High frequency stimulation of the subthalamic nucleus acutely rescues motor deficits and neocortical movement representations following 6-hydroxydopamine administration in rats

Experimental Neurology

Volumn 231, Issue 1, 2011, Pages 82-90

  Brown, Andrew R ^a   Antle, Michael C ^a,b,c   Hu, Bin ^a,c   Teskey, G Campbell ^a,b,c  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

^c UNIVERSITY OF CALGARY   (Canada)

Author keywords

6 Hydroxydopamine; Behaviour; Deep brain stimulation; Dopamine; Motor map; Parkinson's disease; Subthalamic nucleus

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN DEPTH STIMULATION; CONTROLLED STUDY; ELECTRODE; FORELIMB; LIMB MOVEMENT; LOCOMOTION; MALE; MOTOR CORTEX; MOTOR DYSFUNCTION; NEOCORTEX; NONHUMAN; PRIORITY JOURNAL; RAT; STRIATONIGRAL DEGENERATION; SUBTHALAMIC NUCLEUS; THERAPY EFFECT;

ANIMALS; DEEP BRAIN STIMULATION; ELECTRODES, IMPLANTED; MALE; MOVEMENT DISORDERS; NEOCORTEX; NEUROTOXINS; OXIDOPAMINE; PARKINSONIAN DISORDERS; RATS; RATS, LONG-EVANS; SUBTHALAMIC NUCLEUS;

EID: 79961028382     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2011.05.017     Document Type: Article

References (59)

1. Alexander G.E., Crutcher M.D., DeLong M.R. Basal ganglia-thalamocortical circuits: parallel substrates for motor, oculomotor, "prefrontal" and "limbic" functions. Prog. Brain. Res. 1990, 85:119-146.
2. Anderson T., Hu B., Iremonger K., Kiss Z.H. Selective attenuation of afferent synaptic transmission as a mechanism of thalamic deep brain stimulation-induced tremor arrest. J. Neurosci. 2006, 26:841-850.
3. Ashby P., Paradiso G., Saint-Cyr J.A., Chen R., Lang A.E., Lozano A.M. Potentials recorded at the scalp by stimulation near human subthalamic nucleus. Clin. Neurophys. 2001, 112:431-437.
4. Ben V., Blin O., Brugeurolle B. Time-dependent striatal dopamine depletion after injection of 6-hydroxydopamine in the rat. Comparison of single bilateral and double bilateral lesions. J. Pharmacol. 1999, 51:1405-1408.
5. Beurrier C., Biolac B., Audin J., Hammond C. High-frequency stimulation produces a transient blockade of voltage-gated currents in subthalamic neurons. J. Neurophysiol. 2001, 85:1351-1356.
6. Boychuk J.A., Adkins D.L., Kleim J.A. Distributed versus focal cortical stimulation to enhance motor function and motor map plasticity in a rodent model of ischemia. Neurorehab. Neural Repair 2011, 25:88-97.
7. Brown P., Eusebio A. Paradoxes of functional neurosurgery: clues from basal ganglia recordings. Mov. Disord. 2008, 23:12-20.
8. Brown A.R., Hu B., Antle M.C., Teskey G.C. Neocortical movement representations are reduced and reorganized following bilateral intrastriatal 6-hydroxydopamine infusion and dopamine type-2 receptor antagonism. Exp. Neurol. 2009, 220:162-170.
9. Buhmann C., Glauche V., Sturenburg H.J., Oechsner M., Weiller C., Buchel C. Pharmacologically modulated fMRI cortical responsiveness to levodopa in drug-naive hemiparkinsonian patients. Brain 2003, 126:451-461.
10. Ceballos-Baumann A.O., Boecker H., Bartenstein P., von Falkenhayn I., Riescher H., Conrad B., Moringlane J.P., Alexch F. A positron emission tomographic study of subthalamic nucleus stimulation in Parkinson disease. Enhanced movement-related activity of motor-association cortex and decreased motor cortex resting activity. Arch. Neurol. 1999, 56:997-1003.
11. Chomiak T., Hu B. Axonal and somatic filtering of antidromically evoked cortical excitation by simulated deep brain stimulation in rat brain. J. Physiol. 2007, 579:403-412.
12. Dejean C., Hyland B., Arbuthnott G. Cortical effects of subthalamic stimulation correlate with behavioural recovery from dopamine antagonist induced akinesia. Cereb. Cortex. 2009, 19:1055-1063.
13. DeLong M.R., Wichmann T. Basal ganglia-thalamocortical circuits in Parkinsonian signs. Clin. Neurosci. 1993, 1:18-26.
14. Deumens R., Blokland A., Prickaerts J. Modeling Parkinson's disease in rats: an evaluation of 6-OHDA lesions of the nigrostriatal pathway. Exp. Neurol. 2002, 175:303-317.
15. Deuschl G., Schade-Brittinger C., Krack P., Volkmann J., Schäfer H., Bötzel K., Daniels C., Deutschländer A., Dillmann U., Eisner W., et al. A randomized trial of deep-brain stimulation for Parkinson's disease. N. Engl. J. Med. 2006, 355:896-908.
16. Dostrovsky J.O., Lozano A.M. Mechanisms of deep brain stimulation. Mov. Disord. 2002, 17(S3):S63-S68.
17. Flynn C., Young N.A., Teskey G.C. Seizures, but not lowered seizure thresholds, results in larger neocortical motor maps and concomitant disruptions in skilled motor behaviour. Behav. Brain Res. 2010, 214:60-65.
18. Friel K.M., Heddings A.A., Nudo R.J. Effects of postlesion experience on behavioural recovery and neurophysiologic reorganization after cortical injury in primates. Neurorehabil. Neural Repair 2000, 14:187-198.
19. Gradinaru V., Mogri M., Thompson K.R., Henderson J.M., Deisseroth K. Optical deconstruction of parkinsonian neural circuitry. Science 2009, 324:354-359.
20. Haslinger B., Erhard P., Kampfe N., Boecker H., Rummeny E., Schwaiger M., et al. Event-related functional magnetic resonance imaging in Parkinson's disease before and after levodopa. Brain 2001, 124:558-570.
21. Jenkins I.H., Fernandez W., Playford E.D., Lees A.J., Frackowiak R.S., Passingham R.E., et al. Impaired activation of the supplementary motor areas in Parkinson's disease is reversed when akinesia is treated with apomorphine. Ann. Neurol. 1992, 32:749-757.
22. Kleim J.A., Barbay S., Nudo R.J. Functional reorganization of the rat motor cortex following motor skill learning. J. Neurophysiol. 1998, 80:3321-3325.
23. Kleim J.A., Bruneau R., VandenBerg P., MacDonald E., Mulrooney R., Pocock D. Motor cortex stimulation enhances motor recovery and reduces peri-infarct dysfunction following ischemic insult. Neurol. Res. 2003, 25:789-793.
24. Kleim J.A., Hogg T.M., VandenBerg P.M., Cooper N.R., Bruneau R., Remple M. Cortical synaptogenesis and motor map reorganization occur during late, but not early, phase of motor skill learning. J. Neurosci. 2004, 24:628-633.
25. Krack P., Batir A., Van Blercom N., Chabardes S., Fraix V., Ardouin C., Koudsie A., Limousin P.D., Benazzouz A., Lebas J.F., Benabid A.L., Pollack P. Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson's disease. N. Engl. J. Med. 2003, 349:1925-1934.
26. Li S., Arbuthnott G.W., Jutras M.J., Goldberg J.A., Jaeger D. Resonant antidromic cortical circuit activation as a consequence of high-frequency subthalamic deep-brain stimulation. J. Neurophysiol. 2007, 98:3525-3537.
27. Limousin P., Pollak P., Benazzouz A., Hoffmann D., Broussolle E., Perret J.E., Benabid A.L. Bilateral subthalamic nucleus stimulation for severe Parkinson's disease. Mov. Disord. 1995, 10:672-674.
28. McIntyre C.C., Savasta M., Walter B.L., Vitek J.L. How does deep brain stimulation work? Present understanding and future questions. J. Clin. Neurophysiol. 2004, 21:40-50.
29. Metz G.A., Piecharka D.M., Kleim J.A., Whishaw I.Q. Preserved ipsilateral-to-lesion motor map organization in the unilateral 6-OHDA-treated rat model of Parkinson's disease. Brain Res. 2004, 1026:126-135.
30. Molino A., McIntyre D.C. Another inexpensive headplug for the electrical recording and or stimulation of rats. Physiol. Behav. 1972, 9:273-275.
31. Neafsey E.J., Sievert C. A second forelimb motor area exists in the rat frontal cortex. Brain Res. 1992, 232:151-156.
32. Neafsey E.J., Bold E.L., Haas G., Hurley-Gius K.M., Quirk G., Sievert C.F., Terreberry R.R. The organization of the rat motor cortex: a microstimulation mapping study. Brain Res. 1986, 396:77-96.
33. Nudo R.J., Jenkins W.M., Merzenich M.M. Repetitive microstimulation alters the cortical representation of movements in adult rats. Somatosen. Mot. Res. 1990, 7:463-483.
34. Nudo R.J., Plautz E.J., Milliken G.W. Adaptive plasticity in the primate motor cortex as a consequence of behavioural experience and neuronal injury. Semin. Neurosci. 1997, 9:13-23.
35. Orieux G., François C., Féger J., Hirsch E.C. Consequences of dopaminergic denervation on the metabolic activity of the cortical neurons projecting to the subthalamic nucleus in the rat. J. Neurosci. 2002, 22:8762-8770.
36. Parent A., Hazrati L.N. Functional anatomy of the basal ganglia. I. The cortico-basal-ganglia-thalamo-cortical-loop. Brain Res. Rev. 1995, 20:91-127.
37. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 2005, Elsevier Academic Press, San Diego. 5th ed.
38. Perlmutter J.S., Mink J.W. Deep brain stimulation. Annu. Rev. Neurosci. 2006, 29:229-257.
39. Piecharka D.M., Kleim J.A., Whishaw I.Q. Limits on recovery in the corticospinal tract of the rat: partial lesions impair skilled reaching and the topographic representation of the forelimb in the motor cortex. Brain Res. Bull. 2005, 66:203-211.
40. Playford E.D., Jenkins I.H., Passingham R.E., Nutt J., Frackowiak R.S., Brooks D.J. Impaired mesial frontal and putamen activation in Parkinson's disease: a positron emission tomography study. Ann. Neurol. 1992, 32:151-161.
41. Prine E.P., Thomas N.J., Mailing N., Kleim J.A. Differential sensitivity of oral motor vs. Limb motor function in an animal model of Parkinson's disease. Program No 52.2/L11. San Diego, CA: Neuroscience Meeting Planner; 2010, Society for Neuroscience, Online 2010.
42. Rascol O., Sabatini U., Chollet F., Fabre N., Senard J.M., Montastruc J.L., Celsis P., Marc-Vergnes J.P., Rascol A. Normal activation of the supplementary motor area in patients with Parkinson's disease undergoing long-term treatment with levodopa. J. Neurol. Neurosurg. Psychiatry 1994, 57:567-571.
43. Rolland A.S., Herrero M.T., Garcia-Martinez V., Ruberg M., Hirsch E.C., François C. Metabolic activity of cerebellar and basal ganglia-thalamic neurons is reduced in parkinsonism. Brain 2007, 130:265-275.
44. Russell W.M.S., Burch R.L. The Principles of Humane Experimental Technique 1959, Methuen, London.
45. Sabatini U., Boulanouar K., Fabre N., Martin F., Carel C., Colonnese C., Bozzao L., Berry I., Montastruc J.L., Chollet F., Rascol O. Cortical motor reorganization in akinetic patients with Parkinson's disease. Brain 2000, 123:394-403.
46. Schallert T., Woodlee M.T. Orienting and placing. The behavior of the laboratory rat: a handbook with tests. 2005, Oxford University Press, New York. I.Q. Whishaw, B. Kolb (Eds.).
47. Schallert T., Fleming S.M., Leasure J.L., Tillerson J.L., Bland S.T. CNS plasticity and assessment of forelimb sensorimotor outcome in unilateral rat models of stroke, cortical ablation, parkinsonism and spinal cord injury. Neuropharmacology 2000, 39:777-787.
48. Schwarting R.K.W., Huston J.P. The unilateral 6-hydroxydopamine lesion model in behavioural brain research. Analysis of functional deficits, recovery and treatments. Progr. Neurobiol. 1996, 50:275-331.
49. Shi L.H., Woodward D.J., Luo F., Anstrom K., Schallert T., Chang J.Y. High-frequency stimulation of the subthalamic nucleus reverses limb-use asymmetry in rats with unilateral 6-hydroxydopamine lesions. Brain Res. 2004, 1013:98-106.
50. Steiner H., Kitai S.T. Regulation of the rat cortex function by D1 dopamine receptors in the striatum. J. Neurosci. 2000, 20:5449-5460.
51. Stoney S.D., Thompson W.D., Asanuma H. Excitation of pyramidal tract cells by intracortical microstimulation: effective extend of stimulating current. J. Neurophysiol. 1968, 31:659-669.
52. Tandon S., Kambi N., Jain N. Overlapping representations of the neck and whiskers in the rat motor cortex revealed by mapping at different anaesthetic depths. Eur. J. Neurosci. 2008, 27:228-237.
53. Teskey G.C., Monfils M.H., VandenBerg P.M., Kleim J.A. Motor map expansion following repeated cortical and limbic seizures is related to synaptic potentiation. Cereb. Cortex 2002, 12:98-105.
54. Teskey G.C., Young N.A., van Rooyen F., Larson S.E.M., Flynn C., Monfils M.H., Kleim J.A., Henry L.C., Goertzen C.D. Induction of neocortical long-term depression results in smaller movement representations, fewer excitatory perforated synapses and more inhibitory synapses. Cereb. Cortex 2007, 17:434-442.
55. Teskey G.C., Monfils M.H., Flynn C., Young N.A., van Rooyen F., Henry L.C., Ozen L.J., Henderson A.K., Reid A.Y., Brown A.R. Motor maps, seizures, and behaviour. Can. J. Exp. Psychol. 2008, 62:132-139.
56. Trantzer J.P., Thoenen H. Ultramorphologische Veränderungen der sympatischen Nervenendungen der Katze nach Vorbehandlung met 5- und 6-hydroxydopamin. Naunyn Schmiedebergs Arch. Exp. Pathol. Pharmakol. 1967, 5:107-110.
57. Ungerstedt U. 6-Hydroxy-dopamine induced degeneration of central monoamine neurons. Eur. J. Pharmacol. 1968, 5:107-110.
58. Young C.K., Brown A.R., Robinson J.H., Tuor U.I., Dunn J.F., Bland B.H., Teskey G.C. Functional MRI response and correlated electrophysiological changes during posterior hypothalamic nucleus deep brain stimulation. NeuroImage 2011, 56:35-44.
59. Young N.A., Vuong J., Flynn C., Teskey G.C. Optimal parameters for microstimulation derived forelimb movement thresholds and motor maps in rats and mice. J. Neurosci. Meth. 2011, 196:60-69.