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Published in: Brain Structure and Function 6/2015

Open Access 01-11-2015 | Review

Topographic organization of the human and non-human primate subthalamic nucleus

Authors: Anneke Alkemade, Alfons Schnitzler, Birte U. Forstmann

Published in: Brain Structure and Function | Issue 6/2015

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Abstract

Deep brain stimulation (DBS) of the subthalamic nucleus (STN) is used to relieve motor symptoms of Parkinson’s disease. A tripartite system of STN subdivisions serving motoric, associative, and limbic functions was proposed, mainly based on tracing studies, which are limited by low numbers of observations. The evidence is compelling and raises the question as to what extent these functional zones are anatomically segregated. The majority of studies indicate that there is anatomical overlap between STN functional zones. Using ultrahigh-resolution magnetic resonance imaging techniques it is now possible to visualize the STN with high spatial resolution, and it is feasible that in the near future stereotactic guided placement of electrical stimulators aided by high-resolution imaging will allow for more specific stimulation of the STN. The neuroanatomical and functional makeup of these subdivisions and their level of overlap would benefit from clarification before serving as surgical targets. We discuss histological and imaging studies, as well as clinical observations and electrophysiological recordings in DBS patients. These studies provide evidence for a topographical organization within the STN, although it remains unclear to what extent functionally and anatomically distinct subdivisions overlap.
Literature
go back to reference Absher JR, Vogt BA, Clark DG, Flowers DL, Gorman DG, Keyes JW, Wood FB (2000) Hypersexuality and hemiballism due to subthalamic infarction. Neuropsychiatry Neuropsychol Behav Neurol 13(3):220–229PubMed Absher JR, Vogt BA, Clark DG, Flowers DL, Gorman DG, Keyes JW, Wood FB (2000) Hypersexuality and hemiballism due to subthalamic infarction. Neuropsychiatry Neuropsychol Behav Neurol 13(3):220–229PubMed
go back to reference Alegre M, Lopez-Azcarate J, Obeso I, Wilkinson L, Rodriguez-Oroz MC, Valencia M, Garcia-Garcia D, Guridi J, Artieda J, Jahanshahi M, Obeso JA (2013) The subthalamic nucleus is involved in successful inhibition in the stop-signal task: a local field potential study in Parkinson’s disease. Exp Neurol 239:1–12. doi:10.1016/j.expneurol.2012.08.027 CrossRefPubMed Alegre M, Lopez-Azcarate J, Obeso I, Wilkinson L, Rodriguez-Oroz MC, Valencia M, Garcia-Garcia D, Guridi J, Artieda J, Jahanshahi M, Obeso JA (2013) The subthalamic nucleus is involved in successful inhibition in the stop-signal task: a local field potential study in Parkinson’s disease. Exp Neurol 239:1–12. doi:10.​1016/​j.​expneurol.​2012.​08.​027 CrossRefPubMed
go back to reference Alexander GE, Crutcher MD (1990) Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci 13(7):266–271CrossRefPubMed Alexander GE, Crutcher MD (1990) Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci 13(7):266–271CrossRefPubMed
go back to reference Aubert I, Guigoni C, Li Q, Dovero S, Bioulac BH, Gross CE, Crossman AR, Bloch B, Bezard E (2007) Enhanced preproenkephalin-B-derived opioid transmission in striatum and subthalamic nucleus converges upon globus pallidus internalis in L-3,4-dihydroxyphenylalanine-induced dyskinesia. Biol Psychiatry 61(7):836–844. doi:10.1016/j.biopsych.2006.06.038 CrossRefPubMed Aubert I, Guigoni C, Li Q, Dovero S, Bioulac BH, Gross CE, Crossman AR, Bloch B, Bezard E (2007) Enhanced preproenkephalin-B-derived opioid transmission in striatum and subthalamic nucleus converges upon globus pallidus internalis in L-3,4-dihydroxyphenylalanine-induced dyskinesia. Biol Psychiatry 61(7):836–844. doi:10.​1016/​j.​biopsych.​2006.​06.​038 CrossRefPubMed
go back to reference Augood SJ, Waldvogel HJ, Munkle MC, Faull RL, Emson PC (1999) Localization of calcium-binding proteins and GABA transporter (GAT-1) messenger RNA in the human subthalamic nucleus. Neuroscience 88(2):521–534CrossRefPubMed Augood SJ, Waldvogel HJ, Munkle MC, Faull RL, Emson PC (1999) Localization of calcium-binding proteins and GABA transporter (GAT-1) messenger RNA in the human subthalamic nucleus. Neuroscience 88(2):521–534CrossRefPubMed
go back to reference Augood SJ, Hollingsworth ZR, Standaert DG, Emson PC, Penney JB Jr (2000) Localization of dopaminergic markers in the human subthalamic nucleus. J Comp Neurol 421(2):247–255CrossRefPubMed Augood SJ, Hollingsworth ZR, Standaert DG, Emson PC, Penney JB Jr (2000) Localization of dopaminergic markers in the human subthalamic nucleus. J Comp Neurol 421(2):247–255CrossRefPubMed
go back to reference Buot A, Welter ML, Karachi C, Pochon JB, Bardinet E, Yelnik J, Mallet L (2012) Processing of emotional information in the human subthalamic nucleus. J Neurol Neurosurg Psychiatry. doi:10.1136/jnnp-2011-302158 PubMed Buot A, Welter ML, Karachi C, Pochon JB, Bardinet E, Yelnik J, Mallet L (2012) Processing of emotional information in the human subthalamic nucleus. J Neurol Neurosurg Psychiatry. doi:10.​1136/​jnnp-2011-302158 PubMed
go back to reference Chang C, Li N, Wu Y, Geng N, Ge S, Wang J, Wang X, Wang X (2012) Associations between bilateral subthalamic nucleus deep brain stimulation (STN-DBS) and anxiety in Parkinson’s disease patients: a controlled study. J Neuropsychiatry Clin Neurosci 24(3):316–325. doi:10.1176/appi.neuropsych.11070170 CrossRefPubMed Chang C, Li N, Wu Y, Geng N, Ge S, Wang J, Wang X, Wang X (2012) Associations between bilateral subthalamic nucleus deep brain stimulation (STN-DBS) and anxiety in Parkinson’s disease patients: a controlled study. J Neuropsychiatry Clin Neurosci 24(3):316–325. doi:10.​1176/​appi.​neuropsych.​11070170 CrossRefPubMed
go back to reference Charara A, Heilman TC, Levey AI, Smith Y (2000) Pre- and postsynaptic localization of GABA(B) receptors in the basal ganglia in monkeys. Neuroscience 95(1):127–140CrossRefPubMed Charara A, Heilman TC, Levey AI, Smith Y (2000) Pre- and postsynaptic localization of GABA(B) receptors in the basal ganglia in monkeys. Neuroscience 95(1):127–140CrossRefPubMed
go back to reference Chen CC, Pogosyan A, Zrinzo LU, Tisch S, Limousin P, Ashkan K, Yousry T, Hariz MI, Brown P (2006) Intra-operative recordings of local field potentials can help localize the subthalamic nucleus in Parkinson’s disease surgery. Exp Neurol 198(1):214–221. doi:10.1016/j.expneurol.2005.11.019 CrossRefPubMed Chen CC, Pogosyan A, Zrinzo LU, Tisch S, Limousin P, Ashkan K, Yousry T, Hariz MI, Brown P (2006) Intra-operative recordings of local field potentials can help localize the subthalamic nucleus in Parkinson’s disease surgery. Exp Neurol 198(1):214–221. doi:10.​1016/​j.​expneurol.​2005.​11.​019 CrossRefPubMed
go back to reference 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):579–596CrossRefPubMed 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):579–596CrossRefPubMed
go back to reference de Hollander G, Keuken MC, Bazin PL, Weiss M, Neumann J, Reimann K, Wahnert M, Turner R, Forstmann BU, Schafer A (2014) A gradual increase of iron toward the medial-inferior tip of the subthalamic nucleus. Hum Brain Mapp. doi:10.1002/hbm.22485 PubMed de Hollander G, Keuken MC, Bazin PL, Weiss M, Neumann J, Reimann K, Wahnert M, Turner R, Forstmann BU, Schafer A (2014) A gradual increase of iron toward the medial-inferior tip of the subthalamic nucleus. Hum Brain Mapp. doi:10.​1002/​hbm.​22485 PubMed
go back to reference Doshi PK, Chhaya N, Bhatt MH (2002) Depression leading to attempted suicide after bilateral subthalamic nucleus stimulation for Parkinson’s disease. Mov Disord 17(5):1084–1085. doi:10.1002/mds.10198 CrossRefPubMed Doshi PK, Chhaya N, Bhatt MH (2002) Depression leading to attempted suicide after bilateral subthalamic nucleus stimulation for Parkinson’s disease. Mov Disord 17(5):1084–1085. doi:10.​1002/​mds.​10198 CrossRefPubMed
go back to reference Eagle DM, Baunez C, Hutcheson DM, Lehmann O, Shah AP, Robbins TW (2008) Stop-signal reaction-time task performance: role of prefrontal cortex and subthalamic nucleus. Cereb Cortex 18(1):178–188. doi:10.1093/cercor/bhm044 CrossRefPubMed Eagle DM, Baunez C, Hutcheson DM, Lehmann O, Shah AP, Robbins TW (2008) Stop-signal reaction-time task performance: role of prefrontal cortex and subthalamic nucleus. Cereb Cortex 18(1):178–188. doi:10.​1093/​cercor/​bhm044 CrossRefPubMed
go back to reference Fogelson N, Williams D, Tijssen M, van Bruggen G, Speelman H, Brown P (2006) Different functional loops between cerebral cortex and the subthalmic area in Parkinson’s disease. Cereb Cortex 16(1):64–75. doi:10.1093/cercor/bhi084 CrossRefPubMed Fogelson N, Williams D, Tijssen M, van Bruggen G, Speelman H, Brown P (2006) Different functional loops between cerebral cortex and the subthalmic area in Parkinson’s disease. Cereb Cortex 16(1):64–75. doi:10.​1093/​cercor/​bhi084 CrossRefPubMed
go back to reference Fontaine D, Mattei V, Borg M, von Langsdorff D, Magnie MN, Chanalet S, Robert P, Paquis P (2004) Effect of subthalamic nucleus stimulation on obsessive-compulsive disorder in a patient with Parkinson disease. Case report. J Neurosurg 100(6):1084–1086. doi:10.3171/jns.2004.100.6.1084 CrossRefPubMed Fontaine D, Mattei V, Borg M, von Langsdorff D, Magnie MN, Chanalet S, Robert P, Paquis P (2004) Effect of subthalamic nucleus stimulation on obsessive-compulsive disorder in a patient with Parkinson disease. Case report. J Neurosurg 100(6):1084–1086. doi:10.​3171/​jns.​2004.​100.​6.​1084 CrossRefPubMed
go back to reference Haber SN (2003) The primate basal ganglia: parallel and integrative networks. J Chem Neuroanat 26(4):317–330CrossRefPubMed Haber SN (2003) The primate basal ganglia: parallel and integrative networks. J Chem Neuroanat 26(4):317–330CrossRefPubMed
go back to reference Hedreen JC (1999) Tyrosine hydroxylase-immunoreactive elements in the human globus pallidus and subthalamic nucleus. J Comp Neurol 409(3):400–410CrossRefPubMed Hedreen JC (1999) Tyrosine hydroxylase-immunoreactive elements in the human globus pallidus and subthalamic nucleus. J Comp Neurol 409(3):400–410CrossRefPubMed
go back to reference Hirschmann J, Ozkurt TE, Butz M, Homburger M, Elben S, Hartmann CJ, Vesper J, Wojtecki L, Schnitzler A (2011) Distinct oscillatory STN-cortical loops revealed by simultaneous MEG and local field potential recordings in patients with Parkinson’s disease. Neuroimage 55(3):1159–1168. doi:10.1016/j.neuroimage.2010.11.063 CrossRefPubMed Hirschmann J, Ozkurt TE, Butz M, Homburger M, Elben S, Hartmann CJ, Vesper J, Wojtecki L, Schnitzler A (2011) Distinct oscillatory STN-cortical loops revealed by simultaneous MEG and local field potential recordings in patients with Parkinson’s disease. Neuroimage 55(3):1159–1168. doi:10.​1016/​j.​neuroimage.​2010.​11.​063 CrossRefPubMed
go back to reference Hirunsatit R, George ED, Lipska BK, Elwafi HM, Sander L, Yrigollen CM, Gelernter J, Grigorenko EL, Lappalainen J, Mane S, Nairn AC, Kleinman JE, Simen AA (2009) Twenty-one-base-pair insertion polymorphism creates an enhancer element and potentiates SLC6A1 GABA transporter promoter activity. Pharmacogenet Genomics 19(1):53–65. doi:10.1097/FPC.0b013e328318b21a PubMedCentralCrossRefPubMed Hirunsatit R, George ED, Lipska BK, Elwafi HM, Sander L, Yrigollen CM, Gelernter J, Grigorenko EL, Lappalainen J, Mane S, Nairn AC, Kleinman JE, Simen AA (2009) Twenty-one-base-pair insertion polymorphism creates an enhancer element and potentiates SLC6A1 GABA transporter promoter activity. Pharmacogenet Genomics 19(1):53–65. doi:10.​1097/​FPC.​0b013e328318b21a​ PubMedCentralCrossRefPubMed
go back to reference Houeto JL, Mallet L, Mesnage V, Tezenas du Montcel S, Behar C, Gargiulo M, Torny F, Pelissolo A, Welter ML, Agid Y (2006) Subthalamic stimulation in Parkinson disease: behavior and social adaptation. Arch Neurol 63(8):1090–1095. doi:10.1001/archneur.63.8.1090 CrossRefPubMed Houeto JL, Mallet L, Mesnage V, Tezenas du Montcel S, Behar C, Gargiulo M, Torny F, Pelissolo A, Welter ML, Agid Y (2006) Subthalamic stimulation in Parkinson disease: behavior and social adaptation. Arch Neurol 63(8):1090–1095. doi:10.​1001/​archneur.​63.​8.​1090 CrossRefPubMed
go back to reference Hurd YL, Suzuki M, Sedvall GC (2001) D1 and D2 dopamine receptor mRNA expression in whole hemisphere sections of the human brain. J Chem Neuroanat 22(1–2):127–137CrossRefPubMed Hurd YL, Suzuki M, Sedvall GC (2001) D1 and D2 dopamine receptor mRNA expression in whole hemisphere sections of the human brain. J Chem Neuroanat 22(1–2):127–137CrossRefPubMed
go back to reference Jahanshahi M, Ardouin CM, Brown RG, Rothwell JC, Obeso J, Albanese A, Rodriguez-Oroz MC, Moro E, Benabid AL, Pollak P, Limousin-Dowsey P (2000) The impact of deep brain stimulation on executive function in Parkinson’s disease. Brain 123(Pt 6):1142–1154CrossRefPubMed Jahanshahi M, Ardouin CM, Brown RG, Rothwell JC, Obeso J, Albanese A, Rodriguez-Oroz MC, Moro E, Benabid AL, Pollak P, Limousin-Dowsey P (2000) The impact of deep brain stimulation on executive function in Parkinson’s disease. Brain 123(Pt 6):1142–1154CrossRefPubMed
go back to reference Joel D, Weiner I (1997) The connections of the primate subthalamic nucleus: indirect pathways and the open-interconnected scheme of basal ganglia-thalamocortical circuitry. Brain Res Brain Res Rev 23(1–2):62–78CrossRefPubMed Joel D, Weiner I (1997) The connections of the primate subthalamic nucleus: indirect pathways and the open-interconnected scheme of basal ganglia-thalamocortical circuitry. Brain Res Brain Res Rev 23(1–2):62–78CrossRefPubMed
go back to reference Krack P, Poepping M, Weinert D, Schrader B, Deuschl G (2000) Thalamic, pallidal, or subthalamic surgery for Parkinson’s disease? J Neurol 247(Suppl 2:II):122–134 Krack P, Poepping M, Weinert D, Schrader B, Deuschl G (2000) Thalamic, pallidal, or subthalamic surgery for Parkinson’s disease? J Neurol 247(Suppl 2:II):122–134
go back to reference Kultas-Ilinsky K, Leontiev V, Whiting PJ (1998) Expression of 10 GABA(A) receptor subunit messenger RNAs in the motor-related thalamic nuclei and basal ganglia of Macaca mulatta studied with in situ hybridization histochemistry. Neuroscience 85(1):179–204CrossRefPubMed Kultas-Ilinsky K, Leontiev V, Whiting PJ (1998) Expression of 10 GABA(A) receptor subunit messenger RNAs in the motor-related thalamic nuclei and basal ganglia of Macaca mulatta studied with in situ hybridization histochemistry. Neuroscience 85(1):179–204CrossRefPubMed
go back to reference Kumar R, Lozano AM, Kim YJ, Hutchison WD, Sime E, Halket E, Lang AE (1998) Double-blind evaluation of subthalamic nucleus deep brain stimulation in advanced Parkinson’s disease. Neurology 51(3):850–855CrossRefPubMed Kumar R, Lozano AM, Kim YJ, Hutchison WD, Sime E, Halket E, Lang AE (1998) Double-blind evaluation of subthalamic nucleus deep brain stimulation in advanced Parkinson’s disease. Neurology 51(3):850–855CrossRefPubMed
go back to reference Kuwajima M, Hall RA, Aiba A, Smith Y (2004) Subcellular and subsynaptic localization of group I metabotropic glutamate receptors in the monkey subthalamic nucleus. J Comp Neurol 474(4):589–602. doi:10.1002/cne.20158 CrossRefPubMed Kuwajima M, Hall RA, Aiba A, Smith Y (2004) Subcellular and subsynaptic localization of group I metabotropic glutamate receptors in the monkey subthalamic nucleus. J Comp Neurol 474(4):589–602. doi:10.​1002/​cne.​20158 CrossRefPubMed
go back to reference 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. doi:10.1016/j.neuroimage.2015.01.038 PubMed 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. doi:10.​1016/​j.​neuroimage.​2015.​01.​038 PubMed
go back to reference Limousin P, Pollak P, Benazzouz A, Hoffmann D, Le Bas JF, Broussolle E, Perret JE, Benabid AL (1995) Effect of parkinsonian signs and symptoms of bilateral subthalamic nucleus stimulation. Lancet 345(8942):91–95CrossRefPubMed Limousin P, Pollak P, Benazzouz A, Hoffmann D, Le Bas JF, Broussolle E, Perret JE, Benabid AL (1995) Effect of parkinsonian signs and symptoms of bilateral subthalamic nucleus stimulation. Lancet 345(8942):91–95CrossRefPubMed
go back to reference Mallet L, Schupbach 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. doi:10.1073/pnas.0610849104 PubMedCentralCrossRefPubMed Mallet L, Schupbach 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. doi:10.​1073/​pnas.​0610849104 PubMedCentralCrossRefPubMed
go back to reference Mallet L, Polosan M, Jaafari N, Baup N, Welter ML, Fontaine D, du Montcel ST, Yelnik J, Chereau I, Arbus C, Raoul S, Aouizerate B, Damier P, Chabardes 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, Verin M, Houeto JL, Pollak P, Benabid AL, Agid Y, Krack P, Millet B, Pelissolo A, Group SS (2008) Subthalamic nucleus stimulation in severe obsessive-compulsive disorder. N Engl J Med 359(20):2121–2134. doi:10.1056/NEJMoa0708514 CrossRefPubMed Mallet L, Polosan M, Jaafari N, Baup N, Welter ML, Fontaine D, du Montcel ST, Yelnik J, Chereau I, Arbus C, Raoul S, Aouizerate B, Damier P, Chabardes 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, Verin M, Houeto JL, Pollak P, Benabid AL, Agid Y, Krack P, Millet B, Pelissolo A, Group SS (2008) Subthalamic nucleus stimulation in severe obsessive-compulsive disorder. N Engl J Med 359(20):2121–2134. doi:10.​1056/​NEJMoa0708514 CrossRefPubMed
go back to reference Mori S, Takino T, Yamada H, Sano Y (1985) Immunohistochemical demonstration of serotonin nerve fibers in the subthalamic nucleus of the rat, cat and monkey. Neurosci Lett 62(3):305–309CrossRefPubMed Mori S, Takino T, Yamada H, Sano Y (1985) Immunohistochemical demonstration of serotonin nerve fibers in the subthalamic nucleus of the rat, cat and monkey. Neurosci Lett 62(3):305–309CrossRefPubMed
go back to reference Odekerken VJ, van Laar T, Staal MJ, Mosch A, Hoffmann CF, Nijssen PC, Beute GN, van Vugt JP, Lenders MW, Contarino MF, Mink MS, Bour LJ, van den Munckhof P, Schmand BA, de Haan RJ, Schuurman PR, de Bie RM (2013) Subthalamic nucleus versus globus pallidus bilateral deep brain stimulation for advanced Parkinson’s disease (NSTAPS study): a randomised controlled trial. Lancet Neurol 12(1):37–44. doi:10.1016/S1474-4422(12)70264-8 CrossRefPubMed Odekerken VJ, van Laar T, Staal MJ, Mosch A, Hoffmann CF, Nijssen PC, Beute GN, van Vugt JP, Lenders MW, Contarino MF, Mink MS, Bour LJ, van den Munckhof P, Schmand BA, de Haan RJ, Schuurman PR, de Bie RM (2013) Subthalamic nucleus versus globus pallidus bilateral deep brain stimulation for advanced Parkinson’s disease (NSTAPS study): a randomised controlled trial. Lancet Neurol 12(1):37–44. doi:10.​1016/​S1474-4422(12)70264-8 CrossRefPubMed
go back to reference Parent A, Hazrati LN (1995a) Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop. Brain research. Brain Res Rev 20(1):91–127CrossRefPubMed Parent A, Hazrati LN (1995a) Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop. Brain research. Brain Res Rev 20(1):91–127CrossRefPubMed
go back to reference Parent A, Hazrati LN (1995b) Functional anatomy of the basal ganglia. II. The place of subthalamic nucleus and external pallidum in basal ganglia circuitry. Brain research. Brain Res Rev 20(1):128–154CrossRefPubMed Parent A, Hazrati LN (1995b) Functional anatomy of the basal ganglia. II. The place of subthalamic nucleus and external pallidum in basal ganglia circuitry. Brain research. Brain Res Rev 20(1):128–154CrossRefPubMed
go back to reference Parent A, Fortin M, Cote PY, Cicchetti F (1996) Calcium-binding proteins in primate basal ganglia. Neurosci Res 25(4):309–334CrossRefPubMed Parent A, Fortin M, Cote PY, Cicchetti F (1996) Calcium-binding proteins in primate basal ganglia. Neurosci Res 25(4):309–334CrossRefPubMed
go back to reference Polanski WH, Martin KD, Engellandt K, von Kummer R, Klingelhoefer L, Fauser M, Storch A, Schackert G, Sobottka SB (2015) Accuracy of subthalamic nucleus targeting by T2, FLAIR and SWI-3-Tesla MRI confirmed by microelectrode recordings. Acta Neurochir (Wien) 157(3):479–486. doi:10.1007/s00701-014-2328-x CrossRef Polanski WH, Martin KD, Engellandt K, von Kummer R, Klingelhoefer L, Fauser M, Storch A, Schackert G, Sobottka SB (2015) Accuracy of subthalamic nucleus targeting by T2, FLAIR and SWI-3-Tesla MRI confirmed by microelectrode recordings. Acta Neurochir (Wien) 157(3):479–486. doi:10.​1007/​s00701-014-2328-x CrossRef
go back to reference Raynor K, Kong H, Mestek A, Bye LS, Tian M, Liu J, Yu L, Reisine T (1995) Characterization of the cloned human mu opioid receptor. J Pharmacol Exp Ther 272(1):423–428PubMed Raynor K, Kong H, Mestek A, Bye LS, Tian M, Liu J, Yu L, Reisine T (1995) Characterization of the cloned human mu opioid receptor. J Pharmacol Exp Ther 272(1):423–428PubMed
go back to reference Reck C, Himmel M, Florin E, Maarouf M, Sturm V, Wojtecki L, Schnitzler A, Fink GR, Timmermann L (2010) Coherence analysis of local field potentials in the subthalamic nucleus: differences in parkinsonian rest and postural tremor. Eur J Neurosci 32(7):1202–1214. doi:10.1111/j.1460-9568.2010.07362.x CrossRefPubMed Reck C, Himmel M, Florin E, Maarouf M, Sturm V, Wojtecki L, Schnitzler A, Fink GR, Timmermann L (2010) Coherence analysis of local field potentials in the subthalamic nucleus: differences in parkinsonian rest and postural tremor. Eur J Neurosci 32(7):1202–1214. doi:10.​1111/​j.​1460-9568.​2010.​07362.​x CrossRefPubMed
go back to reference Rodriguez-Oroz MC, Rodriguez M, Guridi J, Mewes K, Chockkman V, Vitek J, DeLong MR, Obeso JA (2001) The subthalamic nucleus in Parkinson’s disease: somatotopic organization and physiological characteristics. Brain 124(Pt 9):1777–1790CrossRefPubMed Rodriguez-Oroz MC, Rodriguez M, Guridi J, Mewes K, Chockkman V, Vitek J, DeLong MR, Obeso JA (2001) The subthalamic nucleus in Parkinson’s disease: somatotopic organization and physiological characteristics. Brain 124(Pt 9):1777–1790CrossRefPubMed
go back to reference Rodriguez-Oroz MC, Zamarbide I, Guridi J, Palmero MR, Obeso JA (2004) Efficacy of deep brain stimulation of the subthalamic nucleus in Parkinson’s disease 4 years after surgery: double blind and open label evaluation. J Neurol Neurosurg Psychiatry 75(10):1382–1385. doi:10.1136/jnnp.2003.031294 PubMedCentralCrossRefPubMed Rodriguez-Oroz MC, Zamarbide I, Guridi J, Palmero MR, Obeso JA (2004) Efficacy of deep brain stimulation of the subthalamic nucleus in Parkinson’s disease 4 years after surgery: double blind and open label evaluation. J Neurol Neurosurg Psychiatry 75(10):1382–1385. doi:10.​1136/​jnnp.​2003.​031294 PubMedCentralCrossRefPubMed
go back to reference Smith Y, Parent A (1988) Neurons of the subthalamic nucleus in primates display glutamate but not GABA immunoreactivity. Brain Res 453(1–2):353–356PubMed Smith Y, Parent A (1988) Neurons of the subthalamic nucleus in primates display glutamate but not GABA immunoreactivity. Brain Res 453(1–2):353–356PubMed
go back to reference Temel Y, Boothman LJ, Blokland A, Magill PJ, Steinbusch HW, Visser-Vandewalle V, Sharp T (2007) Inhibition of 5-HT neuron activity and induction of depressive-like behavior by high-frequency stimulation of the subthalamic nucleus. Proc Natl Acad Sci USA 104(43):17087–17092. doi:10.1073/pnas.0704144104 PubMedCentralCrossRefPubMed Temel Y, Boothman LJ, Blokland A, Magill PJ, Steinbusch HW, Visser-Vandewalle V, Sharp T (2007) Inhibition of 5-HT neuron activity and induction of depressive-like behavior by high-frequency stimulation of the subthalamic nucleus. Proc Natl Acad Sci USA 104(43):17087–17092. doi:10.​1073/​pnas.​0704144104 PubMedCentralCrossRefPubMed
go back to reference Thobois S, Mertens P, Guenot M, Hermier M, Mollion H, Bouvard M, Chazot G, Broussolle E, Sindou M (2002) Subthalamic nucleus stimulation in Parkinson’s disease: clinical evaluation of 18 patients. J Neurol 249(5):529–534. doi:10.1007/s004150200059 CrossRefPubMed Thobois S, Mertens P, Guenot M, Hermier M, Mollion H, Bouvard M, Chazot G, Broussolle E, Sindou M (2002) Subthalamic nucleus stimulation in Parkinson’s disease: clinical evaluation of 18 patients. J Neurol 249(5):529–534. doi:10.​1007/​s004150200059 CrossRefPubMed
go back to reference Turner R (2012) Neuroscientific applications of high-field MRI in humans. In: Hennig J, Speck O (eds) High-field MR imaging. Medical radiology. Springer, Berlin, pp 137–149. doi:10.1007/174_2010_103 CrossRef Turner R (2012) Neuroscientific applications of high-field MRI in humans. In: Hennig J, Speck O (eds) High-field MR imaging. Medical radiology. Springer, Berlin, pp 137–149. doi:10.​1007/​174_​2010_​103 CrossRef
go back to reference Visser-Vandewalle V, van der Linden C, Temel Y, Celik H, Ackermans L, Spincemaille G, Caemaert J (2005) Long-term effects of bilateral subthalamic nucleus stimulation in advanced Parkinson disease: a four year follow-up study. Parkinsonism Relat Disord 11(3):157–165. doi:10.1016/j.parkreldis.2004.10.011 CrossRefPubMed Visser-Vandewalle V, van der Linden C, Temel Y, Celik H, Ackermans L, Spincemaille G, Caemaert J (2005) Long-term effects of bilateral subthalamic nucleus stimulation in advanced Parkinson disease: a four year follow-up study. Parkinsonism Relat Disord 11(3):157–165. doi:10.​1016/​j.​parkreldis.​2004.​10.​011 CrossRefPubMed
go back to reference Volkmann J, Allert N, Voges J, Weiss PH, Freund HJ, Sturm V (2001) Safety and efficacy of pallidal or subthalamic nucleus stimulation in advanced PD. Neurology 56(4):548–551CrossRefPubMed Volkmann J, Allert N, Voges J, Weiss PH, Freund HJ, Sturm V (2001) Safety and efficacy of pallidal or subthalamic nucleus stimulation in advanced PD. Neurology 56(4):548–551CrossRefPubMed
go back to reference Weinberger M, Hutchison WD, Lozano AM, Hodaie M, Dostrovsky JO (2009) Increased gamma oscillatory activity in the subthalamic nucleus during tremor in Parkinson’s disease patients. J Neurophysiol 101(2):789–802. doi:10.1152/jn.90837.2008 CrossRefPubMed Weinberger M, Hutchison WD, Lozano AM, Hodaie M, Dostrovsky JO (2009) Increased gamma oscillatory activity in the subthalamic nucleus during tremor in Parkinson’s disease patients. J Neurophysiol 101(2):789–802. doi:10.​1152/​jn.​90837.​2008 CrossRefPubMed
go back to reference Weintraub D, Duda JE, Carlson K, Luo P, Sagher O, Stern M, Follett KA, Reda D, Weaver FM (2013) Suicide ideation and behaviours after STN and GPi DBS surgery for Parkinson’s disease: results from a randomised, controlled trial. J Neurol Neurosurg Psychiatry 84(10):1113–1118. doi:10.1136/jnnp-2012-304396 CrossRefPubMed Weintraub D, Duda JE, Carlson K, Luo P, Sagher O, Stern M, Follett KA, Reda D, Weaver FM (2013) Suicide ideation and behaviours after STN and GPi DBS surgery for Parkinson’s disease: results from a randomised, controlled trial. J Neurol Neurosurg Psychiatry 84(10):1113–1118. doi:10.​1136/​jnnp-2012-304396 CrossRefPubMed
go back to reference Welter ML, Burbaud P, Fernandez-Vidal S, Bardinet E, Coste J, Piallat B, Borg M, Besnard S, Sauleau P, Devaux B, Pidoux B, Chaynes P, Tezenas du Montcel S, Bastian A, Langbour N, Teillant A, Haynes W, Yelnik J, Karachi C, Mallet L, French Stimulation dans Trouble Obsessionnel Compulsif Study G (2011) Basal ganglia dysfunction in OCD: subthalamic neuronal activity correlates with symptoms severity and predicts high-frequency stimulation efficacy. Transl Psychiatry 1:e5. doi:10.1038/tp.2011.5 PubMedCentralCrossRefPubMed Welter ML, Burbaud P, Fernandez-Vidal S, Bardinet E, Coste J, Piallat B, Borg M, Besnard S, Sauleau P, Devaux B, Pidoux B, Chaynes P, Tezenas du Montcel S, Bastian A, Langbour N, Teillant A, Haynes W, Yelnik J, Karachi C, Mallet L, French Stimulation dans Trouble Obsessionnel Compulsif Study G (2011) Basal ganglia dysfunction in OCD: subthalamic neuronal activity correlates with symptoms severity and predicts high-frequency stimulation efficacy. Transl Psychiatry 1:e5. doi:10.​1038/​tp.​2011.​5 PubMedCentralCrossRefPubMed
Metadata
Title
Topographic organization of the human and non-human primate subthalamic nucleus
Authors
Anneke Alkemade
Alfons Schnitzler
Birte U. Forstmann
Publication date
01-11-2015
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 6/2015
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-015-1047-2

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