Top

Published in:

Open Access 01-01-2017 | Original Article

Basal ganglia and cerebellar interconnectivity within the human thalamus

Authors: Esther A. Pelzer, Corina Melzer, Lars Timmermann, D. Yves von Cramon, Marc Tittgemeyer

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

Abstract

Basal ganglia and the cerebellum are part of a densely interconnected network. While both subcortical structures process information in basically segregated loops that primarily interact in the neocortex, direct subcortical interaction has been recently confirmed by neuroanatomical studies using viral transneuronal tracers in non-human primate brains. The thalamus is thought to be the main relay station of both projection systems. Yet, our understanding of subcortical basal ganglia and cerebellar interconnectivity within the human thalamus is rather sparse, primarily due to limitation in the acquisition of in vivo tracing. Consequently, we strive to characterize projections of both systems and their potential overlap within the human thalamus by diffusion MRI and tractography. Our analysis revealed a decreasing anterior-to-posterior gradient for pallido-thalamic connections in: (1) the ventral-anterior thalamus, (2) the intralaminar nuclei, and (3) midline regions. Conversely, we found a decreasing posterior-to-anterior gradient for dentato-thalamic projections predominantly in: (1) the ventral-lateral and posterior nucleus; (2) dorsal parts of the intralaminar nuclei and the subparafascicular nucleus, and (3) the medioventral and lateral mediodorsal nucleus. A considerable overlap of connectivity pattern was apparent in intralaminar nuclei and midline regions. Notably, pallidal and cerebellar projections were both hemispherically lateralized to the left thalamus. While strikingly consistent with findings from transneuronal studies in non-human primates as well as with pre-existing anatomical studies on developmentally expressed markers or pathological human brains, our assessment provides distinctive connectional fingerprints that illustrate the anatomical substrate of integrated functional networks between basal ganglia and the cerebellum. Thereby, our findings furnish useful implications for cerebellar contributions to the clinical symptomatology of movement disorders.

Available only for authorised users

Alexander GE, Crutcher MD (1990) Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci 13(7):266–271. doi:10.1016/0166-2236(90)90107-L CrossRefPubMed

Alexander GE, DeLong MR, Strick PL (1986) Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 9(1):357–381. doi:10.1146/annurev.ne.09.030186.002041 CrossRefPubMed

Andersson JLR, Jenkinson M, Smith S (2010) Non-linear registration, aka spatial normalization. FMRIB Analysis Group of the University of Oxford, FMRIB technical report TR07JA2

Argyelan M, Carbon M, Niethammer M, Ulug AM, Voss HU, Bressman SB, Dhawan V, Eidelberg D (2009) Cerebellothalamocortical connectivity regulates penetrance in dystonia. J Neurosci 29(31):9740–9747. doi:10.1523/JNEUROSCI.2300-09.2009 CrossRefPubMedPubMedCentral

Asanuma C, Thach W, Jones E (1983) Distribution of cerebellar terminations and their relation to other afferent terminations in the ventral lateral thalamic region of the monkey. Brain Res Rev 5(3):237–265. doi:10.1016/0165-0173(83)90015-2 CrossRef

Behrens TEJ, Johansen Berg H, Woolrich MW, Smith SM, Wheeler-Kingshott CAM, Boulby PA, Barker GJ, Sillery EL, Sheehan K, Ciccarelli O, Thompson AJ, Brady JM, Matthews PM (2003) Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat Neurosci 6(7):750–757. doi:10.1038/nn1075 CrossRefPubMed

Bernard JA, Peltier SJ, Benson BL, Wiggins JL, Jaeggi SM, Buschkuehl M, Jonides J, Monk CS, Seidler RD (2014) Dissociable functional networks of the human dentate nucleus. Cereb Cortex 24(8):2151–2159. doi:10.1093/cercor/bht065 CrossRefPubMed

Bosch-Bouju C, Hyland BI, Parr-Brownlie LC (2013) Motor thalamus integration of cortical, cerebellar and basal ganglia information: implications for normal and parkinsonian conditions. Front Comput Neurosci 7:163. doi:10.3389/fncom.2013.00163 CrossRefPubMedPubMedCentral

Bostan AC, Dum RP, Strick PL (2010) The basal ganglia communicate with the cerebellum. Proc Natl Acad Sci U S A 107(18):8452–8456. doi:10.1073/pnas.1000496107 CrossRefPubMedPubMedCentral

Bostan AC, Dum RP, Strick PL (2013) Cerebellar networks with the cerebral cortex and basal ganglia. Trends Cogn Sci 17(5):241–254. doi:10.1016/j.tics.2013.03.003 CrossRefPubMedPubMedCentral

Broser P, Vargha-Khadem F, Clark CA (2011) Robust subdivision of the thalamus in children based on probability distribution functions calculated from probabilistic tractography. Neuroimage 57(2):403–415. doi:10.1016/j.neuroimage.2011.04.054 CrossRefPubMed

Caligiore D, Pezzulo G, Baldassarre G, Bostan AC, Strick PL, Doya K, Helmich RC, Dirkx M, Houk J, Jörntell H, Lago-Rodriguez A, Galea JM, Miall RC, Popa T, Kishore A, Verschure PFMJ, Zucca R, Herreros I (2016) Consensus Paper: Towards a Systems-Level View of Cerebellar Function: the Interplay Between Cerebellum, Basal Ganglia, and Cortex. Cerebellum, Ahead of Print. doi: papers3://publication/doi/10.1007/s12311-016-0763-3

Carmel PW (1970) Efferent projections of the ventral anterior nucleus of the thalamus in the monkey. Am J Anat 128(2):159–183. doi:10.1002/aja.1001280204 CrossRefPubMed

Carpenter MB, Strominger NL (1967) Efferent fibers of the subthalamic nucleus in the monkey. A comparison of the efferent projections of the subthalamic nucleus, substantia nigra and globus pallidus. Am J Anat 121(1):41–72. doi:10.1002/aja.1001210105 CrossRefPubMed

Carter D, Fibiger H (1978) The projections of the entopeduncular nucleus and globus pallidus in rat as demonstrated by autoradiography and horseradish peroxidase histochemistry. J Comp Neurol 177(1):113–123. doi:10.1002/cne.901770108 CrossRefPubMed

Chen CH, Fremont R, Arteaga-Bracho EE, Khodakhah K (2014) Short latency cerebellar modulation of the basal ganglia. Nat Neurosci 17(12):1767–1775. doi:10.1038/nn.3868 CrossRefPubMedPubMedCentral

De Zeeuw CI, Simpson JI, Hoogenraad CC, Galjart N, Koekkoek SK, Ruigrok TJ (1998) Microcircuitry and function of the inferior olive. Trends Neurosci 21(9):391–400. doi:10.1016/S0166-2236(98)01310-1 CrossRefPubMed

DeVito JL, Anderson ME, Walsh KE (1980) A horseradish peroxidase study of afferent connections of the globus pallidus in Macaca mulatta. Exp Brain Res 38(1):65–73. doi:10.1007/BF00237932 CrossRefPubMed

Draganski B, Kherif F, Kloeppel S, Cook PA, Alexander DC, Parker GJM, Deichmann R, Ashburner J, Frackowiak RSJ (2008) Evidence for segregated and integrative connectivity patterns in the human basal ganglia. J Neurosci 28(28):7143–7152. doi:10.1523/JNEUROSCI.1486-08.2008 CrossRefPubMed

Fénelon G, François C, Percheron G, Yelnik J (1990) Topographic distribution of pallidal neurons projecting to the thalamus in macaques. Brain Res 520(1–2):27–35. doi:10.1016/0006-8993(90)91688-D CrossRefPubMed

Gallay MN, Jeanmonod D, Liu J, Morel A (2008) Human pallidothalamic and cerebellothalamic tracts: anatomical basis for functional stereotactic neurosurgery. Brain Struct Func 212(6):443–463. doi:10.1007/s00429-007-0170-0 CrossRef

Galvan A, Smith Y (2011) The primate thalamostriatal systems: anatomical organization, functional roles and possible involvement in Parkinson’s disease. Basal Ganglia 1(4):179–189. doi:10.1016/j.baga.2011.09.001 CrossRefPubMedPubMedCentral

Gotts SJ, Jo HJ, Wallace GL, Saad ZS, Cox RW, Martin A (2013) Two distinct forms of functional lateralization in the human brain. Proc Natl Acad Sci U S A 110(36):E3435–E3444. doi:10.1073/pnas.1302581110 CrossRefPubMedPubMedCentral

Halliday GM (2009) Thalamic changes in Parkinson’s disease. Parkinsonism Relat Disord 15(Supplement 3):S152–S155. doi:10.1016/S1353-8020(09)70804-1 CrossRefPubMed

Harnois C, Filion M (1982) Pallidofugal projections to thalamus and midbrain: a quantitative antidromic activation study in monkeys and cats. Exp Brain Res 47(2):277–285. doi:10.1007/BF00239387 CrossRefPubMed

Haroian AJ, Massopust LC, Young PA (1981) Cerebellothalamic projections in the rat: an autoradiographic and degeneration study. J Comp Neurol 197(2):217–236. doi:10.1002/cne.901970205 CrossRefPubMed

Hirai T, Jones EG (1989) A new parcellation of the human thalamus on the basis of histochemical staining. Brain Res Rev 14(1):1–34. doi:10.1016/0165-0173(89)90007-6 CrossRefPubMed

Hoshi E, Tremblay L, Féger J, Carras PL, Strick PL (2005) The cerebellum communicates with the basal ganglia. Nat Neurosci 8(11):1491–1493. doi:10.1038/nn1544 CrossRefPubMed

Ichinohe N, Shoumura K (1998) A di-synaptic projection from the superior colliculus to the head of the caudate nucleus via the centromedian-parafascicular complex in the cat: an anterograde and retrograde labeling study. Neurosci Res 32(4):295–303. doi:10.1016/S0168-0102(98)00095-9 CrossRefPubMed

Ilinsky KK, Fallet C (2004) Development of the human motor-related thalamic nuclei during the first half of gestation, with special emphasis on GABAergic circuits. J Comp Neurol. doi:10.1002/cne.20216

Ilinsky IA, Kultas-Ilinsky K (1987) Sagittal cytoarchitectonic maps of the Macaca mulatta thalamus with a revised nomenclature of the motor-related nuclei validated by observations on their connectivity. J Comp Neurol 262(3):331–364. doi:10.1002/cne.902620303 CrossRefPubMed

Jbabdi S, Sotiropoulos SN, Haber SN, Van Essen DC, Behrens TE (2015) Measuring macroscopic brain connections in vivo. Nat Neurosci 18(11):1546–1555. doi:10.1038/nn.4134 CrossRefPubMed

Jenkinson M, Smith S (2001a) A global optimisation method for robust affine registration of brain images. Med Image Anal 5(2):143–156. doi:10.1016/S1361-8415(01)00036-6 CrossRefPubMed

Jenkinson M, Smith S (2001b) A global optimisation method for robust affine registration of brain images. Med Image Anal 5(2):143–156CrossRefPubMed

Johansen-Berg H, Behrens TEJ, Sillery E, Ciccarelli O, Thompson AJ, Smith SM, Matthews PM (2005) Functional-anatomical validation and individual variation of diffusion tractography-based segmentation of the human thalamus. Cereb Cortex 15(1):31–39. doi:10.1093/cercor/bhh105 CrossRefPubMed

Jones EG (2007) The thalamus, 2nd edn. Cambridge University Press, New York

Kalil K (1981) Projections of the cerebellar and dorsal column nuclei upon the thalamus of the rhesus monkey. J Comp Neurol 195(1):25–50. doi:10.1002/cne.901950105 CrossRefPubMed

Kim R, Nakano K, Jayaraman A, Carpenter MB (1976) Projections of the globus pallidus and adjacent structures: an autoradiographic study in the monkey. J Comp Neurol 169(3):263–290. doi:10.1002/cne.901690302 CrossRefPubMed

Kincaid AE, Penney JB, Young AB, Newman SW (1991) The globus pallidus receives a projection from the parafascicular nucleus in the rat. Brain Res 553(1):18–26. doi:10.1016/0006-8993(91)90224-J CrossRefPubMed

Klein JC, Rushworth MF, Behrens TE, Mackay CE, de Crespigny AJ, D’Arceuil H, Johansen-Berg H (2010) Topography of connections between human prefrontal cortex and mediodorsal thalamus studied with diffusion tractography. Neuroimage 51(2):555–564. doi:10.1016/j.neuroimage.2010.02.062 CrossRefPubMedPubMedCentral

Krack P, Dostrovsky J, Ilinsky I, Kultas-Ilinsky K, Lenz F, Lozano A, Vitek J (2002) Surgery of the motor thalamus: problems with the present nomenclatures. Mov Disord 17(Suppl 3):S2–S8. doi:10.1002/mds.10136 CrossRefPubMed

Krauth A, Blanc R, Poveda A, Jeanmonod D, Morel A, Székely G (2010) A mean three-dimensional atlas of the human thalamus: generation from multiple histological data. Neuroimage 49(3):2053–2062. doi:10.1016/j.neuroimage.2009.10.042 CrossRefPubMed

Kultas-Ilinsky K, Ilinsky IA, Young PA, Smith KR (1980) Ultrastructure of degenerating cerebellothalamic terminals in the ventral medial nucleus of the cat. Exp Brain Res 38(2):125–135. doi:10.1007/BF00236734 CrossRefPubMed

Kumar V, Mang S, Grodd W (2015) Direct diffusion-based parcellation of the human thalamus. Brain Struct Func 220(3):1619–1635. doi:10.1007/s00429-014-0748-2 CrossRef

Kuo JS, Carpenter MB (2004) Organization of pallidothalamic projections in the rhesus monkey. J Comp Neurol 151(3):201–235. doi:10.1002/cne.901510302 CrossRef

Kuramoto E, Fujiyama F, Nakamura KC, Tanaka Y, Hioki H, Kaneko T (2011) Complementary distribution of glutamatergic cerebellar and GABAergic basal ganglia afferents to the rat motor thalamic nuclei. Eur J Neurosci 33(1):95–109. doi:10.1111/j.1460-9568.2010.07481.x CrossRefPubMed

Kusama T, Mabuchi M, Sumino T (1971) Cerebellar projections to the thalamic nuclei in monkeys. Proc Japan Acad 47:505–510. doi:10.2183/pjab1945.47.505

Larsen KD, Sutin J (1978) Output organization of the feline entopeduncular and subthalamic nuclei. Brain Res 157(1):21–31. doi:10.1016/0006-8993(78)90993-9 CrossRefPubMed

Magnotta VA, Adix ML, Caprahan A, Lim K, Gollub R, Andreasen NC (2008) Investigating connectivity between the cerebellum and thalamus in schizophrenia using diffusion tensor tractography: a pilot study. Psychiatry Res 163(3):193–200. doi:10.1016/j.pscychresns.2007.10.005 CrossRefPubMed

Mai JK, Majtanik M, Paxinos G (2015) Atlas of the human brain, 4th edn. Academic Press, San Diego

Mattay VS, Callicott JH, Bertolino A, Santha AK, Van Horn JD, Tallent KA, Frank JA, Weinberger DR (1998) Hemispheric control of motor function: a whole brain echo planar fMRI study. Psychiatry Res 83(1):7–22. doi:10.1016/S0925-4927(98)00023-7 CrossRefPubMed

Middleton FA, Strick PL (2000) Basal ganglia and cerebellar loops: motor and cognitive circuits. Brain Res Rev 31(2–3):236–250. doi:10.1016/S0165-0173(99)00040-5 CrossRefPubMed

Mitchell AS, Chakraborty S (2013) What does the mediodorsal thalamus do? Front Syst Neurosci 7:37. doi:10.3389/fnsys.2013.00037 CrossRefPubMedPubMedCentral

Mollink J, van Baarsen KM, Dederen PJWC, Foxley S, Miller KL, Jbabdi S, Slump CH, Grotenhuis JA, Kleinnijenhuis M, van Cappellen van Walsum AM (2015) Dentatorubrothalamic tract localization with postmortem MR diffusion tractography compared to histological 3D reconstruction. Brain Struct Func, Ahead of Print. doi:10.1007/s00429-015-1115-7

Morel A (2007) Stereotactic atlas of the human thalamus and basal ganglia. CRC Press, NewYorkCrossRef

Motulsky HJ, Brown RE (2006) Detecting outliers when fitting data with nonlinear regression—a new method based on robust nonlinear regression and the false discovery rate. BMC Bioinform 7:123. doi:10.1186/1471-2105-7-123 CrossRef

Murray MM, Wallace MT (2011) The neural bases of multisensory processes. CRC Press, Boca Raton, FL

Nakamura KC, Sharott A, Magill PJ (2012) Temporal coupling with cortex distinguishes spontaneous neuronal activities in identified basal ganglia-recipient and cerebellar-recipient zones of the motor thalamus. Cereb Cortex. doi:10.1093/cercor/bhs287 PubMedPubMedCentral

Nauta WJ, Mehler WR (1966) Projections of the lentiform nucleus in the monkey. Brain Res 1(1):3–42. doi:10.1016/0006-8993(66)90103-X CrossRefPubMed

O’Muircheartaigh J, Vollmar C, Traynor C, Barker GJ, Kumari V, Symms MR, Thompson P, Duncan JS, Koepp MJ, Richardson MP (2011) Clustering probabilistic tractograms using independent component analysis applied to the thalamus. Neuroimage 54(3):2020–2032. doi:10.1016/j.neuroimage.2010.09.054 CrossRefPubMedPubMedCentral

O’Muircheartaigh J, Keller SS, Barker GJ, Richardson MP (2015) White matter connectivity of the thalamus delineates the functional architecture of competing thalamocortical systems. Cereb Cortex 25(11):4477–4489. doi:10.1093/cercor/bhv063 CrossRefPubMedPubMedCentral

Parent A, De Bellefeuille L (1982) Organization of efferent projections from the internal segment of globus pallidus in primate as revealed by flourescence retrograde labeling method. Brain Res 245(2):201–213. doi:10.1016/0006-8993(82)90802-2 CrossRefPubMed

Pelzer EA, Hintzen A, Goldau M, von Cramon DY, Timmermann L, Tittgemeyer M (2013) Cerebellar networks with basal ganglia: feasibility for tracking cerebello-pallidal and subthalamo-cerebellar projections in the human brain. Eur J Neurosci 38(8):3106–3114. doi:10.1111/ejn.12314 CrossRefPubMed

Penney JB, Young AB (1981) GABA as the pallidothalamic neurotransmitter: implications for basal ganglia function. Brain Res 207(1):195–199. doi:10.1016/0006-8993(81)90693-4 CrossRefPubMed

Percheron G, François C, Talbi B, Yelnik J, Fénelon G (1996) The primate motor thalamus. Brain Res Rev 22(2):93–181. doi:10.1016/S0165-0173(96)00003-3 CrossRefPubMed

Planetta PJ, Schulze ET, Geary EK, Corcos DM, Goldman JG, Little DM, Vaillancourt DE (2013) Thalamic projection fiber integrity in de novo Parkinson disease. Am J Neuroradiol 34(1):74–79. doi:10.3174/ajnr.A3178 CrossRefPubMed

Reese TG, Heid O, Weisskoff RM, Wedeen VJ (2003) Reduction of eddy-current-induced distortion in diffusion MRI using a twice-refocused spin echo. Magn Reson Med 49(1):177–182. doi:10.1002/mrm.10308 CrossRefPubMed

Ristanović D, Milošević NT, Stefanović BD, Marić DL, Rajković K (2010) Morphology and classification of large neurons in the adult human dentate nucleus: a qualitative and quantitative analysis of 2D images. Neurosci Res 67(1):1–7. doi:10.1016/j.neures.2010.01.002 CrossRefPubMed

Rolland A-S, Herrero M-T, Garcia-Martinez V, Ruberg M, Hirsch EC, François C (2006) Metabolic activity of cerebellar and basal ganglia-thalamic neurons is reduced in parkinsonism. Brain 130(1):265–275. doi:10.1093/brain/awl337 CrossRef

Rouiller EME, Liang FF, Babalian AA, Moret VV, Wiesendanger MM (1994) Cerebellothalamocortical and pallidothalamocortical projections to the primary and supplementary motor cortical areas: a multiple tracing study in macaque monkeys. J Comp Neurol 345(2):185–213. doi:10.1002/cne.903450204 CrossRefPubMed

Rozanski VE, Vollmar C, Cunha JP, Tafula SMN, Ahmadi S-A, Patzig M, Mehrkens J-H, Bötzel K (2013) Connectivity patterns of pallidal DBS electrodes in focal dystonia: a diffusion tensor tractography study. Neuroimage 84(1):435–442. doi:10.1016/j.neuroimage.2013.09.009 PubMed

Sadikot AF, Rymar VV (2009) The primate centromedian-parafascicular complex: anatomical organization with a note on neuromodulation. Brain Res Bull 78(2–3):122CrossRefPubMed

Sakai ST, Bruce K (2004) Pallidothalamocortical pathway to the medial agranular cortex in the rat: a double labeling light and electron microscopic study. Thalamus Relat Syst 2(4):273–286. doi:10.1016/j.tharel.2003.12.002 CrossRef

Sakai ST, Patton K (1993) Distribution of cerebellothalamic and nigrothalamic projections in the dog: a double anterograde tracing study. J Comp Neurol 330(2):183–194. doi:10.1002/cne.903300204 CrossRefPubMed

Sakai S, Inase M, Tanji J (1996) Comparison of cerebellothalamic and pallidothalamic projections in the monkey (Macaca fuscata): a double anterograde labeling study. J Comp Neurol 368(2):215–228. doi:10.1002/(SICI)1096-9861(19960429)368:2<215:AID-CNE4>3.0.CO;2-6 CrossRefPubMed

Schaltenbrand G, Wahren W (1977) Atlas for stereotaxy of the human brain, 2nd edn. Thieme, Stuttgart

Schlerf JE, Galea JM, Spampinato D, Celnik PA (2015) Laterality differences in cerebellar-motor cortex connectivity. Cereb Cortex 25(7):1827–1834. doi:10.1093/cercor/bht422 CrossRefPubMed

Schmahmann JD (2003) Vascular syndromes of the thalamus. Stroke 34(9):2264–2278. doi:10.1161/01.STR.0000087786.38997.9E CrossRefPubMed

Scholz VH, Flaherty AW, Kraft E, Keltner JR, Kwong KK, Chen YI, Rosen BR, Jenkins BG (2000) Laterality, somatotopy and reproducibility of the basal ganglia and motor cortex during motor tasks. Brain Res 879(1–2):204–215. doi:10.1016/S0006-8993(00)02749-9 CrossRefPubMed

Seifert S, von Cramon DY, Imperati D, Tittgemeyer M, Ullsperger M (2011) Thalamocingulate interactions in performance monitoring. J Neurosci 31(9):3375–3383. doi:10.1523/JNEUROSCI.6242-10.2011 CrossRefPubMed

Sharman M, Valabregue R, Perlbarg V, Marrakchi-Kacem L, Vidailhet M, Benali H, Brice A, Lehéricy S (2013) Parkinson’s disease patients show reduced cortical-subcortical sensorimotor connectivity. Mov Disord 28(4):447–454. doi:10.1002/mds.25255 CrossRefPubMed

Sidibe M, Bevan MD, Bolam JP, Smith Y (1997) Efferent connections of the internal globus pallidus in the squirrel monkey: I. Topography and synaptic organization of the pallidothalamic projection. J Comp Neurol 382(3):323–347CrossRefPubMed

Smith SM (2002) Fast robust automated brain extraction. Hum Brain Mapp 17(3):143–155. doi:10.1002/hbm.10062 CrossRefPubMed

Smith Y, Raju D, Nanda B, Pare J-F, Galvan A, Wichmann T (2009) The thalamostriatal systems: anatomical and functional organization in normal and parkinsonian states. Brain Res Bull 78(2–3):60–68. doi:10.1016/j.brainresbull.2008.08.015 CrossRefPubMed

Smith Y, Galvan A, Ellender TJ, Doig N, Villalba RM, Huerta-Ocampo I, Wichmann T, Bolam JP (2014) The thalamostriatal system in normal and diseased states. Front Syst Neurosci 8:5. doi:10.3389/fnsys.2014.00005 PubMedPubMedCentral

Snider RS, Maiti A (1976) Cerebellar contributions to the Papez circuit. J Neurosci Res 2(2):133–146. doi:10.1002/jnr.490020204 CrossRefPubMed

Stanton GB (1980) Topographical organization of ascending cerebellar projections from the dentate and interposed nuclei in Macaca mulatta: an anterograde degeneration study. J Comp Neurol 190(4):699–731. doi:10.1002/cne.901900406 CrossRefPubMed

Stephan KE, Fink GR, Marshall JC (2007) Mechanisms of hemispheric specialization: insights from analyses of connectivity. Neuropsychologia 45(2):209–228. doi:10.1016/j.neuropsychologia.2006.07.002 CrossRefPubMedPubMedCentral

Stephan KE, Tittgemeyer M, Knösche TR, Moran RJ, Friston KJ (2009) Tractography-based priors for dynamic causal models. Neuroimage 47(4):1628–1638. doi:10.1016/j.neuroimage.2009.05.096 CrossRefPubMedPubMedCentral

Traynor C, Heckemann RA, Hammers A, O’Muircheartaigh J, Crum WR, Barker GJ, Richardson MP (2010) Reproducibility of thalamic segmentation based on probabilistic tractography. Neuroimage 52(1):69–85. doi:10.1016/j.neuroimage.2010.04.024 CrossRefPubMed

Van der Werf YD, Witter MP, Groenewegen HJ (2002) The intralaminar and midline nuclei of the thalamus. Anatomical and functional evidence for participation in processes of arousal and awareness. Brain Res Rev 39(2–3):107–140. doi:10.1016/S0165-0173(02)00181-9 CrossRefPubMed

Vogt C, Vogt O (1920) Zur Lehre der Erkrankungen des striatären systems. J Psychol Neurol 25(suppl 3):627–846

Vogt C, Vogt O (1941) Thalamusstudien I-III. J Psychol Neurol 50:33–154

Wichmann T, DeLong MR (1996) Functional and pathophysiological models of the basal ganglia. Curr Opin Neurobiol 6(6):751–758. doi:10.1016/S0959-4388(96)80024-9 CrossRefPubMed

Wu T, Hallett M (2013) The cerebellum in Parkinson’s disease. Brain 136(Pt 3):696–709. doi:10.1093/brain/aws360 CrossRefPubMed

Yasukawa TT, Kita TT, Xue YY, Kita HH (2004) Rat intralaminar thalamic nuclei projections to the globus pallidus: a biotinylated dextran amine anterograde tracing study. J Comp Neurol 471(2):153–167. doi:10.1002/cne.20029 CrossRefPubMed

Title: Basal ganglia and cerebellar interconnectivity within the human thalamus
Authors: Esther A. Pelzer
Corina Melzer
Lars Timmermann
D. Yves von Cramon
Marc Tittgemeyer
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/s00429-016-1223-z

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Basal ganglia and cerebellar interconnectivity within the human thalamus

Abstract

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 1/2017

Oxidative and nitrosative stress pathways in the brain of socially isolated adult male rats demonstrating depressive- and anxiety-like symptoms

Activity in the rat olfactory cortex is correlated with behavioral response to odor: a microPET study

Neuroanatomy of the killer whale (Orcinus orca): a magnetic resonance imaging investigation of structure with insights on function and evolution

Embryonic interneurons from the medial, but not the caudal ganglionic eminence trigger ocular dominance plasticity in adult mice

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

Deep brain stimulation of the nucleus ventralis intermedius: a thalamic site of graviceptive modulation