Skip to main content
Top
Published in: Brain Structure and Function 6/2015

01-11-2015 | Original Article

Stimulation of the subthalamic nucleus engages the cerebellum for motor function in parkinsonian rats

Authors: Alexander C. Sutton, Katherine A. O’Connor, Julie G. Pilitsis, Damian S. Shin

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

Login to get access

Abstract

Deep brain stimulation (DBS) is effective in managing motor symptoms of Parkinson’s disease in well-selected individuals. Recently, research has shown that DBS in the basal ganglia (BG) can alter neural circuits beyond the traditional basal ganglia-thalamus-cortical (BG-TH-CX) loop. For instance, functional imaging showed alterations in cerebellar activity with DBS in the subthalamic nucleus (STN). However, these imaging studies revealed very little about how cell-specific cerebellar activity responds to STN stimulation or if these changes contribute to its efficacy. In this study, we assess whether STN-DBS provides efficacy in managing motor symptoms in Parkinson’s disease by recruiting cerebellar activity. We do this by applying STN-DBS in hemiparkinsonian rats and simultaneously recording neuronal activity from the STN, brainstem and cerebellum. We found that STN neurons decreased spiking activity by 55 % during DBS (P = 0.038), which coincided with a decrease in most pedunculopontine tegmental nucleus and Purkinje neurons by 29 % (P < 0.001) and 28 % (P = 0.003), respectively. In contrast, spike activity in the deep cerebellar nuclei increased 45 % during DBS (P < 0.001), which was likely from reduced afferent activity of Purkinje cells. Then, we applied STN-DBS at sub-therapeutic current along with stimulation of the deep cerebellar nuclei and found similar improvement in forelimb akinesia as with therapeutic STN-DBS alone. This suggests that STN-DBS can engage cerebellar activity to improve parkinsonian motor symptoms. Our study is the first to describe how STN-DBS in Parkinson’s disease alters cerebellar activity using electrophysiology in vivo and reveal a potential for stimulating the cerebellum to potentiate deep brain stimulation of the subthalamic nucleus.
Appendix
Available only for authorised users
Literature
go back to reference Allen GI, Tsukahara N (1974) Cerebrocerebellar communication systems. Physiol Rev 54:957–1006PubMed Allen GI, Tsukahara N (1974) Cerebrocerebellar communication systems. Physiol Rev 54:957–1006PubMed
go back to reference Allen GI, Azzena GB, Ohno T (1974) Somatotopically organized inputs from fore- and hindlimb areas of sensorimotor cortex to cerebellar Purkyne cells. Exp Brain Res 20:255–272PubMed Allen GI, Azzena GB, Ohno T (1974) Somatotopically organized inputs from fore- and hindlimb areas of sensorimotor cortex to cerebellar Purkyne cells. Exp Brain Res 20:255–272PubMed
go back to reference Azulay JP, Mesure S, Amblard B, Blin O, Sangla I, Pouget J (1999) Visual control of locomotion in Parkinson’s disease. Brain 122(Pt 1):111–120PubMedCrossRef Azulay JP, Mesure S, Amblard B, Blin O, Sangla I, Pouget J (1999) Visual control of locomotion in Parkinson’s disease. Brain 122(Pt 1):111–120PubMedCrossRef
go back to reference Ballanger B et al (2009) Cerebral blood flow changes induced by pedunculopontine nucleus stimulation in patients with advanced Parkinson’s disease: a [(15)O] H2O PET study. Hum Brain Mapp 30:3901–3909. doi:10.1002/hbm.20815 PubMedCrossRef Ballanger B et al (2009) Cerebral blood flow changes induced by pedunculopontine nucleus stimulation in patients with advanced Parkinson’s disease: a [(15)O] H2O PET study. Hum Brain Mapp 30:3901–3909. doi:10.​1002/​hbm.​20815 PubMedCrossRef
go back to reference Bastian AJ, Martin TA, Keating JG, Thach WT (1996) Cerebellar ataxia: abnormal control of interaction torques across multiple joints. J Neurophysiol 76:492–509PubMed Bastian AJ, Martin TA, Keating JG, Thach WT (1996) Cerebellar ataxia: abnormal control of interaction torques across multiple joints. J Neurophysiol 76:492–509PubMed
go back to reference Breit S, Martin A, Lessmann L, Cerkez D, Gasser T, Schulz JB (2008) Bilateral changes in neuronal activity of the basal ganglia in the unilateral 6-hydroxydopamine rat model. J Neurosci Res 86:1388–1396. doi:10.1002/jnr.21588 PubMedCrossRef Breit S, Martin A, Lessmann L, Cerkez D, Gasser T, Schulz JB (2008) Bilateral changes in neuronal activity of the basal ganglia in the unilateral 6-hydroxydopamine rat model. J Neurosci Res 86:1388–1396. doi:10.​1002/​jnr.​21588 PubMedCrossRef
go back to reference Canedo A (1997) Primary motor cortex influences on the descending and ascending systems. Prog Neurobiol 51:287–335PubMedCrossRef Canedo A (1997) Primary motor cortex influences on the descending and ascending systems. Prog Neurobiol 51:287–335PubMedCrossRef
go back to reference Cicirata F, Angaut P, Serapide MF, Panto MR, Nicotra G (1992) Multiple representation in the nucleus lateralis of the cerebellum: an electrophysiologic study in the rat. Exp Brain Res 89:352–362PubMedCrossRef Cicirata F, Angaut P, Serapide MF, Panto MR, Nicotra G (1992) Multiple representation in the nucleus lateralis of the cerebellum: an electrophysiologic study in the rat. Exp Brain Res 89:352–362PubMedCrossRef
go back to reference Coltz JD, Johnson MT, Ebner TJ (1999) Cerebellar Purkinje cell simple spike discharge encodes movement velocity in primates during visuomotor arm tracking. J Neurosci 19:1782–1803PubMed Coltz JD, Johnson MT, Ebner TJ (1999) Cerebellar Purkinje cell simple spike discharge encodes movement velocity in primates during visuomotor arm tracking. J Neurosci 19:1782–1803PubMed
go back to reference Do MT, Bean BP (2003) Subthreshold sodium currents and pacemaking of subthalamic neurons: modulation by slow inactivation. Neuron 39:109–120PubMedCrossRef Do MT, Bean BP (2003) Subthreshold sodium currents and pacemaking of subthalamic neurons: modulation by slow inactivation. Neuron 39:109–120PubMedCrossRef
go back to reference Doya K (2000) Complementary roles of basal ganglia and cerebellum in learning and motor control. Curr Opin Neurobiol 10:732–739. pii: S0959-4388(00)00153-7PubMedCrossRef Doya K (2000) Complementary roles of basal ganglia and cerebellum in learning and motor control. Curr Opin Neurobiol 10:732–739. pii: S0959-4388(00)00153-7PubMedCrossRef
go back to reference Eccles JC, Sabah NH, Schmidt RF, Taborikova H (1972) Integration by Purkyne cells of mossy and climbing fiber inputs from cutaneous mechanoreceptors. Exp Brain Res 15:498–520PubMedCrossRef Eccles JC, Sabah NH, Schmidt RF, Taborikova H (1972) Integration by Purkyne cells of mossy and climbing fiber inputs from cutaneous mechanoreceptors. Exp Brain Res 15:498–520PubMedCrossRef
go back to reference Freeman JS, Cody FW, Schady W (1993) The influence of external timing cues upon the rhythm of voluntary movements in Parkinson’s disease. J Neurol Neurosurg Psychiatry 56:1078–1084PubMedCentralPubMedCrossRef Freeman JS, Cody FW, Schady W (1993) The influence of external timing cues upon the rhythm of voluntary movements in Parkinson’s disease. J Neurol Neurosurg Psychiatry 56:1078–1084PubMedCentralPubMedCrossRef
go back to reference Fu QG, Flament D, Coltz JD, Ebner TJ (1997) Relationship of cerebellar Purkinje cell simple spike discharge to movement kinematics in the monkey. J Neurophysiol 78:478–491PubMed Fu QG, Flament D, Coltz JD, Ebner TJ (1997) Relationship of cerebellar Purkinje cell simple spike discharge to movement kinematics in the monkey. J Neurophysiol 78:478–491PubMed
go back to reference Georgiou N, Iansek R, Bradshaw JL, Phillips JG, Mattingley JB, Bradshaw JA (1993) An evaluation of the role of internal cues in the pathogenesis of parkinsonian hypokinesia. Brain 116(Pt 6):1575–1587PubMedCrossRef Georgiou N, Iansek R, Bradshaw JL, Phillips JG, Mattingley JB, Bradshaw JA (1993) An evaluation of the role of internal cues in the pathogenesis of parkinsonian hypokinesia. Brain 116(Pt 6):1575–1587PubMedCrossRef
go back to reference Grant G (1962) Spinal course and somatotopically localized termination of the spinocerebellar tracts. An experimental study in the cat. Acta Physiol Scand Suppl 56:1–61PubMedCrossRef Grant G (1962) Spinal course and somatotopically localized termination of the spinocerebellar tracts. An experimental study in the cat. Acta Physiol Scand Suppl 56:1–61PubMedCrossRef
go back to reference Grodd W, Hulsmann E, Lotze M, Wildgruber D, Erb M (2001) Sensorimotor mapping of the human cerebellum: fMRI evidence of somatotopic organization. Hum Brain Mapp 13:55–73PubMedCrossRef Grodd W, Hulsmann E, Lotze M, Wildgruber D, Erb M (2001) Sensorimotor mapping of the human cerebellum: fMRI evidence of somatotopic organization. Hum Brain Mapp 13:55–73PubMedCrossRef
go back to reference Gubellini P, Eusebio A, Oueslati A, Melon C, Kerkerian-Le Goff L, Salin P (2006) Chronic high-frequency stimulation of the subthalamic nucleus and L-DOPA treatment in experimental parkinsonism: effects on motor behaviour and striatal glutamate transmission. Eur J Neurosci 24:1802–1814. doi:10.1111/j.1460-9568.2006.05047.x EJN5047PubMedCrossRef Gubellini P, Eusebio A, Oueslati A, Melon C, Kerkerian-Le Goff L, Salin P (2006) Chronic high-frequency stimulation of the subthalamic nucleus and L-DOPA treatment in experimental parkinsonism: effects on motor behaviour and striatal glutamate transmission. Eur J Neurosci 24:1802–1814. doi:10.​1111/​j.​1460-9568.​2006.​05047.​x EJN5047PubMedCrossRef
go back to reference Hammond C, Rouzaire-Dubois B, Feger J, Jackson A, Crossman AR (1983) Anatomical and electrophysiological studies on the reciprocal projections between the subthalamic nucleus and nucleus tegmenti pedunculopontinus in the rat. Neuroscience 9:41–52. pii: S0306-4522(83)90045-3PubMedCrossRef Hammond C, Rouzaire-Dubois B, Feger J, Jackson A, Crossman AR (1983) Anatomical and electrophysiological studies on the reciprocal projections between the subthalamic nucleus and nucleus tegmenti pedunculopontinus in the rat. Neuroscience 9:41–52. pii: S0306-4522(83)90045-3PubMedCrossRef
go back to reference Hudson JL et al (1993) Correlation of apomorphine- and amphetamine-induced turning with nigrostriatal dopamine content in unilateral 6-hydroxydopamine lesioned rats. Brain Res 626:167–174. pii: S0006-8993(93)90576-9PubMedCrossRef Hudson JL et al (1993) Correlation of apomorphine- and amphetamine-induced turning with nigrostriatal dopamine content in unilateral 6-hydroxydopamine lesioned rats. Brain Res 626:167–174. pii: S0006-8993(93)90576-9PubMedCrossRef
go back to reference Ichinohe N, Teng B, Kitai ST (2000) Morphological study of the tegmental pedunculopontine nucleus, substantia nigra and subthalamic nucleus, and their interconnections in rat organotypic culture. Anat Embryol 201:435–453PubMedCrossRef Ichinohe N, Teng B, Kitai ST (2000) Morphological study of the tegmental pedunculopontine nucleus, substantia nigra and subthalamic nucleus, and their interconnections in rat organotypic culture. Anat Embryol 201:435–453PubMedCrossRef
go back to reference Ito M, Yoshida M, Obata K, Kawai N, Udo M (1970) Inhibitory control of intracerebellar nuclei by the Purkinje cell axons. Exp Brain Res 10:64–80PubMedCrossRef Ito M, Yoshida M, Obata K, Kawai N, Udo M (1970) Inhibitory control of intracerebellar nuclei by the Purkinje cell axons. Exp Brain Res 10:64–80PubMedCrossRef
go back to reference Jackson A, Crossman AR (1983) Nucleus tegmenti pedunculopontinus: efferent connections with special reference to the basal ganglia, studied in the rat by anterograde and retrograde transport of horseradish peroxidase. Neuroscience 10:725–765PubMedCrossRef Jackson A, Crossman AR (1983) Nucleus tegmenti pedunculopontinus: efferent connections with special reference to the basal ganglia, studied in the rat by anterograde and retrograde transport of horseradish peroxidase. Neuroscience 10:725–765PubMedCrossRef
go back to reference Jahanshahi M, Jenkins IH, Brown RG, Marsden CD, Passingham RE, Brooks DJ (1995) Self-initiated versus externally triggered movements. I. An investigation using measurement of regional cerebral blood flow with PET and movement-related potentials in normal and Parkinson’s disease subjects. Brain 118:913–933PubMedCrossRef Jahanshahi M, Jenkins IH, Brown RG, Marsden CD, Passingham RE, Brooks DJ (1995) Self-initiated versus externally triggered movements. I. An investigation using measurement of regional cerebral blood flow with PET and movement-related potentials in normal and Parkinson’s disease subjects. Brain 118:913–933PubMedCrossRef
go back to reference Jenkins IH, Jahanshahi M, Jueptner M, Passingham RE, Brooks DJ (2000) Self-initiated versus externally triggered movements. II. The effect of movement predictability on regional cerebral blood flow. Brain 123(Pt 6):1216–1228PubMedCrossRef Jenkins IH, Jahanshahi M, Jueptner M, Passingham RE, Brooks DJ (2000) Self-initiated versus externally triggered movements. II. The effect of movement predictability on regional cerebral blood flow. Brain 123(Pt 6):1216–1228PubMedCrossRef
go back to reference Jueptner M, Weiller C (1998) A review of differences between basal ganglia and cerebellar control of movements as revealed by functional imaging studies. Brain 121(Pt 8):1437–1449PubMedCrossRef Jueptner M, Weiller C (1998) A review of differences between basal ganglia and cerebellar control of movements as revealed by functional imaging studies. Brain 121(Pt 8):1437–1449PubMedCrossRef
go back to reference Jueptner M, Jenkins IH, Brooks DJ, Frackowiak RS, Passingham RE (1996) The sensory guidance of movement: a comparison of the cerebellum and basal ganglia. Exp Brain Res 112:462–474PubMedCrossRef Jueptner M, Jenkins IH, Brooks DJ, Frackowiak RS, Passingham RE (1996) The sensory guidance of movement: a comparison of the cerebellum and basal ganglia. Exp Brain Res 112:462–474PubMedCrossRef
go back to reference Kitahama K, Denoroy L, Goldstein M, Jouvet M, Pearson J (1988) Immunohistochemistry of tyrosine hydroxylase and phenylethanolamine N-methyltransferase in the human brain stem: description of adrenergic perikarya and characterization of longitudinal catecholaminergic pathways. Neuroscience 25:97–111PubMedCrossRef Kitahama K, Denoroy L, Goldstein M, Jouvet M, Pearson J (1988) Immunohistochemistry of tyrosine hydroxylase and phenylethanolamine N-methyltransferase in the human brain stem: description of adrenergic perikarya and characterization of longitudinal catecholaminergic pathways. Neuroscience 25:97–111PubMedCrossRef
go back to reference Lavoie B, Parent A (1994) Pedunculopontine nucleus in the squirrel monkey: distribution of cholinergic and monoaminergic neurons in the mesopontine tegmentum with evidence for the presence of glutamate in cholinergic neurons. J Comp Neurol 344:190–209. doi:10.1002/cne.903440203 PubMedCrossRef Lavoie B, Parent A (1994) Pedunculopontine nucleus in the squirrel monkey: distribution of cholinergic and monoaminergic neurons in the mesopontine tegmentum with evidence for the presence of glutamate in cholinergic neurons. J Comp Neurol 344:190–209. doi:10.​1002/​cne.​903440203 PubMedCrossRef
go back to reference LeDoux MS, Hurst DC, Lorden JF (1998) Single-unit activity of cerebellar nuclear cells in the awake genetically dystonic rat. Neuroscience 86:533–545PubMedCrossRef LeDoux MS, Hurst DC, Lorden JF (1998) Single-unit activity of cerebellar nuclear cells in the awake genetically dystonic rat. Neuroscience 86:533–545PubMedCrossRef
go back to reference Lewis MM, Galley S, Johnson S, Stevenson J, Huang X, McKeown MJ (2013) The role of the cerebellum in the pathophysiology of Parkinson’s disease. Can J Neurol Sci 40:299–306 P75M6432U3U148L5PubMedCrossRef Lewis MM, Galley S, Johnson S, Stevenson J, Huang X, McKeown MJ (2013) The role of the cerebellum in the pathophysiology of Parkinson’s disease. Can J Neurol Sci 40:299–306 P75M6432U3U148L5PubMedCrossRef
go back to reference Llinas R, Sugimori M (1980a) Electrophysiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices. J Physiol 305:197–213PubMedCentralPubMedCrossRef Llinas R, Sugimori M (1980a) Electrophysiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices. J Physiol 305:197–213PubMedCentralPubMedCrossRef
go back to reference Machado AG, Cooperrider J, Furmaga HT, Baker KB, Park HJ, Chengabigabi Z, Gale J (2013) Chronic 30 Hz deep cerebellar stimulation coupled with training enhances post-ischemia motor recovery and peri-infarct synaptophysin expression in rodents. Neurosurgery 73:344–353. doi:10.1227/01.neu.0000430766.80102.ac PubMedCrossRef Machado AG, Cooperrider J, Furmaga HT, Baker KB, Park HJ, Chengabigabi Z, Gale J (2013) Chronic 30 Hz deep cerebellar stimulation coupled with training enhances post-ischemia motor recovery and peri-infarct synaptophysin expression in rodents. Neurosurgery 73:344–353. doi:10.​1227/​01.​neu.​0000430766.​80102.​ac PubMedCrossRef
go back to reference Martin GF, Cabana T, Culberson JL, Curry JJ, Tschismadia I (1980) The early development of corticobulbar and corticospinal systems. Studies using the North American opossum. Anat Embryol 161:197–213PubMedCrossRef Martin GF, Cabana T, Culberson JL, Curry JJ, Tschismadia I (1980) The early development of corticobulbar and corticospinal systems. Studies using the North American opossum. Anat Embryol 161:197–213PubMedCrossRef
go back to reference Martinez-Gonzalez C, Wang HL, Micklem BR, Bolam JP, Mena-Segovia J (2012) Subpopulations of cholinergic, GABAergic and glutamatergic neurons in the pedunculopontine nucleus contain calcium-binding proteins and are heterogeneously distributed. Eur J Neurosci 35:723–734. doi:10.1111/j.1460-9568.2012.08002.x PubMedCrossRef Martinez-Gonzalez C, Wang HL, Micklem BR, Bolam JP, Mena-Segovia J (2012) Subpopulations of cholinergic, GABAergic and glutamatergic neurons in the pedunculopontine nucleus contain calcium-binding proteins and are heterogeneously distributed. Eur J Neurosci 35:723–734. doi:10.​1111/​j.​1460-9568.​2012.​08002.​x PubMedCrossRef
go back to reference Mehta A, Menalled L, Chesselet MF (2005) Behavioral responses to injections of muscimol into the subthalamic nucleus: temporal changes after nigrostriatal lesions. Neuroscience 131:769–778PubMedCrossRef Mehta A, Menalled L, Chesselet MF (2005) Behavioral responses to injections of muscimol into the subthalamic nucleus: temporal changes after nigrostriatal lesions. Neuroscience 131:769–778PubMedCrossRef
go back to reference Miall RC, Keating JG, Malkmus M, Thach WT (1998) Simple spike activity predicts occurrence of complex spikes in cerebellar Purkinje cells. Nat Neurosci 1:13–15. doi:10.1038/212 PubMedCrossRef Miall RC, Keating JG, Malkmus M, Thach WT (1998) Simple spike activity predicts occurrence of complex spikes in cerebellar Purkinje cells. Nat Neurosci 1:13–15. doi:10.​1038/​212 PubMedCrossRef
go back to reference Monakow KH, Akert K, Kunzle H (1979) Projections of precentral and premotor cortex to the red nucleus and other midbrain areas in Macaca fascicularis. Exp Brain Res 34:91–105PubMedCrossRef Monakow KH, Akert K, Kunzle H (1979) Projections of precentral and premotor cortex to the red nucleus and other midbrain areas in Macaca fascicularis. Exp Brain Res 34:91–105PubMedCrossRef
go back to reference Moroz VM, Bures J (1984) Effects of lateralized reaching and cerebellar stimulation on unit activity of motor cortex and caudate nucleus in rats. Exp Neurol 84:47–57 0014-4886(84)90005-0PubMedCrossRef Moroz VM, Bures J (1984) Effects of lateralized reaching and cerebellar stimulation on unit activity of motor cortex and caudate nucleus in rats. Exp Neurol 84:47–57 0014-4886(84)90005-0PubMedCrossRef
go back to reference Mushiake H, Strick PL (1995) Pallidal neuron activity during sequential arm movements. J Neurophysiol 74:2754–2758PubMed Mushiake H, Strick PL (1995) Pallidal neuron activity during sequential arm movements. J Neurophysiol 74:2754–2758PubMed
go back to reference Nauta HJ, Cole M (1974) Efferent projections of the subthalamic nucleus. Trans Am Neurol Assoc 99:170–173PubMed Nauta HJ, Cole M (1974) Efferent projections of the subthalamic nucleus. Trans Am Neurol Assoc 99:170–173PubMed
go back to reference Newman DB, Ginsberg CY (1992) Brainstem reticular nuclei that project to the cerebellum in rats: a retrograde tracer study. Brain Behav Evol 39:24–68PubMedCrossRef Newman DB, Ginsberg CY (1992) Brainstem reticular nuclei that project to the cerebellum in rats: a retrograde tracer study. Brain Behav Evol 39:24–68PubMedCrossRef
go back to reference Nowak DA, Tisch S, Hariz M, Limousin P, Topka H, Rothwell JC (2006) Sensory timing cues improve akinesia of grasping movements in Parkinson’s disease: a comparison to the effects of subthalamic nucleus stimulation. Mov Disord 21:166–172. doi:10.1002/mds.20657 PubMedCrossRef Nowak DA, Tisch S, Hariz M, Limousin P, Topka H, Rothwell JC (2006) Sensory timing cues improve akinesia of grasping movements in Parkinson’s disease: a comparison to the effects of subthalamic nucleus stimulation. Mov Disord 21:166–172. doi:10.​1002/​mds.​20657 PubMedCrossRef
go back to reference Olsson M, Nikkhah G, Bentlage C, Bjorklund A (1995) Forelimb akinesia in the rat Parkinson model: differential effects of dopamine agonists and nigral transplants as assessed by a new stepping test. J Neurosci 15:3863–3875PubMed Olsson M, Nikkhah G, Bentlage C, Bjorklund A (1995) Forelimb akinesia in the rat Parkinson model: differential effects of dopamine agonists and nigral transplants as assessed by a new stepping test. J Neurosci 15:3863–3875PubMed
go back to reference Parent A, Smith Y (1987) Organization of efferent projections of the subthalamic nucleus in the squirrel monkey as revealed by retrograde labeling methods. Brain Res 436:296–310 0006-8993(87)91674-XPubMedCrossRef Parent A, Smith Y (1987) Organization of efferent projections of the subthalamic nucleus in the squirrel monkey as revealed by retrograde labeling methods. Brain Res 436:296–310 0006-8993(87)91674-XPubMedCrossRef
go back to reference Paxonis G, Watson C (1998) The rat atlas: in stereotaxic coordinates, 4th edn. Academic Press, San Diego Paxonis G, Watson C (1998) The rat atlas: in stereotaxic coordinates, 4th edn. Academic Press, San Diego
go back to reference Peeters RR, Verhoye M, Vos BP, Van Dyck D, Van Der Linden A, De Schutter E (1999) A patchy horizontal organization of the somatosensory activation of the rat cerebellum demonstrated by functional MRI. Eur J Neurosci 11:2720–2730 ejn687PubMedCrossRef Peeters RR, Verhoye M, Vos BP, Van Dyck D, Van Der Linden A, De Schutter E (1999) A patchy horizontal organization of the somatosensory activation of the rat cerebellum demonstrated by functional MRI. Eur J Neurosci 11:2720–2730 ejn687PubMedCrossRef
go back to reference Rascol O et al (1997) The ipsilateral cerebellar hemisphere is overactive during hand movements in akinetic parkinsonian patients. Brain 120(Pt 1):103–110PubMedCrossRef Rascol O et al (1997) The ipsilateral cerebellar hemisphere is overactive during hand movements in akinetic parkinsonian patients. Brain 120(Pt 1):103–110PubMedCrossRef
go back to reference Ruggiero DA, Anwar M, Golanov EV, Reis DJ (1997) The pedunculopontine tegmental nucleus issues collaterals to the fastigial nucleus and rostral ventrolateral reticular nucleus in the rat. Brain Res 760:272–276PubMedCrossRef Ruggiero DA, Anwar M, Golanov EV, Reis DJ (1997) The pedunculopontine tegmental nucleus issues collaterals to the fastigial nucleus and rostral ventrolateral reticular nucleus in the rat. Brain Res 760:272–276PubMedCrossRef
go back to reference Rye DB, Saper CB, Lee HJ, Wainer BH (1987) Pedunculopontine tegmental nucleus of the rat: cytoarchitecture, cytochemistry, and some extrapyramidal connections of the mesopontine tegmentum. J Comp Neurol 259:483–528. doi:10.1002/cne.902590403 PubMedCrossRef Rye DB, Saper CB, Lee HJ, Wainer BH (1987) Pedunculopontine tegmental nucleus of the rat: cytoarchitecture, cytochemistry, and some extrapyramidal connections of the mesopontine tegmentum. J Comp Neurol 259:483–528. doi:10.​1002/​cne.​902590403 PubMedCrossRef
go back to reference Schallert T, Fleming SM, Leasure JL, Tillerson JL, Bland ST (2000) CNS plasticity and assessment of forelimb sensorimotor outcome in unilateral rat models of stroke, cortical ablation, Parkinsonism and spinal cord injury. Neuropharmacology 39:777–787. pii: S0028390800000058PubMedCrossRef Schallert T, Fleming SM, Leasure JL, Tillerson JL, Bland ST (2000) CNS plasticity and assessment of forelimb sensorimotor outcome in unilateral rat models of stroke, cortical ablation, Parkinsonism and spinal cord injury. Neuropharmacology 39:777–787. pii: S0028390800000058PubMedCrossRef
go back to reference Schell GR, Strick PL (1984) The origin of thalamic inputs to the arcuate premotor and supplementary motor areas. J Neurosci 4:539–560PubMed Schell GR, Strick PL (1984) The origin of thalamic inputs to the arcuate premotor and supplementary motor areas. J Neurosci 4:539–560PubMed
go back to reference Sestini S, Ramat S, Formiconi AR, Ammannati F, Sorbi S, Pupi A (2005) Brain networks underlying the clinical effects of long-term subthalamic stimulation for Parkinson’s disease: a 4-year follow-up study with rCBF SPECT. J Nucl Med 46:1444–1454 46/9/1444PubMed Sestini S, Ramat S, Formiconi AR, Ammannati F, Sorbi S, Pupi A (2005) Brain networks underlying the clinical effects of long-term subthalamic stimulation for Parkinson’s disease: a 4-year follow-up study with rCBF SPECT. J Nucl Med 46:1444–1454 46/9/1444PubMed
go back to reference Shinoda Y, Kano M, Futami T (1985) Synaptic organization of the cerebello-thalamo-cerebral pathway in the cat. I. Projection of individual cerebellar nuclei to single pyramidal tract neurons in areas 4 and 6. Neurosci Res 2:133–156. pii:S0168-0102(85)90009-4PubMedCrossRef Shinoda Y, Kano M, Futami T (1985) Synaptic organization of the cerebello-thalamo-cerebral pathway in the cat. I. Projection of individual cerebellar nuclei to single pyramidal tract neurons in areas 4 and 6. Neurosci Res 2:133–156. pii:S0168-0102(85)90009-4PubMedCrossRef
go back to reference Takakusaki K, Shiroyama T, Kitai ST (1997) Two types of cholinergic neurons in the rat tegmental pedunculopontine nucleus: electrophysiological and morphological characterization. Neuroscience 79:1089–1109. pii: S0306-4522(97)00019-5PubMedCrossRef Takakusaki K, Shiroyama T, Kitai ST (1997) Two types of cholinergic neurons in the rat tegmental pedunculopontine nucleus: electrophysiological and morphological characterization. Neuroscience 79:1089–1109. pii: S0306-4522(97)00019-5PubMedCrossRef
go back to reference Vajnerova O, Zhuravin IA, Brozek G (2000) Functional ablation of deep cerebellar nuclei temporarily impairs learned coordination of forepaw and tongue movements. Behav Brain Res 108:189–195. pii: S0166432899001473PubMedCrossRef Vajnerova O, Zhuravin IA, Brozek G (2000) Functional ablation of deep cerebellar nuclei temporarily impairs learned coordination of forepaw and tongue movements. Behav Brain Res 108:189–195. pii: S0166432899001473PubMedCrossRef
go back to reference van Donkelaar P, Stein JF, Passingham RE, Miall RC (2000) Temporary inactivation in the primate motor thalamus during visually triggered and internally generated limb movements. J Neurophysiol 83:2780–2790PubMed van Donkelaar P, Stein JF, Passingham RE, Miall RC (2000) Temporary inactivation in the primate motor thalamus during visually triggered and internally generated limb movements. J Neurophysiol 83:2780–2790PubMed
Metadata
Title
Stimulation of the subthalamic nucleus engages the cerebellum for motor function in parkinsonian rats
Authors
Alexander C. Sutton
Katherine A. O’Connor
Julie G. Pilitsis
Damian S. Shin
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/s00429-014-0876-8

Other articles of this Issue 6/2015

Brain Structure and Function 6/2015 Go to the issue