43):17163–17168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Catani M, Dell’acqua F, Vergani F, Malik F, Hodge H, Roy P, Valabregue R, Thiebaut de Schotten M (2012) Short frontal lobe connections of the human brain. Cortex 48(2):273–291

    Article  PubMed  Google Scholar 

  • Catani M, Dell’acqua F, Thiebaut de Schotten M (2013) A revised limbic system model for memory, emotion and behaviour. Neurosci Biobehav Rev 37(8):1724–1737

    Article  PubMed  Google Scholar 

  • Cerliani L, Thomas RM, Jbabdi S, Siero JC, Nanetti L, Crippa A, Gazzola V, D’Arceuil H, Keysers C (2012) Probabilistic tractography recovers a rostrocaudal trajectory of connectivity variability in the human insular cortex. Hum Brain Mapp 33(9):2005–2034

    Article  PubMed  PubMed Central  Google Scholar 

  • Charlton RA, Barrick TR, Markus HS, Morris RG (2010) The relationship between episodic long-term memory and white matter integrity in normal aging. Neuropsychologia 48(1):114–122

    Article  CAS  PubMed  Google Scholar 

  • Christoff K, Keramatian K, Gordon AM, Smith R, Madler B (2009) Prefrontal organization of cognitive control according to levels of abstraction. Brain Res 1286:94–105

    Article  CAS  PubMed  Google Scholar 

  • Ciccarelli O, Toosy AT, Parker GJ, Wheeler-Kingshott CA, Barker GJ, Miller DH, Thompson AJ (2003) Diffusion tractography based group mapping of major white-matter pathways in the human brain. NeuroImage 19(4):1545–1555

    Article  CAS  PubMed  Google Scholar 

  • Clark CA, Barrick TR, Murphy MM, Bell BA (2003) White matter fiber tracking in patients with space-occupying lesions of the brain: a new technique for neurosurgical planning? Neuroimage 20(3):1601–1608

    Article  PubMed  Google Scholar 

  • Coffey CE, Saxton JA, Ratcliff G, Bryan RN, Lucke JF (1999) Relation of education to brain size in normal aging: implications for the reserve hypothesis. Neurology 53(1):189–196

    Article  CAS  PubMed  Google Scholar 

  • Craig MC, Catani M, Deeley Q, Latham R, Daly E, Kanaan R, Picchioni M, McGuire PK, Fahy T, Murphy DG (2009) Altered connections on the road to psychopathy. Mol Psychiatry 14 (10):946–953, 907

  • Curiati PK, Tamashiro JH, Squarzoni P, Duran FL, Santos LC, Wajngarten M, Leite CC, Vallada H, Menezes PR, Scazufca M, Busatto GF, Alves TC (2009) Brain structural variability due to aging and gender in cognitively healthy Elders: results from the Sao Paulo Ageing and Health study. AJNR Am J Neuroradiol 30(10):1850–1856

    Article  CAS  PubMed  Google Scholar 

  • Curtis CE, D’Esposito M (2003) Success and failure suppressing reflexive behavior. J Cogn Neurosci 15(3):409–418

    Article  PubMed  Google Scholar 

  • Dauguet J, Peled S, Berezovskii V, Delzescaux T, Warfield SK, Born R, Westin CF (2006) 3D histological reconstruction of fiber tracts and direct comparison with diffusion tensor MRI tractography. Med Image Comput Comput Assist Interv MICCAI Int Conf Med Image Comput Comput Assist Interv 9(Pt 1):109–116

    Google Scholar 

  • Dauguet J, Peled S, Berezovskii V, Delzescaux T, Warfield SK, Born R, Westin CF (2007) Comparison of fiber tracts derived from in-vivo DTI tractography with 3D histological neural tract tracer reconstruction on a macaque brain. Neuroimage 37(2):530–538

  • Davis SW, Dennis NA, Buchler NG, White LE, Madden DJ, Cabeza R (2009) Assessing the effects of age on long white matter tracts using diffusion tensor tractography. NeuroImage 46(2):530–541

    Article  PubMed  PubMed Central  Google Scholar 

  • Dell’Acqua F, Catani M (2012) Structural human brain networks: hot topics in diffusion tractography. Curr Opin Neurol 25(4):375–383

    PubMed  Google Scholar 

  • Dell’acqua F, Scifo P, Rizzo G, Catani M, Simmons A, Scotti G, Fazio F (2010) A modified damped Richardson-Lucy algorithm to reduce isotropic background effects in spherical deconvolution. Neuroimage 49(2):1446–1458

    Article  PubMed  Google Scholar 

  • Dell’Acqua F, Simmons A, Williams SC, Catani M (2013) Can spherical deconvolution provide more information than fiber orientations? Hindrance modulated orientational anisotropy, a true-tract specific index to characterize white matter diffusion. Hum Brain Mapp 34(10):2464–2483

    Article  PubMed  Google Scholar 

  • Descoteaux M, Angelino E, Fitzgibbons S, Deriche R (2007) Regularized, fast, and robust analytical Q-ball imaging. Magn Reson Med 58(3):497–510

    Article  PubMed  Google Scholar 

  • Draganski B, Ashburner J, Hutton C, Kherif F, Frackowiak RS, Helms G, Weiskopf N (2011) Regional specificity of MRI contrast parameter changes in normal ageing revealed by voxel-based quantification (VBQ). Neuroimage 55(4):1423–1434

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fischer FU, Wolf D, Scheurich A, Fellgiebel A (2014) Association of structural global brain network properties with intelligence in normal aging. PLoS One 9(1):e86258

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):189–198

    Article  CAS  PubMed  Google Scholar 

  • Geerligs L, Saliasi E, Maurits NM, Renken RJ, Lorist MM (2014) Brain mechanisms underlying the effects of aging on different aspects of selective attention. Neuroimage 91:52–62

    Article  PubMed  Google Scholar 

  • Giorgio A, Santelli L, Tomassini V, Bosnell R, Smith S, De Stefano N, Johansen-Berg H (2010) Age-related changes in grey and white matter structure throughout adulthood. Neuroimage 51(3):943–951

    Article  PubMed  PubMed Central  Google Scholar 

  • Gonen-Yaacovi G, de Souza LC, Levy R, Urbanski M, Josse G, Volle E (2013) Rostral and caudal prefrontal contribution to creativity: a meta-analysis of functional imaging data. Front Hum Neurosci 7:465

    Article  PubMed  PubMed Central  Google Scholar 

  • Good CD, Johnsrude IS, Ashburner J, Henson RN, Friston KJ, Frackowiak RS (2001) Cerebral asymmetry and the effects of sex and handedness on brain structure: a voxel-based morphometric analysis of 465 normal adult human brains. NeuroImage 14(3):685–700

    Article  CAS  PubMed  Google Scholar 

  • Gootjes L, Van Strien JW, Bouma A (2004) Age effects in identifying and localising dichotic stimuli: a corpus callosum deficit? J Clin Exp Neuropsychol 26(6):826–837

    Article  PubMed  Google Scholar 

  • Haber SN, Fudge JL, McFarland NR (2000) Striatonigrostriatal pathways in primates form an ascending spiral from the shell to the dorsolateral striatum. J Neurosci 20(6):2369–2382

    CAS  PubMed  Google Scholar 

  • Hasan KM, Iftikhar A, Kamali A, Kramer LA, Ashtari M, Cirino PT, Papanicolaou AC, Fletcher JM, Ewing-Cobbs L (2009a) Development and aging of the healthy human brain uncinate fasciculus across the lifespan using diffusion tensor tractography. Brain Res 1276:67–76

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hasan KM, Kamali A, Iftikhar A, Kramer LA, Papanicolaou AC, Fletcher JM, Ewing-Cobbs L (2009b) Diffusion tensor tractography quantification of the human corpus callosum fiber pathways across the lifespan. Brain Res 1249:91–100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hasan KM, Kamali A, Abid H, Kramer LA, Fletcher JM, Ewing-Cobbs L (2010) Quantification of the spatiotemporal microstructural organization of the human brain association, projection and commissural pathways across the lifespan using diffusion tensor tractography. Brain Struct Funct 214(4):361–373

    Article  PubMed  PubMed Central  Google Scholar 

  • Holtrop JL, Loucks TM, Sosnoff JJ, Sutton BP (2014) Investigating Age-related changes in fine motor control across different effectors and the impact of white matter integrity. Neuroimage 96:81–87

    Article  PubMed  PubMed Central  Google Scholar 

  • Hsu JL, Leemans A, Bai CH, Lee CH, Tsai YF, Chiu HC, Chen WH (2008) Gender differences and age-related white matter changes of the human brain: a diffusion tensor imaging study. Neuroimage 39(2):566–577

    Article  PubMed  Google Scholar 

  • Jeurissen B, Leemans A, Tournier JD, Jones DK, Sijbers J (2013) Investigating the prevalence of complex fiber configurations in white matter tissue with diffusion magnetic resonance imaging. Hum Brain Mapp 34(11):2747–2766

    Article  PubMed  Google Scholar 

  • Johansen-Berg H, Della-Maggiore V, Behrens TEJ, Smith SM, Paus T (2007) Integrity of white matter in the corpus callosum correlates with bimanual co-ordination skills. NeuroImage 36(Suppl 2):T16–T21

    Article  PubMed  PubMed Central  Google Scholar 

  • Jones DK, Catani M, Pierpaoli C, Reeves SJ, Shergill SS, O’Sullivan M, Golesworthy P, McGuire P, Horsfield MA, Simmons A, Williams SC, Howard RJ (2006) Age effects on diffusion tensor magnetic resonance imaging tractography measures of frontal cortex connections in schizophrenia. Hum Brain Mapp 27(3):230–238

    Article  PubMed  Google Scholar 

  • Jones DK, Knosche TR, Turner R (2013) White matter integrity, fiber count, and other fallacies: the do’s and don’ts of diffusion MRI. Neuroimage 73:239–254

    Article  PubMed  Google Scholar 

  • Klingler J (1935) Erleichterung der makroskopischen Präparation des Gehirn durch den Gefrierprozess. Schweiz Arch Neurol Psychiat 36:247–256

    Google Scholar 

  • Koechlin E, Summerfield C (2007) An information theoretical approach to prefrontal executive function. Trends Cogn Sci 11(6):229–235

    Article  PubMed  Google Scholar 

  • Koechlin E, Basso G, Pietrini P, Panzer S, Grafman J (1999) The role of the anterior prefrontal cortex in human cognition. Nature 399(6732):148–151

    Article  CAS  PubMed  Google Scholar 

  • Koechlin E, Ody C, Kouneiher F (2003) The architecture of cognitive control in the human prefrontal cortex. Science 302(5648):1181–1185

    Article  CAS  PubMed  Google Scholar 

  • Kristo G, Leemans A, de Gelder B, Raemaekers M, Rutten GJ, Ramsey N (2013a) Reliability of the corticospinal tract and arcuate fasciculus reconstructed with DTI-based tractography: implications for clinical practice. Eur Radiol 23(1):28–36

    Article  PubMed  Google Scholar 

  • Kristo G, Leemans A, Raemaekers M, Rutten GJ, de Gelder B, Ramsey NF (2013b) Reliability of two clinically relevant fiber pathways reconstructed with constrained spherical deconvolution. Magn Reson Med 70(6):1544–1556

    Article  PubMed  Google Scholar 

  • Kroger JK, Sabb FW, Fales CL, Bookheimer SY, Cohen MS, Holyoak KJ (2002) Recruitment of anterior dorsolateral prefrontal cortex in human reasoning: a parametric study of relational complexity. Cereb Cortex 12(5):477–485

    Article  PubMed  Google Scholar 

  • Lawes INC, Barrick TR, Murugam V, Spierings N, Evans DR, Song M, Clark CA (2008) Atlas-based segmentation of white matter tracts of the human brain using diffusion tensor tractography and comparison with classical dissection. NeuroImage 39(1):62–79

    Article  PubMed  Google Scholar 

  • Le Bihan D, Breton E (1985) Imagerie de diffusion in vivo par résonance magnétique nucléaire. Comptes rendus de l’Académie des sciences 301:1109–1112

    Google Scholar 

  • Lebel C, Beaulieu C (2011) Longitudinal development of human brain wiring continues from childhood into adulthood. J Neurosci 31(30):10937–10947

    Article  CAS  PubMed  Google Scholar 

  • Lebel C, Walker L, Leemans A, Phillips L, Beaulieu C (2008) Microstructural maturation of the human brain from childhood to adulthood. Neuroimage 40(3):1044–1055

    Article  CAS  PubMed  Google Scholar 

  • Lebel C, Caverhill-Godkewitsch S, Beaulieu C (2010) Age-related regional variations of the corpus callosum identified by diffusion tensor tractography. Neuroimage 52(1):20–31

    Article  PubMed  Google Scholar 

  • Madden DJ, Whiting WL, Huettel SA, White LE, MacFall JR, Provenzale JM (2004) Diffusion tensor imaging of adult age differences in cerebral white matter: relation to response time. Neuroimage 21(3):1174–1181

    Article  PubMed  Google Scholar 

  • Madden DJ, Spaniol J, Whiting WL, Bucur B, Provenzale JM, Cabeza R, White LE, Huettel SA (2007) Adult age differences in the functional neuroanatomy of visual attention: a combined fMRI and DTI study. Neurobiol Aging 28(3):459–476

    Article  PubMed  PubMed Central  Google Scholar 

  • Michielse S, Coupland N, Camicioli R, Carter R, Seres P, Sabino J, Malykhin N (2010) Selective effects of aging on brain white matter microstructure: a diffusion tensor imaging tractography study. Neuroimage 52(4):1190–1201

    Article  PubMed  Google Scholar 

  • Montgomery SA, Asberg M (1979) A new depression scale designed to be sensitive to change. Br J Psychiatry 134:382–389

    Article  CAS  PubMed  Google Scholar 

  • Mori S, Oishi K, Jiang H, Li X, Akhter K, Hua K, Faria AV, Mahmood A, Woods R, Toga AW, Pike GB, Neto PR, Evans A, Zhang J, Huang H, Miller MI, van Zijl PC, Mazziotta J (2008) Stereotaxic white matter atlas based on diffusion tensor imaging in an ICBM template. NeuroImage 40(2):570–582

    Article  PubMed  PubMed Central  Google Scholar 

  • Moscovitch M (1992) Memory and working-with-memory: a component process model based on modules and central systems. J Cogn Neurosci 4(3):257–267

    Article  CAS  PubMed  Google Scholar 

  • Myers RE (1965) Organization of forebrain commissures. In: Ettlinger EG (ed) Functions of the Corpus Callosum. CIBA Foundation Study Group 20, London, pp 133–143

    Google Scholar 

  • O’Donnell LJ, Westin CF (2007) Automatic tractography segmentation using a high-dimensional white matter atlas. IEEE Trans Med Imaging 26(11):1562–1575

    Article  PubMed  Google Scholar 

  • O’Sullivan M, Jones DK, Summers PE, Morris RG, Williams SC, Markus HS (2001) Evidence for cortical “disconnection” as a mechanism of age-related cognitive decline. Neurology 57(4):632–638

    Article  PubMed  Google Scholar 

  • Panadero A, Gonzalo Sanz LM (1988) Memory and aging: changes in the mammillary body and anterior thalamic nuclei due to age. Rev Med Univ Navarra 32(4):191–200

    CAS  PubMed  Google Scholar 

  • Pantoni L (2010) Cerebral small vessel disease: from pathogenesis and clinical characteristics to therapeutic challenges. Lancet Neurol 9(7):689–701

    Article  PubMed  Google Scholar 

  • Phillips OR, Clark KA, Luders E, Azhir R, Joshi SH, Woods RP, Mazziotta JC, Toga AW, Narr KL (2013) Superficial white matter: effects of age, sex, and hemisphere. Brain Connect 3(2):146–159

    Article  PubMed  PubMed Central  Google Scholar 

  • Raffelt D, Tournier JD, Rose S, Ridgway GR, Henderson R, Crozier S, Salvado O, Connelly A (2012) Apparent fibre density: a novel measure for the analysis of diffusion-weighted magnetic resonance images. Neuroimage 59(4):3976–3994

    Article  PubMed  Google Scholar 

  • Raz N (2005) The aging brain observed in vivo: differential changes and their modifiers, in: cognitive neuroscience of aging: linking cognitive and cerebral aging. In: Cabeza R, Nyberg L (eds) Cognitive neuroscience of aging. Park DC, New-York, pp 19–57

    Google Scholar 

  • Raz N, Williamson A, Gunning-Dixon F, Head D, Acker JD (2000) Neuroanatomical and cognitive correlates of adult age differences in acquisition of a perceptual-motor skill. Microsc Res Tech 51(1):85–93

    Article  CAS  PubMed  Google Scholar 

  • Raz N, Gunning-Dixon F, Head D, Rodrigue KM, Williamson A, Acker JD (2004) Aging, sexual dimorphism, and hemispheric asymmetry of the cerebral cortex: replicability of regional differences in volume. Neurobiol Aging 25(3):377–396

    Article  PubMed  Google Scholar 

  • Reuter-Lorenz PA, Stanczak L (2000) Differential effects of aging on the functions of the corpus callosum. Dev Neuropsychol 18(1):113–137

    Article  CAS  PubMed  Google Scholar 

  • Roine T, Jeurissen B, Perrone D, Aelterman J, Leemans A, Philips W, Sijbers J (2014) Isotropic non-white matter partial volume effects in constrained spherical deconvolution. Front Neuroinform 8:28

    Article  PubMed  PubMed Central  Google Scholar 

  • Sakai K, Passingham RE (2003) Prefrontal interactions reflect future task operations. Nat Neurosci 6(1):75–81

    Article  CAS  PubMed  Google Scholar 

  • Sala JB, Rämä P, Courtney SM (2003) Functional topography of a distributed neural system for spatial and nonspatial information maintenance in working memory. Neuropsychologia 41(3):341–356

    Article  PubMed  Google Scholar 

  • Salat DH, Kaye JA, Janowsky JS (1999) Prefrontal gray and white matter volumes in healthy aging and Alzheimer disease. Arch Neurol 56(3):338–344

    Article  CAS  PubMed  Google Scholar 

  • Schmahmann JD, Pandya DN (1995) Prefrontal cortex projections to the basilar pons in rhesus monkey: implications for the cerebellar contribution to higher function. Neurosci Lett 199(3):175–178

    Article  CAS  PubMed  Google Scholar 

  • Schulte T, Maddah M, Muller-Oehring EM, Rohlfing T, Pfefferbaum A, Sullivan EV (2013) Fiber tract-driven topographical mapping (FTTM) reveals microstructural relevance for interhemispheric visuomotor function in the aging brain. Neuroimage 77:195–206

    Article  PubMed  PubMed Central  Google Scholar 

  • Shapiro S, Wilk M (1965) An analysis of variance test for normality (complete samples). Biometrika 52(3/4):591–611

    Article  Google Scholar 

  • Smith EE, Jonides J (1999) Storage and executive processes in the frontal lobes. Science 283(5408):1657–1661

    Article  CAS  PubMed  Google Scholar 

  • Smith R, Keramatian K, Christoff K (2007) Localizing the rostrolateral prefrontal cortex at the individual level. Neuroimage 36(4):1387–1396

    Article  PubMed  Google Scholar 

  • Spearman C (1904) The proof and measurement of association between two things. Am J Psychol 15(1):441–471

    Article  Google Scholar 

  • Stern Y (2002) What is cognitive reserve? Theory and research application of the reserve concept. J Int Neuropsychol Soc 8:448–460

    Article  PubMed  Google Scholar 

  • Stern Y (2009) Cognitive reserve. Neuropsychologia 47(10):2015–2028

    Article  PubMed  PubMed Central  Google Scholar 

  • Stern Y, Habeck C, Moeller J, Scarmeas N, Anderson KE, Hilton HJ, Flynn J, Sackeim H, van Heertum R (2005) Brain networks associated with cognitive reserve in healthy young and old adults. Cereb Cortex 15(4):394–402

    Article  PubMed  PubMed Central  Google Scholar 

  • Stern Y, Zarahn E, Habeck C, Holtzer R, Rakitin BC, Kumar A, Flynn J, Steffener J, Brown T (2008) A common neural network for cognitive reserve in verbal and object working memory in young but not old. Cereb Cortex 18(4):959–967

    Article  PubMed  PubMed Central  Google Scholar 

  • Stuss DT, Knight RT (2013) Principles of frontal lobe function. Oxford University Press, Oxford

    Book  Google Scholar 

  • Tamnes CK, Ostby Y, Fjell AM, Westlye LT, Due-Tonnessen P, Walhovd KB (2010) Brain maturation in adolescence and young adulthood: regional age-related changes in cortical thickness and white matter volume and microstructure. Cereb Cortex 20(3):534–548

  • Thiebaut de Schotten M, Ffytche DH, Bizzi A, Dell’Acqua F, Allin M, Walshe M, Murray R, Williams SC, Murphy DG, Catani M (2011) Atlasing location, asymmetry and inter-subject variability of white matter tracts in the human brain with MR diffusion tractography. Neuroimage 54(1):49–59

    Article  PubMed  Google Scholar 

  • Thiebaut de Schotten M, Dell’acqua F, Valabregue R, Catani M (2012) Monkey to human comparative anatomy of the frontal lobe association tracts. Cortex 48:82–96

    Article  PubMed  Google Scholar 

  • Thiebaut de Schotten M, Cohen L, Amemiya E, Braga LW, Dehaene S (2014a) Learning to read improves the structure of the arcuate fasciculus. Cereb Cortex 24(4):989–995

    Article  PubMed  Google Scholar 

  • Thiebaut de Schotten M, Tomaiuolo F, Aiello M, Merola S, Silvetti M, Lecce F, Bartolomeo P, Doricchi F (2014b) Damage to white matter pathways in subacute and chronic spatial neglect: a group study and 2 single-case studies with complete virtual “in vivo” tractography dissection. Cereb Cortex 24(3):691–706

    Article  PubMed  Google Scholar 

  • Tournier JD, Calamante F, Gadian DG, Connelly A (2004) Direct estimation of the fiber orientation density function from diffusion-weighted MRI data using spherical deconvolution. NeuroImage 23(3):1176–1185

    Article  PubMed  Google Scholar 

  • Tuch DS, Reese TG, Wiegell MR, Wedeen VJ (2003) Diffusion MRI of complex neural architecture. Neuron 40(5):885–895

    Article  CAS  PubMed  Google Scholar 

  • Vartanian O (2012) Dissociable neural systems for analogy and metaphor: implications for the neuroscience of creativity. Br J Psychol 103(3):302–316

    Article  PubMed  Google Scholar 

  • Verhoeven JS, Sage CA, Leemans A, Van Hecke W, Callaert D, Peeters R, De Cock P, Lagae L, Sunaert S (2010) Construction of a stereotaxic DTI atlas with full diffusion tensor information for studying white matter maturation from childhood to adolescence using tractography-based segmentations. Hum Brain Mapp 31(3):470–486

    PubMed  Google Scholar 

  • Volle E, Kinkingnehun S, Pochon JB, Mondon K, Thiebaut de Schotten M, Seassau M, Duffau H, Samson Y, Dubois B, Levy R (2008) The functional architecture of the left posterior and lateral prefrontal cortex in humans. Cereb Cortex 18(10):2460–2469

    Article  PubMed  Google Scholar 

  • Volle E, Gilbert SJ, Benoit RG, Burgess PW (2010) Specialization of the rostral prefrontal cortex for distinct analogy processes. Cereb Cortex 20(11):2647–2659

    Article  PubMed  PubMed Central  Google Scholar 

  • Volle E, Gonen-Yaacovi G, Costello Ade L, Gilbert SJ, Burgess PW (2011) The role of rostral prefrontal cortex in prospective memory: a voxel-based lesion study. Neuropsychologia 49(8):2185–2198

    Article  PubMed  PubMed Central  Google Scholar 

  • Volle E, Levy R, Burgess PW (2013) A new era for lesion-behavior mapping of prefrontal functions. In: D.T. S, Knight RT (eds) Principles of Frontal Lobe Function. pp 500–523

  • Vos SB, Jones DK, Jeurissen B, Viergever MA, Leemans A (2012) The influence of complex white matter architecture on the mean diffusivity in diffusion tensor MRI of the human brain. Neuroimage 59(3):2208–2216

    Article  PubMed  Google Scholar 

  • Wakana S, Caprihan A, Panzenboeck MM, Fallon JH, Perry M, Gollub RL, Hua K, Zhang J, Jiang H, Dubey P, Blitz A, van Zijl PC, Mori S (2007) Reproducibility of quantitative tractography methods applied to cerebral white matter. NeuroImage 36(3):630–644

    Article  PubMed  PubMed Central  Google Scholar 

  • Wedeen VJ, Hagmann P, Tseng W-YI, Reese TG, Weisskoff RM (2005) Mapping complex tissue architecture with diffusion spectrum magnetic resonance imaging. Magn Reson Med Off J Soc Magn Reson Med Soc Magn Reson Med 54(6):1377–1386

    Article  Google Scholar 

  • West RL (1996) An application of prefrontal cortex function theory to cognitive aging. Psychol Bull 120(2):272–292

    Article  CAS  PubMed  Google Scholar 

  • Xiong YY, Mok V (2011) Age-related white matter changes. J Aging Res 2011:617927

    Article  PubMed  PubMed Central  Google Scholar 

  • Yushkevich PA, Zhang H, Simon TJ, Gee JC (2008) Structure-specific statistical mapping of white matter tracts. Neuroimage 41(2):448–461

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We thank Dr. Marco Catani for his assistance with the anatomical dissection and insightful discussions. We also thank the French Agence Nationale de la Recherche for its support of this project (project CAFORPFC, No. ANR-09-RPDOC-004-01 and project PHENOTYPES, No. ANR-13-JSV4-0001-01). In addition, we also thank the program “Investissements d’avenir” (ANR-10-IAIHU-06) for its generous support.

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Authors and Affiliations

  1. CNRS UMR 7225, Inserm, UPMC-Paris6, UMR_S 1127, CRICM, GH Pitié-Salpêtrière, 75013, Paris, France

    K. Rojkova, E. Volle, M. Urbanski & M. Thiebaut de Schotten

  2. Natbrainlab, Brain and Spine Institute, Paris, France

    K. Rojkova & M. Thiebaut de Schotten

  3. Service de Médecine et de Réadaptation Gériatrique et Neurologique, Hôpitaux de Saint-Maurice, Saint-Maurice, France

    M. Urbanski

  4. Centre de Neuroimagerie de Recherche CENIR, Groupe Hospitalier Pitié-Salpêtrière, Paris, France

    F. Humbert

  5. Natbrainlab, Sackler Institute of Translational Neurodevelopment, Institute of Psychiatry, King’s College London, London, UK

    M. Thiebaut de Schotten

  6. Department of Neuroimaging, Institute of Psychiatry, Natbrainlab, King’s College London, London, UK

    F. Dell’Acqua

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  1. K. Rojkova
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  2. E. Volle
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  3. M. Urbanski
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  6. M. Thiebaut de Schotten
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Correspondence to M. Thiebaut de Schotten.

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Rojkova, K., Volle, E., Urbanski, M. et al. Atlasing the frontal lobe connections and their variability due to age and education: a spherical deconvolution tractography study. Brain Struct Funct 221, 1751–1766 (2016). https://doi.org/10.1007/s00429-015-1001-3

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  • DOI: https://doi.org/10.1007/s00429-015-1001-3

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