Contralateral cerebello-thalamo-cortical pathways with prominent involvement of associative areas in humans in vivo
Tóm tắt
In addition to motor functions, it has become clear that in humans the cerebellum plays a significant role in cognition too, through connections with associative areas in the cerebral cortex. Classical anatomy indicates that neo-cerebellar regions are connected with the contralateral cerebral cortex through the dentate nucleus, superior cerebellar peduncle, red nucleus and ventrolateral anterior nucleus of the thalamus. The anatomical existence of these connections has been demonstrated using virus retrograde transport techniques in monkeys and rats ex vivo. In this study, using advanced diffusion MRI tractography we show that it is possible to calculate streamlines to reconstruct the pathway connecting the cerebellar cortex with contralateral cerebral cortex in humans in vivo. Corresponding areas of the cerebellar and cerebral cortex encompassed similar proportion (about 80 %) of the tract, suggesting that the majority of streamlines passing through the superior cerebellar peduncle connect the cerebellar hemispheres through the ventrolateral thalamus with contralateral associative areas. This result demonstrates that this kind of tractography is a useful tool to map connections between the cerebellum and the cerebral cortex and moreover could be used to support specific theories about the abnormal communication along these pathways in cognitive dysfunctions in pathologies ranging from dyslexia to autism.
Tài liệu tham khảo
Akhlaghi H, Yu J, Corben L et al (2013) Cognitive deficits in friedreich ataxia correlate with micro-structural changes in dentatorubral tract. Cerebellum. doi:10.1007/s12311-013-0525-4
Alexander AL, Hasan KM, Lazar M et al (2001) Analysis of partial volume effects in diffusion-tensor MRI. Magn Reson Med 45:770–780
Alexander DC, Barker GJ, Arridge SR (2002) Detection and modeling of non-Gaussian apparent diffusion coefficient profiles in human brain data. Magn Reson Med 48:331–340. doi:10.1002/mrm.10209
Amaral DG (2000) The functional organization of perception and movement. In: Kandel ER, Schwartz JH, Jessell TM (eds) Princ. Neural Sci., 4th edn. McGraw-Hill, New York, pp 337–348
Amodio DM, Frith CD (2006) Meeting of minds: the medial frontal cortex and social cognition. Nat Rev Neurosci 7:268–277. doi:10.1038/nrn1884
Anderson VM, CaM Wheeler-Kingshott, Abdel-Aziz K et al (2011) A comprehensive assessment of cerebellar damage in multiple sclerosis using diffusion tractography and volumetric analysis. Mult Scler 17:1079–1087. doi:10.1177/1352458511403528
Arguello PA, Enquist LW, Wang SS-H (2012) Long-distance connectivity between prefrontal cortex and cerebellum in mouse. Neurosci. Meet. Planner. New Orleans, LA. Soc Neurosci 104:30
Bauman ML, Kemper TL (2005) Neuroanatomic observations of the brain in autism: a review and future directions. Int J Dev Neurosci 23:183–187. doi:10.1016/j.ijdevneu.2004.09.006
Behrens TEJ, Johansen-Berg H, Woolrich MW et al (2003a) Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat Neurosci 6:750–757. doi:10.1038/nn1075
Behrens TEJ, Woolrich MW, Jenkinson M et al (2003b) Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magn Reson Med 50:1077–1088. doi:10.1002/mrm.10609
Behrens TEJ, Berg HJ, Jbabdi S et al (2007) Probabilistic diffusion tractography with multiple fibre orientations: what can we gain? Neuroimage 34:144–155. doi:10.1016/j.neuroimage.2006.09.018
Booth JR, Wood L, Lu D et al (2007) The role of the basal ganglia and cerebellum in language processing. Brain Res 1133:136–144. doi:10.1016/j.brainres.2006.11.074
Boso M, Emanuele E, Prestori F et al (2010) Autism and genius: is there a link? The involvement of central brain loops and hypotheses for functional testing. Funct Neurol 25:27–32
Brodmann K (2006) Brodmann’s localisation in the cerebral cortex, 3rd edn, pp 1–298
Buckner RL, Krienen FM, Castellanos A et al (2011) The organization of the human cerebellum estimated by intrinsic functional connectivity. J Neurophysiol 106:2322–2345. doi:10.1152/jn.00339.2011
Calamante F, Tournier J-D, Jackson GD, Connelly A (2010) Track-density imaging (TDI): super-resolution white matter imaging using whole-brain track-density mapping. Neuroimage 53:1233–1243. doi:10.1016/j.neuroimage.2010.07.024
Calamante F, Oh S-H, Tournier J-D et al (2013) Super-resolution track-density imaging of thalamic substructures: comparison with high-resolution anatomical magnetic resonance imaging at 7.0T. Hum Brain Mapp 34:2538–2548. doi:10.1002/hbm.22083
Catani M, Dell’acqua F, Vergani F et al (2012) Short frontal lobe connections of the human brain. Cortex 48:273–291. doi:10.1016/j.cortex.2011.12.001
Chen CH, Khodakhah K (2012) Short latency cerebellar modulation of the basal ganglia. Neuroscience
Ciccarelli O, Toosy A, Parker GJ et al (2003) Diffusion tractography based group mapping of major white-matter pathways in the human brain. Neuroimage 19:1545–1555. doi:10.1016/S1053-8119(03)00190-3
Clower DM, West RA, Lynch JC, Strick PL, Strick PL (2001) The inferior parietal lobule is the target of output from the superior colliculus, hippocampus, and cerebellum. J Neurosci 21:6283–6291
Clower DM, Dum RP, Strick PL (2005) Basal ganglia and cerebellar inputs to “AIP”. Cereb Cortex 15:913–920. doi:10.1093/cercor/bhh190
Cook PA, Symms M, Boulby PA, Alexander DC (2007) Optimal acquisition orders of diffusion-weighted MRI measurements. J Magn Reson Imaging 25:1051–1058. doi:10.1002/jmri.20905
D’Angelo E, Casali S (2013) Seeking a unified framework for cerebellar function and dysfunction: from circuit operations to cognition. Front Neural Circuits 6:1–23. doi:10.3389/fncir.2012.00116
Dayan M, Olivito G, Molinari M et al (2013) Impact of cerebellar atrophy on cortical grey matter and cerebellar peduncles as assessed by voxel based morphometry and diffusion imaging. In: Proc Int Soc Magn Reson Med, p 1014
Dell’Acqua F, Bodi I, Slater D et al (2013) MR diffusion histology and micro-tractography reveal mesoscale features of the human cerebellum. Cerebellum 12:923–931. doi:10.1007/s12311-013-0503-x
Diedrichsen J, Balsters JH, Flavell J et al (2009) A probabilistic MR atlas of the human cerebellum. Neuroimage 46:39–46. doi:10.1016/j.neuroimage.2009.01.045
Dolan L, Janmaat K, Willemsen V et al (1993) Cellular organisation of the Arabidopsis thaliana root. Dev Suppl 119:71–84
Doron KW, Funk CM, Glickstein M (2010) Fronto-cerebellar circuits and eye movement control: a diffusion imaging tractography study of human cortico-pontine projections. Brain Res 1307:63–71. doi:10.1016/j.brainres.2009.10.029
Du Boisgueheneuc F, Levy R, Volle E et al (2006) Functions of the left superior frontal gyrus in humans: a lesion study. Brain 129:3315–3328. doi:10.1093/brain/awl244
Evarts EV, Thach WT (1969) Motor mechanisms of the CNS: cerebrocerebellar interrelations. Annu Rev Physiol 31:451–498
Fernandez-Miranda JC, Pathak S, Engh J et al (2012) High-definition fiber tractography of the human brain: neuroanatomical validation and neurosurgical applications. Neurosurgery 71:430–453. doi:10.1227/NEU.0b013e3182592faa
Granziera C, Schmahmann JD, Hadjikhani N et al (2009) Diffusion spectrum imaging shows the structural basis of functional cerebellar circuits in the human cerebellum in vivo. PLoS ONE 4:e5101. doi:10.1371/journal.pone.0005101
Grefkes C, Ritzl A, Zilles K, Fink GR (2004) Human medial intraparietal cortex subserves visuomotor coordinate transformation. Neuroimage 23:1494–1506. doi:10.1016/j.neuroimage.2004.08.031
Grodd W, Hülsmann E, Lotze M et al (2001) Sensorimotor mapping of the human cerebellum: fMRI evidence of somatotopic organization. Hum Brain Mapp 13:55–73
Guerrasio L, Quinet J, Bu U, Goffart L (2010) Fastigial oculomotor region and the control of foveation during fixation. J Neurophysiol 103:1988–2001. doi:10.1152/jn.00771.2009
Habas C, Cabanis EA (2007a) Cortical projection to the human red nucleus: complementary results with probabilistic tractography at 3 T. Neuroradiology 49:777–784. doi:10.1007/s00234-007-0260-y
Habas C, Cabanis EA (2007b) Anatomical parcellation of the brainstem and cerebellar white matter: a preliminary probabilistic tractography study at 3 T. Neuroradiology 49:849–863. doi:10.1007/s00234-007-0267-4
Habas C, Kamdar N, Nguyen D et al (2009) Distinct cerebellar contributions to intrinsic connectivity networks. J Neurosci 29:8586–8594. doi:10.1523/JNEUROSCI.1868-09.2009
He Y, Zang Y, Jiang T et al (2004) Detecting functional connectivity of the cerebellum using low frequency fluctuations (LFFs). Med Image Comput Comput Assist Interv 3217:907–915
Heath RG, Harper JW (1974) Ascending projections of the cerebellar fastigial nucleus to the hippocampus, amygdala, and other temporal lobe sites: evoked potential and histological studies in monkeys and cats. Exp Neurol 45:268–287
Heath RG, Dempesy CW, Fontana CJ, Myers WA (1978) Cerebellar stimulation: effects on septal region, hippocampus, and amygdala of cats and rats. Biol Psychiatry 13:501–529
Holmes G (1939) The cerebellum of man. Brain 62:1–30
Hyam JA, Owen SLF, Kringelbach ML et al (2012) Contrasting connectivity of the ventralis intermedius and ventralis oralis posterior nuclei of the motor thalamus demonstrated by probabilistic tractography. Neurosurgery 70:162–9. (discussion 169) doi:10.1227/NEU.0b013e3182262c9a
Ito M (2008) Control of mental activities by internal models in the cerebellum. Nat Rev Neurosci 9:304–313. doi:10.1038/nrn2332
Jenkinson M, Bannister P, Brady M, Smith S (2002) Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 17:825–841. doi:10.1006/nimg.2002.1132
Jissendi P, Baudry S, Balériaux D (2008) Diffusion tensor imaging (DTI) and tractography of the cerebellar projections to prefrontal and posterior parietal cortices: a study at 3T. J Neuroradiol 35:42–50. doi:10.1016/j.neurad.2007.11.001
Jones DK, Knösche 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. doi:10.1016/j.neuroimage.2012.06.081
Kelly RM, Strick PL (2003) Cerebellar loops with motor cortex and prefrontal cortex of a nonhuman primate. J Neurosci 23:8432–8444
Klein A, Andersson J, Ardekani B a et al (2009) Evaluation of 14 nonlinear deformation algorithms applied to human brain MRI registration. Neuroimage 46:786–802. doi:10.1016/j.neuroimage.2008.12.037
Krienen FM, Buckner RL (2009) Segregated fronto-cerebellar circuits revealed by intrinsic functional connectivity. Cereb Cortex 19:2485–2497. doi:10.1093/cercor/bhp135
Kwon HG, Hong JH, Hong CP et al (2011) Dentatorubrothalamic tract in human brain: diffusion tensor tractography study. Neuroradiology 53:787–791. doi:10.1007/s00234-011-0878-7
Mang SC, Busza A, Reiterer S et al (2012) Thalamus segmentation based on the local diffusion direction: a group study. Magn Reson Med 67:118–126. doi:10.1002/mrm.22996
Mastropasqua C, Bozzali M, Ponzo V et al (2013) Functional connectivity in patients with progressive sopranuclear palsy is modulated by cerebellar intermittent theta burst stimulation. In: Proc Int Soc Magn Reson Med, p 2847
McNab JA, Jbabdi S, Deoni SCL et al (2009) High resolution diffusion-weighted imaging in fixed human brain using diffusion-weighted steady state free precession. Neuroimage 46:775–785. doi:10.1016/j.neuroimage.2009.01.008
Middleton FA, Strick PL (1994) Anatomical evidence for cerebellar and basal ganglia involvement in higher cognition function. Science 266(80):458–461
Middleton FA, Strick PL (2001) Cerebellar projections to the prefrontal cortex of the primate. J Neurosci 21:700–712
Middleton FA, Strick PL (2002) Basal-ganglia “projections” to the prefrontal cortex of the primate. Cereb Cortex 12:926–935
Milad MR, Quirk GJ (2002) Neurons in medial prefrontal cortex signal memory for fear extinction. Nature 420:70–74. doi:10.1038/nature01144.1
Miller KL, Stagg CJ, Douaud G et al (2011) Diffusion imaging of whole, post-mortem human brains on a clinical MRI scanner. Neuroimage 57:167–181. doi:10.1016/j.neuroimage.2011.03.070
Mittleman G, Goldowitz D, Heck DH, Blaha CD (2008) Cerebellar modulation of frontal cortex dopamine efflux in mice: relevance to autism and schizophrenia. Synapse 62:544–550. doi:10.1002/syn.20525
Morgan MA, Romanski LM, LeDoux JE (1993) Extinction of emotional learning: contribution of medial prefrontal cortex. Neurosci Lett 163:109–113
Mori S, van Zijl PCM (2002) Fiber tracking: principles and strategies—a technical review. NMR Biomed 15:468–480. doi:10.1002/nbm.781
Nandi D, Aziz TZ, Liu X, Stein JF (2002) Brainstem motor loops in the control of movement. Mov Disord 17:22–27. doi:10.1002/mds.10139
Noda H, Sugita S, Ikeda Y (1990) Afferent and efferent connections of the oculomotor region of the fastigial nucleus in the macaque monkey. J Comp Neurol 302:330–348
Olivito G, Dayan M, Molinari M et al (2013) The contribution of cerebellar white matter damage to cortical grey matter: evidence from voxel based morphometry and diffusion imaging. In: Proc Int Soc Magn Reson Med, p 1099
Palesi F, Tournier D, Calamante F et al (2013) Reconstructing cerebellar–cortical connections with advanced diffusion tractography. In: Proc Int Soc Magn Reson Med, p 3163
Pascual-Leone A, Wassermann EM, Grafman J, Hallett M (1996) The role of the dorsolateral prefrontal cortex in implicit procedural learning. Exp Brain Res 107:479–485
Petrides M (2000) The role of the mid-dorsolateral prefrontal cortex in working memory. Exp Brain Res 133:44–54
Pochon JB, Levy R, Poline JB et al (2001) The role of dorsolateral prefrontal cortex in the preparation of forthcoming actions: an fMRI study. Cereb Cortex 11:260–266
Ramnani N (2006) The primate cortico-cerebellar system: anatomy and function. Nat Rev Neurosci 7:511–522. doi:10.1038/nrn1953
Ramnani N, Owen AM (2004) Anterior prefrontal cortex: insights into function from anatomy and neuroimaging. Nat Rev Neurosci 5:184–194. doi:10.1038/nrn1343
Ridderinkhof KR, Ullsperger M, Crone EA, Nieuwenhuis S (2004) The role of the medial frontal cortex in cognitive control. Science 306(80):443–447. doi:10.1126/science.1100301
Salamon N, Sicotte N, Alger J et al (2005) Analysis of the brain-stem white-matter tracts with diffusion tensor imaging. Neuroradiology 47:895–902. doi:10.1007/s00234-005-1439-8
Salamon N, Sicotte N, Drain A et al (2007) White matter fiber tractography and color mapping of the normal human cerebellum with diffusion tensor imaging. J Neuroradiol 34:115–128
Schmahmann JD, Caplan D (2006) Cognition, emotion and the cerebellum. Brain 129:290–292. doi:10.1093/brain/awh729
Schmahmann JD, Pandya DN (1993) Prelunate, occipitotemporal, and parahippocampal projections to the basis pontis in rhesus monkey. J Comp Neurol 337:94–112
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 199:175–178
Schmahmann JD, Doyon J, McDonald D et al (1999) Three-dimensional MRI atlas of the human cerebellum in proportional stereotaxic space. Neuroimage 10:233–260. doi:10.1006/nimg.1999.0459
Seehaus AK, Roebroeck A, Chiry O et al (2013) Histological validation of DW-MRI tractography in human postmortem tissue. Cereb Cortex
Smith SM (2006) BET: brain extraction tool. Rev Lit Arts Am 39:1–2. doi:10.1080/08905760600696445
Smith RE, Tournier J-D, Calamante F, Connelly A (2012) Anatomically-constrained tractography: improved diffusion MRI streamlines tractography through effective use of anatomical information. Neuroimage 62:1924–1938. doi:10.1016/j.neuroimage.2012.06.005
Smith RE, Tournier J-D, Calamante F, Connelly A (2013) SIFT: spherical-deconvolution informed filtering of tractograms. Neuroimage 67:298–312. doi:10.1016/j.neuroimage.2012.11.049
Snider R, Eldred E (1952) Cerebrocerebellar relationships in the monkey. J Neurophysiol 15:27–40
Standring S (2008) The cerebellum. Gray’s Anat. Anat. basis Clin. Pract., 40th edn. Churchill Livingstone, pp 297–309
Strick PL, Dum RP, Fiez JA (2009) Cerebellum and nonmotor function. Annu Rev Neurosci 32:413–434. doi:10.1146/annurev.neuro.31.060407.125606
Sultan F (2002) Analysis of mammalian brain architecture. Nature 415:133–134. doi:10.1038/415133a
Takahashi E, Song JW, Folkerth RD et al (2013) Detection of postmortem human cerebellar cortex and white matter pathways using high angular resolution diffusion tractography: a feasibility study. Neuroimage 68:105–111. doi:10.1016/j.neuroimage.2012.11.042
Tilikete C, Koene A, Nighoghossian N et al (2006) Saccadic lateropulsion in Wallenberg syndrome: a window to access cerebellar control of saccades? Exp Brain Res 174:555–565. doi:10.1007/s00221-006-0495-6
Tournier J-D, Calamante F, Connelly A (2007) Robust determination of the fibre orientation distribution in diffusion MRI: non-negativity constrained super-resolved spherical deconvolution. Neuroimage 35:1459–1472
Tournier J-D, Mori S, Leemans A (2011) Diffusion tensor imaging and beyond. Magn Reson Med 65:1532–1556. doi:10.1002/mrm.22924
Tournier J-D, Calamante F, Connelly A (2012) MRtrix: diffusion tractography in crossing fiber regions. Int J Imaging Syst Technol 22:53–66. doi:10.1002/ima.22005
Tuch DS (2004) Q-ball imaging. Magn Reson Med 52:1358–1372. doi:10.1002/mrm.20279
Tuch DS, Reese TG, Wiegell MR et al (2002) High angular resolution diffusion imaging reveals intravoxel white matter fiber heterogeneity. Magn Reson Med 48:577–582. doi:10.1002/mrm.10268
Tunik E, Frey SH, Grafton ST (2005) Virtual lesions of the anterior intraparietal area disrupt goal-dependent on-line adjustments of grasp. Nat Neurosci 8:505–511. doi:10.1038/nn1430
Van Baarsen K, Kleinnijenhuis M, Konert T et al (2013) Tractography demonstrates dentate-rubro-thalamic tract disruption in an adult with cerebellar mutism. Cerebellum 12:617–622. doi:10.1007/s12311-013-0473-z
Voogd J (2003) The human cerebellum. J Chem Neuroanat 26:243–252. doi:10.1016/j.jchemneu.2003.07.005
Watson TC, Jones MW, Apps R (2009) Electrophysiological mapping of novel prefrontal—cerebellar pathways. Front Integr Neurosci 3:1–11. doi:10.3389/neuro.07
Watson TC, Becker N, Apps R, Jones MW (2014) Back to front: cerebellar connections and interactions with the prefrontal cortex. Front Syst Neurosci 8:1–11. doi:10.3389/fnsys.2014.00004
Watt C, Mihailoff G (1983) The cerebellopontine system in the rat. I. Autoradiographic studies. J Comp Neurol 215:312–330
Wedeen VJ, Hagmann P, Tseng W-YI et al (2005) Mapping complex tissue architecture with diffusion spectrum magnetic resonance imaging. Magn Reson Med 54:1377–1386. doi:10.1002/mrm.20642
Wedeen VJ, Wang RP, Schmahmann JD et al (2008) Diffusion spectrum magnetic resonance imaging (DSI) tractography of crossing fibers. Neuroimage 41:1267–1277. doi:10.1016/j.neuroimage.2008.03.036
Weinberger DR, Berman KF, Zec RF (1986) Physiologic dysfunction of dorsolateral prefrontal cortex in schizophrenia. I. Regional cerebral blood flow evidence. Arch Gen Psychiatry 43:114–124
Weinberger DR, Berman KF, Illowsky BP (1988) Physiological dysfunction of dorsolateral prefrontal cortex in schizophrenia. Arch Gen Psychiatry 45:609–615
Zhang D, Snyder AZ, Fox MD et al (2008) Intrinsic functional relations between human cerebral cortex and thalamus. J Neurophysiol 100:1740–1748. doi:10.1152/jn.90463.2008