Effect of ventrolateral thalamic nucleus lesions in the unilateral 6-hydroxydopamine rat model

Whilst dysfunction of basal ganglia-thalamic circuitry is implicated in the genesis of parkinsonian symptomatology, few studies have examined the effects of lesioning the motor thalamus in the context of parkinsonism. Forty rats were therefore subdivided into four lesion groups each of 10 rats with lesions or sham surgery targeting (1) the medial forebrain bundle and/or (2) motor thalamus, resulting in: Sham/Sham, 6-OHDA/Sham, Sham/NMDA and 6-OHDA/NMDA groups. Behavioural testing was performed prior to any surgery and after each surgery including analysis of posture, drug-induced rotation, sensorimotor and autonomic deficits. As expected 6-OHDA lesions induced abnormalities in posture, locomotion, sensorimotor and pilomotor function, ipsilateral and contralateral rotational asymmetries after amphetamine and apomorphine, respectively. These behavioural changes reflect parkinsonism in this model. Additional thalamic lesions virtually abolished apomorphine-induced rotational asymmetry and improved sensorimotor response latency to tactile stimulation on the contralateral side. These data support the contribution of dysfunctional motor thalamic circuitry in rotational asymmetry and abnormal sensorimotor function in parkinsonian rats.

[1]  U. Ungerstedt,et al.  Postsynaptic supersensitivity after 6-hydroxy-dopamine induced degeneration of the nigro-striatal dopamine system. , 1971, Acta physiologica Scandinavica. Supplementum.

[2]  J. Henderson,et al.  Behavioural effects of parafascicular thalamic lesions in an animal model of parkinsonism , 2005, Behavioural Brain Research.

[3]  H. Narabayashi Stereotactic Surgery and Parkinson’s Disease , 1998, Stereotactic and Functional Neurosurgery.

[4]  Gregory F. Molnar,et al.  Short and long latency afferent inhibition in Parkinson's disease. , 2003, Brain : a journal of neurology.

[5]  Marc A Sommer,et al.  The role of the thalamus in motor control , 2003, Current Opinion in Neurobiology.

[6]  M. Matsumura,et al.  Tremor-mediating thalamic zone studied in humans and in monkeys. , 1993, Stereotactic and functional neurosurgery.

[7]  U. Castiello,et al.  The bilateral reach-to-grasp movement of Parkinson's disease subjects. , 1997, Brain : a journal of neurology.

[8]  R Iansek,et al.  Bimanual co-ordination in Parkinson's disease. , 1998, Brain : a journal of neurology.

[9]  Nikolaus R. McFarland,et al.  Organization of thalamostriatal terminals from the ventral motor nuclei in the macaque , 2001, The Journal of comparative neurology.

[10]  T. Schallert,et al.  ‘Disengage’ sensorimotor deficit following apparent recovery from unilateral dopamine depletion , 1988, Behavioural Brain Research.

[11]  J. Parkinson An Essay on the Shaking Palsy , 2002 .

[12]  F. Fenelon [Neurosurgery of parkinsonian syndrome by direct intervention on the extrapyramidal tracts immediately below the lenticular nucleus. Communication followed by film showing patient before and after intervention]. , 1950, Revue neurologique.

[13]  P. Strick,et al.  The origin of thalamic inputs to the arcuate premotor and supplementary motor areas , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  J. D. Parkes,et al.  "ON-OFF" EFFECTS IN PATIENTS WITH PARKINSON'S DISEASE ON CHRONIC LEVODOPA THERAPY , 1976, The Lancet.

[15]  E. G. Jones,et al.  A new parcellation of the human thalamus on the basis of histochemical staining , 1989, Brain Research Reviews.

[16]  Y. Smith,et al.  The thalamostriatal system: a highly specific network of the basal ganglia circuitry , 2004, Trends in Neurosciences.

[17]  Dopamine mediated circling behaviour is modulated by lesions of the ventromedial nucleus of the thalamus [proceedings]. , 1979, British journal of pharmacology.

[18]  C. Markham,et al.  Parkinson's disease , 1987, Neurology.

[19]  Entopeduncular lesions facilitate and thalamic lesions depress spontaneous and drug‐evoked motor behavior in the hemiparkinsonian rat , 2001, Synapse.

[20]  J. Schneider,et al.  Alterations in intralaminar and motor thalamic physiology following nigrostriatal dopamine depletion , 1996, Brain Research.

[21]  G. E. Alexander Basal Ganglia‐Thalamocortical Circuits: Their Role in Control of Movements , 1994, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[22]  C. Ohye,et al.  Lesioning the Thalamus for Dyskinesia , 2002, Stereotactic and Functional Neurosurgery.

[23]  J. Lanciego,et al.  Considerations on the thalamostriatal system with some functional implications. , 2000, Histology and histopathology.

[24]  G. Percheron,et al.  The primate motor thalamus , 1996, Brain Research Reviews.

[25]  Takashi Hanakawa,et al.  Cognitive Slowing in Parkinson's Disease: A Behavioral Evaluation Independent of Motor Slowing , 2002, The Journal of Neuroscience.

[26]  J. Henderson,et al.  Effects of pallidotomy on motor symptoms in an animal model of Parkinson's disease , 2006, Behavioural Brain Research.

[27]  L. Annett,et al.  Behavioural effects of subthalamic nucleus lesions in the hemiparkinsonian marmoset (Callithrix jacchus) , 1998, The European journal of neuroscience.

[28]  M. Kassiou,et al.  Developing a preclinical model of Parkinson's disease: A study of behaviour in rats with graded 6-OHDA lesions , 2006, Behavioural Brain Research.

[29]  C. Meshul,et al.  Lesion of subthalamic or motor thalamic nucleus in 6‐hydroxydopamine‐treated rats: Effects on striatal glutamate and apomorphine‐induced contralateral rotations , 2004, Synapse.

[30]  C. Honey,et al.  Circling behaviour in 6-hydroxydopamine-lesioned rats given pulsed levodopa is reduced more by lesions in the entopeduncular nucleus/substantia nigra pars reticulata than in the subthalamic nucleus , 1998, Neuroscience Letters.

[31]  L. Schiffer,et al.  Aromatic amino acids and modification of parkinsonism. , 1967, The New England journal of medicine.

[32]  C. Marsden,et al.  Disturbance of sequential movements in patients with Parkinson's disease. , 1987, Brain : a journal of neurology.

[33]  A. Benabid,et al.  Effect on parkinsonian signs and symptoms of bilateral subthalamic nucleus stimulation , 1995, The Lancet.

[34]  C. Marsden,et al.  Basal ganglia outflow pathways and circling behaviour in the rat , 2005, Journal of Neural Transmission.

[35]  C. Worringham,et al.  The control of bimanual aiming movements in Parkinson's disease. , 1988, Journal of neurology, neurosurgery, and psychiatry.

[36]  W. Heindel,et al.  Sensorimotor disinhibition in Parkinson's disease: Effects of levodopa , 1992, Annals of neurology.

[37]  M. Horne,et al.  Postural changes after lesions of the substantia nigra pars reticulata in hemiparkinsonian monkeys , 2005, Behavioural Brain Research.

[38]  T. Matsui,et al.  Cat odour exposure decreases exploratory activity and alters neuropeptide gene expression in CCK2 receptor deficient mice, but not in their wild-type littermates , 2006, Behavioural Brain Research.

[39]  D. Togasaki,et al.  Dose-dependent lesions of the dopaminergic nigrostriatal pathway induced by instrastriatal injection of 6-hydroxydopamine , 1995, Neuroscience.

[40]  C. Borlongan,et al.  Elevated body swing test: a new behavioral parameter for rats with 6- hydroxydopamine-induced hemiparkinsonism , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[41]  M. Horne,et al.  Projections from the substantia nigra pars reticulata to the motor thalamus of the rat: Single axon reconstructions and immunohistochemical study , 2001, The Journal of comparative neurology.

[42]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[43]  J. Henderson,et al.  Use of the narrow beam test in the rat, 6-hydroxydopamine model of Parkinson's disease , 2007, Journal of Neuroscience Methods.

[44]  M. Hallett,et al.  Pathophysiology of bradykinesia in Parkinson's disease. , 2001, Brain : a journal of neurology.

[45]  D. Pow,et al.  Study of projections from the entopeduncular nucleus to the thalamus of the rat , 2000, The Journal of comparative neurology.

[46]  J. Caston,et al.  Effects of centrolateral or medial thalamic lesions on motor coordination and spatial orientation in rats , 2000, Neuroscience Research.

[47]  L. Ryan,et al.  Subthalamic nucleus lesions induce deficits as well as benefits in the hemiparkinsonian rat , 1999, The European journal of neuroscience.

[48]  I. S. Cooper,et al.  Chemopallidectomy and chemothalamectomy. , 1958, Journal of neurosurgery.

[49]  U. Ungerstedt Striatal dopamine release after amphetamine or nerve degeneration revealed by rotational behaviour. , 1971, Acta physiologica Scandinavica. Supplementum.

[50]  C. Marsden,et al.  Dual task performance and processing resources in normal subjects and patients with Parkinson's disease. , 1991, Brain : a journal of neurology.

[51]  A. Benabid,et al.  Long-term suppression of tremor by chronic stimulation of the ventral intermediate thalamic nucleus , 1991, The Lancet.

[52]  A. Weindl,et al.  Sensory processing in Parkinson's and Huntington's disease: investigations with 3D H(2)(15)O-PET. , 1999, Brain : a journal of neurology.

[53]  M. Carpenter,et al.  Projections of the globus pallidus and adjacent structures: An autoradiographic study in the monkey , 1976, The Journal of comparative neurology.

[54]  J. P. Huston,et al.  The unilateral 6-hydroxydopamine lesion model in behavioral brain research. Analysis of functional deficits, recovery and treatments , 1996, Progress in Neurobiology.

[55]  A. Moore,et al.  Impaired sensorimotor integration in parkinsonism and dyskinesia: a role for corollary discharges? , 1987, Journal of neurology, neurosurgery, and psychiatry.

[56]  J. Henderson,et al.  Convulsive and postural effects of lesioning the mid-substantia nigra pars reticulata in naı̈ve and 6-hydroxydopamine lesioned rats , 2003, Brain Research Bulletin.