Skip to main content
SpringerLink
Log in

The anatomo-functional organization of the hyperdirect cortical pathway to the subthalamic area using in vivo structural connectivity imaging in humans

  • Original Article
  • Published:
Brain Structure and Function Aims and scope Submit manuscript

Abstract

The subthalamic nucleus (STN) receives direct cortical inputs which constitute the so-called hyperdirect pathway. In monkeys, motor cortices innervate the whole extent of the STN whereas limbic cortices innervate only its anteromedial part extending more medially outside the nucleus. Tractography studies in humans have also identified motor cortical inputs to the STN, but little is known about the associative and limbic cortical projections. Therefore, the aim of this study was to investigate the anatomo-functional organization of the cortical projections to the STN and to the adjacent medial subthamic region (MSR). We used diffusion-weighted imaging-based tractography acquired from 30 subjects from the Human Connectome Project. We performed a whole-brain probabilistic tractography using MRTrix and extracted streamlines of interest between 39 cortical masks and both the STN and the MSR to provide track-density maps. Agglomerative clustering method was used to classify the voxels of the regions of interest. We found that the STN receives major inputs from the sensorimotor cortices and few inputs from the limbic cortices. On the other hand, the MSR receives mainly cortical limbic projections and few from the sensorimotor cortices. Weak connections were found between the associative cortices and both the STN and the MSR. We found a dominant motor cluster located in the posterolateral STN, a limbic cluster located medially in the MSR, and an intermediate motor-limbic cluster in between. Our findings show that the hyperdirect pathway is anatomo-functionally organized with a poor participation of associative cortices.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

BA:

Brodmann areas

DBS:

Deep brain stimulation

DWI:

Diffusion-weighted imaging

FA:

Fractional anisotropy

FOD:

Fiber orientation distributions

MSR:

Medial subthalamic region

MR:

Magnetic resonance

MRI:

Magnetic resonance imaging

PD:

Parkinson’s disease

ROI:

Region of interest

STN:

Subthalamic nucleus

LH:

Left hemisphere

RH:

Right hemisphere

References

  • Accolla EA, Dukart J, Helms G, Weiskopf N, Kherif F, Lutti A, Chowdhury R, Hetzer S, Haynes JR, Kühn AA, Draganski B (2014) Brain tissue properties differentiate between motor and limbic basal ganglia circuits. Hum Brain Mapp 35(10):5083–5092

    PubMed  PubMed Central  Google Scholar 

  • Afsharpour S (1985) Topographical projections of the cerebral cortex to the subthalamic nucleus. J Comp Neurol 236:14–28

    CAS  PubMed  Google Scholar 

  • Akram H, Miller S, Lagrata S, Hariz M, Ashburner J, Behrens T, Matharu M, Zrinzo L (2017a) Optimal deep brain stimulation site and target connectivity for chronic cluster headache. Neurology 89(20):2083–2091. https://doi.org/10.1212/WNL.0000000000004646

    Article  PubMed  PubMed Central  Google Scholar 

  • Akram H, Sotiropoulos SN, Jbabdi S, Georgiev D, Mahlknecht P, Hyam J, Foltynie T, Limousin P, De Vita E, Jahanshahi M, Hariz M, Ashburner J, Behrens T, Zrinzo L (2017b) Subthalamic deep brain stimulation sweet spots and hyperdirect cortical connectivity in Parkinson’s disease. NeuroImage 158:332–345. https://doi.org/10.1016/j.neuroimage.2017b.07.012

    Article  PubMed  PubMed Central  Google Scholar 

  • Alkemade A, Forstmann BU (2014) Do we need to revise the tripartite subdivision hypothesis of the human subthalamic nucleus (STN)? NeuroImage 95:326–329

    PubMed  Google Scholar 

  • Andersson JL, Sotiropoulos SN (2015) Non-parametric representation and prediction of single- and multi-shell diffusion-weighted MRI data using Gaussian processes. NeuroImage 122:166–176

    PubMed  PubMed Central  Google Scholar 

  • Aravamuthan BR, Muthusamy KA, Stein JF, Aziz TZ, Johansen-Berg H (2007) Topography of cortical and subcortical connections of the human pedunculopontine and subthalamic nuclei. NeuroImage 37:694–705. https://doi.org/10.1016/j.neuroimage.2007.05.050

    Article  CAS  PubMed  Google Scholar 

  • Aron AR, Behrens TE, Smith S, Frank MJ, Poldrack RA (2007) Triangulating a cognitive control network using diffusion-weighted magnetic resonance imaging (MRI) and functional MRI. J Neurosci 27(14):3743–3752

    CAS  PubMed  PubMed Central  Google Scholar 

  • Avecillas-Chasin JM, Rascón-Ramírez F (2016) Tractographical model of the cortico-basal ganglia and corticothalamic connections: improving our understanding of deep brain stimulation. Clin Anat 29(4):481–492

    PubMed  Google Scholar 

  • Bardinet E, Bhattacharjee M, Dormont D, Pidoux B, Malandain G, Schüpbach M, Ayache N, Cornu P, Agid Y, Yelnik J (2009) A three-dimensional histological atlas of the human basal ganglia. II. Atlas deformation strategy and evaluation in deep brain stimulation for Parkinson disease. J Neurosurg 110:208–219. https://doi.org/10.3171/2008.3.17469

    Article  PubMed  Google Scholar 

  • Bejjani BP, Houeto JL, Hariz M, Yelnik J, Mesnage V, Bonnet AM, Pidoux B, Dormont D, Cornu P, Agid Y (2002) Aggressive behavior induced by intraoperative stimulation in the triangle of Sano. Neurology 59(9):1425–1427

    CAS  PubMed  Google Scholar 

  • Benabid AL, Chabardes S, Mitrofanis J, Pollak P (2000) Deep brain stimulation of the subthalamic nucleus for the treatment of Parkinson’s disease. Lancet Neurol 8(1):67–81. https://doi.org/10.1016/S1474-4422(08)70291-6

    Article  Google Scholar 

  • Brunenberg EJ, Moeskops P, Backes WH, Pollo C, Cammoun L, Vilanova A, Janssen ML, Visser-Vandewalle VE, ter Haar Romeny BM, Thiran JP, Platel B (2012) Structural and resting state functional connectivity of the subthalamic nucleus: identification of motor STN parts and the hyperdirect pathway. PLoS One 7(6):e39061

    CAS  PubMed  PubMed Central  Google Scholar 

  • Calamante F, Tournier JD, Jackson GD, Connelly A (2010) Track-density imaging (TDI): super-resolution white matter imaging using whole-brain track-density mapping. NeuroImage 53:1233–1243

    PubMed  Google Scholar 

  • Canteras NS, Shammah-Lagnado SJ, Silva BA, Ricardo JA (1990) Afferent connections of the subthalamic nucleus: a combined retrograde and anterograde horseradish peroxidase study in the rat. Brain Res 513:43–59

    CAS  PubMed  Google Scholar 

  • Chabardès S, Polosan M, Krack P, Bastin J, Krainik A, David O, Bougerol T, Benabid AL (2013) Deep brain stimulation for obsessive-compulsive disorder: subthalamic nucleus target. World Neurosurg 80(3–4):S31.e1-8. https://doi.org/10.1016/j.wneu.2012.03.010

    Article  PubMed  Google Scholar 

  • Christiaens D, Reiser M, Dhollander T, Sunaert S, Suetens P, Global Maes F (2015) tractography of multi shell diffusion weighted imaging data using a multi-tissue model. NeuroImage 123:89–101

    PubMed  Google Scholar 

  • Coenen VA, Schlaepfer TE, Maedler B, Panksepp J (2011) Cross-species affective functions of the medial forebrain bundle-implications for the treatment of affective pain and depression in humans. Neurosci Biobehav Rev 35(9):1971–1981. https://doi.org/10.1016/j.neubiorev.2010.12.009

    Article  PubMed  Google Scholar 

  • Coenen VA, Schumacher LV, Kaller C, Schlaepfer TE, Reinacher PC, Egger K, Urbach H, Reisert M (2018) The anatomy of the human medial forebrain bundle: ventral tegmental area connections to reward-associated subcortical and frontal lobe regions. Neuroimage Clin 18:770–783. https://doi.org/10.1016/j.nicl.2018.03.019

    Article  PubMed  PubMed Central  Google Scholar 

  • Coudé D, Parent A, Parent M (2018) Single-axon tracing of the corticosubthalamic hyperdirect pathway in primates. Brain Struct Funct 223(9):3959–3973. https://doi.org/10.1007/s00429-018-1726-x

    Article  PubMed  Google Scholar 

  • Crossman AR, Sambrook MA, Jackson A (1984) Experimental hemichorea/hemiballismus in the monkey. Studies on the intracerebral site of action in a drug-induced dyskinesia. Brain 107(Pt 2):579–596

    PubMed  Google Scholar 

  • Dhollander T, Raffelt D, Connelly A (2016) Unsupervised 3-tissue response function estimation from single-shell or multi-shell diffusion MR data without a co-registered T1 image. ISMRM Workshop on Breaking the Barriers of Diffusion MRI, 5

  • Forel A (1877) Untersuchungen über die Haubenregion und ihre oberen Verknüpfungen im Gehirne des Menschen und einiger Säugethiere, mit Beiträgen zu den Methoden der Gehirnuntersuchung. Archiv für Psychiatrie und Nervenkrankheiten. Springer-Verlag 7(3):393–495

    Google Scholar 

  • François C, Grabli D, McCairn K, Jan C, Karachi C, Hirsch EC, Féger J, Tremblay L (2004) Behavioural disorders induced by external globus pallidus dysfunction in primates II. Anatomical study. Brain 127(Pt 9):2055–2070

    PubMed  Google Scholar 

  • Franzini A, Ferroli P, Leone M, Broggi G (2003) Stimulation of the posterior hypothalamus for treatment of chronic intractable cluster headaches: first reported series. Neurosurgery 52(5):1095–1099

    PubMed  Google Scholar 

  • Franzini A, Broggi G, Cordella R, Dones I, Messina G (2013) Deep-brain stimulation for aggressive and disruptive behavior. World Neurosurg 80(3–4):S29

    PubMed  Google Scholar 

  • Gan G, Ma C, Wu J (2007) Data clustering: theory, algorithms, and applications. Vol 20 Siam

  • Glasser MF, Sotiropoulos SN, Wilson JA, Coalson TS, Fischl B, Andersson JL, Xu J, Jbabdi S, Webster M, Polimeni JR, Van Essen DC, Jenkinson M (2013) The minimal preprocessing pipelines for the Human Connectome Project. Neuroimage 80:105–124. https://doi.org/10.1016/j.neuroimage.2013.04.127

    Article  PubMed  PubMed Central  Google Scholar 

  • Goto M, Swanson LW (2004) Axonal projections from the parasubthalamic nucleus. J Comp Neurol 169(4):581–607

    Google Scholar 

  • Haber SN, Lynd-Balta E, Mitchell SJ (1993) The organization of the descending ventral pallidal projections in the monkey. J Comp Neurol 329(1):111–128

    CAS  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  PubMed Central  Google Scholar 

  • Hammond C, Yelnik J (1983) Intracellular labelling of rat subthalamic neurones with horseradish peroxidase: computer analysis of dendrites and characterization of axon arborization. Neuroscience 8(4):781–790

    CAS  PubMed  Google Scholar 

  • Hartmann-von Monakow K, Akert K, Künzle H (1978) Projections of the precentral motor cortex and other cortical areas of the frontal lobe to the subthalamic nucleus in the monkey. Exp Brain Res 33:395–403

    Google Scholar 

  • Haynes W, Haber S (2013) The organization of prefrontal subthalamic inputs in primates provides an anatomical substrate for both functional specificity and integration: implications for basal ganglia models and deep brain stimulation. J Neurosci 33:4804–4814

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jbabdi S, Sotiropoulos SN, Haber SN, Van Essen DC, Behrens TE (2015) Measuring macroscopic brain connections in vivo. Nat Neurosci 18(11):1546–1555. https://doi.org/10.1038/nn.4134Epub 2015 Oct 27

    Article  CAS  PubMed  Google Scholar 

  • Jeurissen B, Tournier JD, Dhollander T, Connelly A, Sijbers J (2014) Multi-tissue constrained spherical deconvolution for improved analysis of multi-shell diffusion MRI data. Neuroimage 103:411–426

    PubMed  Google Scholar 

  • Jürgens U (1984) The efferent and afferent connections of the supplementary motor area. Brain Res 300:63–81

    PubMed  Google Scholar 

  • Karachi C, Yelnik J, Tandé D, Tremblay L, Hirsch E, François C (2005) The pallido- subthalamic projection: an anatomical substrate for nonmotor functions of the subthalamic nucleus in primates. Mov Disord 20(2):172–180

    PubMed  Google Scholar 

  • Karachi C, Grabli D, Baup N, Mounayar S, Tandé D, François C, Hirsch EC (2009) Dysfunction of the subthalamic nucleus induces behavioral and movement disorders in monkeys. Mov Disord 24(8):1183–1192. https://doi.org/10.1002/mds.22547

    Article  PubMed  Google Scholar 

  • Kim JS, Kim HJ, Lee JY, Kim JM, Yun JY, Jeon BS (2012) Hypomania induced by subthalamic nucleus stimulation in a Parkinson’s disease patient: does it suggest a dysfunction of the limbic circuit? J Mov Disord 5(1):14–17. https://doi.org/10.14802/jmd.12004

    Article  PubMed  PubMed Central  Google Scholar 

  • Künzle H (1975) Bilateral projections from precentral motor cortex to the putamen and other parts of the basal ganglia. An autoradiographic study in Macaca fascicularis. Brain Res 88:195–209

    PubMed  Google Scholar 

  • Künzle H (1978) An autoradiographic analysis of the efferent connections from premotor and adjacent prefrontal regions (areas 6 and 9) in Macaca fascicularis. Brain Behav Evol 15:185–234

    PubMed  Google Scholar 

  • Künzle H, Akert K (1977) Efferent connections of cortical, area 8 (frontal eye field) in Macaca fascicularis. A reinvestigation using the autoradiographic technique. J Comp Neurol 173:147–164

    PubMed  Google Scholar 

  • Lambert C, Zrinzo L, Nagy Z, Lutti A, Hariz M, Foltynie T, Draganski B, Ashburner J, Frackowiak R (2012) Confirmation of functional zones within the human subthalamic nucleus: patterns of connectivity and sub-parcellation using diffusion weighted imaging. Neuroimage 60:83–94. https://doi.org/10.1016/j.neuroimage.2011.11.082

    Article  PubMed  PubMed Central  Google Scholar 

  • Lambert C, Zrinzo L, Nagy Z, Lutti A, Hariz M, Foltynie T, Draganski B, Ashburner J, Frackowiak R (2015) Do we need to revise the tripartite subdivision hypothesis of the human subthalamic nucleus (STN)? Response to Alkemade and Forstmann. Neuroimage 110:1–2. https://doi.org/10.1016/j.neuroimage.2015.01.038

    Article  PubMed  Google Scholar 

  • Leone M, Franzini A, Bussone G (2001) Stereotactic stimulation of posterior hypothalamic gray matter in a patient with intractable cluster headache. N Engl J Med 345(19):1428–1429

    CAS  PubMed  Google Scholar 

  • Limousin P, Krack P, Pollak P, Benazzouz A, Ardouin C, Hoffman D, Benabid AL (1998) Electrical stimulation of the subthalamic nucleus in advanced Parkinson’s disease. N Engl J Med 339:1105–1111

    CAS  PubMed  Google Scholar 

  • Maier-Hein KH, Neher PF, Houde JC, Côté MA, Garyfallidis E, Zhong J, Chamberland M, Descoteaux M (2017) The challenge of mapping the human connectome based on diffusion tractography. Nat Commun 8:1349. https://doi.org/10.1038/s41467-017-01285-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mallet L, Schüpbach M, N’Diaye K, Remy P, Bardinet E, Czernecki V, Welter ML, Pelissolo A, Ruberg M, Agid Y, Yelnik J (2007) Stimulation of subterritories of the subthalamic nucleus reveals its role in the integration of the emotional and motor aspects of behavior. Proc Natl Acad Sci USA 104(25):10661–10666

    CAS  PubMed  Google Scholar 

  • Mallet L, Polosan M, Jaafari N, Baup N, Welter ML, Fontaine D, du Montcel ST, Yelnik J, Chéreau I, Arbus C, Raoul S, Aouizerate B, Damier P, Chabardès S, Czernecki V, Ardouin C, Krebs MO, Bardinet E, Chaynes P, Burbaud P, Cornu P, Derost P, Bougerol T, Bataille B, Mattei V, Dormont D, Devaux B, Vérin M, Houeto JL, Pollak P, Benabid AL, Agid Y, Krack P, Millet B, Pelissolo A, STOC Study Group (2008) Subthalamic nucleus stimulation in severe obsessive-compulsive disorder. N Engl J Med 359(20):2121–2134

    CAS  PubMed  Google Scholar 

  • Maurice N, Deniau JM, Glowinski J, Thierry A (1998) Relationships between the prefrontal cortex and the basal ganglia in the rat: physiology of the corticosubthalamic circuits. J Neurosci 18(22):9539–9546

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mulder MJ, Boekel W, Ratcliff R, Forstmann BU (2014) Cortico-subthalamic connection predicts individual differences in value-driven choice bias. Brain Struct Funct 219(4):1239–1249

    PubMed  Google Scholar 

  • Nambu A, Takada M, Inase M, Tokuno H (1996) Dual somatotopical representations in the primate subthalamic nucleus: evidence for ordered but reversed body-map transformations from the primary motor cortex and the supplementary motor area. J Neurosci 16(8):2671–2683

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nambu A, Tokuno H, Inase M, Takada M (1997) Corticosubthalamic input zones from forelimb representations of the dorsal and ventral divisions of the premotor cortex in the macaque monkey: comparison with the input zones from the primary motor cortex and the supplementary motor area. Neurosci Lett 239:13–16

    CAS  PubMed  Google Scholar 

  • Neudorfer C, Maarouf M (2018) Neuroanatomical background and functional considerations for stereotactic interventions in the H fields of Forel. Brain Struct Funct 223(1):17–30. https://doi.org/10.1007/s00429-017-1570-4

    Article  PubMed  Google Scholar 

  • Parent A, Hazrati LN (1995) Functional anatomy of the basal ganglia. II. The place of subthalamic nucleus and external pallidum in basal ganglia circuitry. Brain Res Rev 20(1):128–154

    CAS  PubMed  Google Scholar 

  • Petersen MV, Lund TE, Sunde N, Frandsen J, Rosendal F, Juul N, Østergaard K (2016) Probabilistic versus deterministic tractography for delineation of the cortico-subthalamic hyperdirect pathway in patients with Parkinson disease selected for deep brain stimulation. J Neurosurg 126(5):1657–1668

    PubMed  Google Scholar 

  • Rizzi M, Trezza A, Messina G, De Benedictis A, Franzini A, Marras CE (2017) Exploring the brain through posterior hypothalamus surgery for aggressive behavior. Neurosurg Focus 43(3):E14. https://doi.org/10.3171/2017.6.FOCUS17231

    Article  PubMed  Google Scholar 

  • Rizzolatti G, Fogassi L, Gallese V (2002) Motor and cognitive functions of the ventral premotor cortex. Curr Opin Neurobiol 12(2):149–154

    CAS  PubMed  Google Scholar 

  • Sano K (1962) Sedative neurosurgery with special reference to posteromedial hypothalamotomy. Neurol Me Chi (Tokyo) 4:112–142

    Google Scholar 

  • Sano K, Yoshioka M, Ogashiwa M, Ishijima B, Ohye C (1966) Postero-medial hypothalamotomy in the treatment of aggressive behaviors. Confinia neurol 27:164–167

    CAS  Google Scholar 

  • Sano K, Mayanagi Y, Sekino H, Ogashiwa M, Ishijima B (1970) Results of stimulation and destruction of the posterior hypothalamus in man. J Neurosurg 33(6):689–707

    CAS  PubMed  Google Scholar 

  • Sébille SB, Belaid H, Philippe AC, André A, Lau B, François C, Karachi C, Bardinet E (2017) Anatomical evidence for functional diversity in the mesencephalic locomotor region of primates. Neuroimage 147:66–78. https://doi.org/10.1016/j.neuroimage.2016.12.011

    Article  PubMed  Google Scholar 

  • Shink E, Bevan MD, Bolam JP, Smith Y (1996) The subthalamic nucleus and the external pallidum: two tightly interconnected structures that control the output of the basal ganglia in the monkey. Neuroscience 73:335–357

    CAS  PubMed  Google Scholar 

  • Shook BL, Schlag-Rey M, Schlag J (1991) Primate supplementary eye field. II. Comparative aspects of connections with the thalamus, corpus striatum, and related forebrain nuclei. J Comp Neurol 307:562–583

    CAS  PubMed  Google Scholar 

  • Sinke M, Otte W, Christiaens D, Schmitt O, Leemans A, Toorn A, Sarabdjitsingh A, Joels M, Dijkhuizen R (2018) Diffusion MRI-based cortical connectome reconstruction: dependency on tractography procedures and neuroanatomical characteristics. Brain Struct Func 223(5):2269–2285

    Google Scholar 

  • Smith RE, Tournier JD, Calamante E, Connelly A (2013) SIFT: spherical-deconvolution informed filtering of tractograms. NeuroImage 67:298–312

    PubMed  Google Scholar 

  • Sotiropoulos SN, Jbabdi S, Xu J, Andersson JL, Moeller S, Auerbach EJ, Glasser MF, Hernandez M, Sapiro G, Jenkinson M, Feinberg DA, Yacoub E, Lenglet C, Van Essen DC, Ugurbil K, Behrens TEJ (2013) Advances in diffusion MRI acquisition and processing in the Human Connectome Project. Neuroimage 80:125–143. https://doi.org/10.1016/j.neuroimage.2013.05.057

    Article  PubMed  PubMed Central  Google Scholar 

  • Takada M, Tokuno H, Hamada I, Inase M, Ito Y, Imanishi M, Hasegawa N, Akazawa T, Hatanaka N, Nambu A (2001) Organization of inputs from cingulate motor areas to basal ganglia in macaque monkey. Eur J Neurosci 14(10):1633–1650

    CAS  PubMed  Google Scholar 

  • Tournier JD, Calamante F, Connelly A (2010) Improved probabilistic streamlines tractography by 2nd order integration over fibre orientation distributions. Proc Intl Soc Mag Reson Med (ISMRM) 18:1670

    Google Scholar 

  • Tournier JD, Calamante F, Connelly A (2012) MRtrix: diffusion tractography in crossing fiber regions. Int J Imaging Syst Technol 22:53–66. https://doi.org/10.1002/ima.22005

    Article  Google Scholar 

  • Ugurlu D, Firat Z, Ture U, Unal G (2018) Neighborhood resolved fiber orientation distributions (NRFOD) in automatic labeling of white matter fiber pathways. Med Image Anal 46:130–145

    PubMed  Google Scholar 

  • Van Essen DC, Smith SM, Barch DM, Behrens TEJ, Yacoub E, Ugurbil K (2013) The WU-minn human connectome project: an overview. Neuroimage 80:62–79. https://doi.org/10.1016/j.neuroimage.2013.05.041

    Article  PubMed  PubMed Central  Google Scholar 

  • Veazey RB, Amaral DG, Cowan WM (1982) The morphology and connections of the posterior hypothalamus in the cynomolgus monkey (Macaca fascicularis). II. Efferent connections. J Comp Neurol 207(2):135–156

    CAS  PubMed  Google Scholar 

  • Wang L, Mruczek EB, Arcaro MJ, Kastner S (2018) Probabilistic maps of visual topography in human cortex. Cereb Cortex 25:3911–3931

    Google Scholar 

  • Welter ML, Schüpbach M, Czernecki V, Karachi C, Fernandez-Vidal S, Golmard JL, Serra G, Navarro S, Welaratne A, Hartmann A, Mesnage V, Pineau F, Cornu P, Pidoux B, Worbe Y, Zikos P, Grabli D, Galanaud D, Bonnet AM, Belaid H, Dormont D, Vidailhet M, Mallet L, Houeto JL, Bardinet E, Yelnik J, Agid Y (2014) Optimal target localization for subthalamic stimulation in patients with Parkinson disease. Neurology 82(15):1352–1361

    PubMed  PubMed Central  Google Scholar 

  • Wilkins B, Lee N, Gajawelli N, Law M, Leporé N (2015) Fiber estimation and tractography in diffusion MRI: development of simulated brain images and comparison of multi-fiber analysis methods at clinical b-values. Neuroimage 109:341–356

    PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by ‘Investissements d’avenir’ (Investing in the future programme ANR-10-IAIHU-O6). G. Temiz was supported by the “Fondation pour la Recherche” Médicale (FRM) (Project:DIC20161236441) and by Boston Scientific. The authors would like to thank Max Westby for language editing.

Funding

This work was supported by ‘Investissements d’avenir’ (Investing in the future programme ANR-10-IAIHU-O6). G. Temiz was supported by the “Fondation pour la Recherche” Médicale (FRM) (Project:DIC20161236441) and by Boston Scientific.

Author information

Authors and Affiliations

  1. Sorbonne Universités, UPMC Univ Paris 06, CNRS, INSERM, APHP GH Pitié-Salpêtrière, Institut du cerveau et de la moelle épinière (ICM), 75013, Paris, France

    Gizem Temiz, Sophie B. Sébille, Chantal Francois, Eric Bardinet & Carine Karachi

  2. Center for Neuroimaging Research, CENIR, Paris, France

    Gizem Temiz, Sophie B. Sébille & Eric Bardinet

  3. Department of Neurosurgery, AP-HP, Hôpital de la Pitié-Salpêtrière, Paris, France

    Carine Karachi

Authors
  1. Gizem Temiz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sophie B. Sébille
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chantal Francois
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Eric Bardinet
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Carine Karachi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Chantal Francois.

Ethics declarations

Conflict of interest

The authors declare no other conflicts of interest

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 11 kb)

Supplementary material 2 (TIFF 36792 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Temiz, G., Sébille, S.B., Francois, C. et al. The anatomo-functional organization of the hyperdirect cortical pathway to the subthalamic area using in vivo structural connectivity imaging in humans. Brain Struct Funct 225, 551–565 (2020). https://doi.org/10.1007/s00429-019-02012-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-019-02012-6

Keywords

Search

Navigation