Network effects of subthalamic deep brain stimulation drive a unique mixture of responses in basal ganglia output

European Journal of Neuroscience

Volumn 36, Issue 2, 2012, Pages 2240-2251

  Humphries, Mark D ^a,b   Gurney, Kevin ^b  

^a ECOLE NORMALE SUPÉRIEURE   (France)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

Basal ganglia; High frequency stimulation; Parkinson's disease

Indexed keywords

ARTICLE; BASAL GANGLION; BRAIN DEPTH STIMULATION; CELL ACTIVATION; CORPUS STRIATUM; GABAERGIC TRANSMISSION; MATHEMATICAL MODEL; NERVE CELL INHIBITION; NERVE CELL MEMBRANE POTENTIAL; NERVE CELL NETWORK; NERVE CELL STIMULATION; PARKINSON DISEASE; PREDICTION; PRIORITY JOURNAL; THERAPY EFFECT; TREATMENT OUTCOME;

ANIMALS; BASAL GANGLIA; BRAIN WAVES; DEEP BRAIN STIMULATION; EVOKED POTENTIALS; MODELS, NEUROLOGICAL; NERVE NET; PARKINSON DISEASE; RATS; SUBTHALAMIC NUCLEUS; SYNAPTIC TRANSMISSION;

EID: 84863993886     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2012.08085.x     Document Type: Article

References (64)

1. Alexander, G.E. & Crutcher, M.D. (1990) Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci., 13, 266-272.
2. Arenkiel, B.R., Peca, J., Davison, I.G., Feliciano, C., Deisseroth, K., Augustine, G.J., Ehlers, M.D. & Feng, G. (2007) In vivo light-induced activation of neural circuitry in transgenic mice expressing channelrhodopsin-2. Neuron, 54, 205-218.
3. Beurrier, C., Congar, P., Bioulac, M. & Hammond, C. (1999) Subthalamic nucleus neurons switch from single spike-activity to burst-firing mode. J. Neurosci., 19, 599-609.
4. Beurrier, C., Bioulac, B., Audin, J. & Hammond, C. (2001) High-frequency stimulation produces a transient blockade of voltage-gated currents in subthalamic neurons. J. Neurophysiol., 85, 1351-1356.
5. Bevan, M.D. & Bolam, J.P. (1995) Cholinergic, GABAergic, and glutamate-enriched inputs from the mesopontine tegmentum to the subthalamic nucleus in the rat. J. Neurosci., 15, 7105-7120.
6. Bevan, M.D., Francis, C.M. & Bolam, J.P. (1995) The glutamate-enriched cortical and thalamic input to neurons in the subthalamic nucleus of the rat: convergence with GABA-positive terminals. J. Comp. Neurol., 361, 491-511.
7. Bevan, M.D., Magill, P.J., Hallworth, N.E., Bolam, J.P. & Wilson, C.J. (2002) Regulation of the timing and pattern of action potential generation in rat subthalamic neurons in vitro by GABA-A IPSPs. J. Neurophysiol., 87, 1348-1362.
8. Birdno, M.J. & Grill, W.M. (2008) Mechanisms of deep brain stimulation in movement disorders as revealed by changes in stimulus frequency. Neurotherapeutics, 5, 14-25.
9. Birdno, M.J., Cooper, S.E., Rezai, A.R. & Grill, W.M. (2007) Pulse-to-pulse changes in the frequency of deep brain stimulation affect tremor and modeled neuronal activity. J. Neurophysiol., 98, 1675-1684.
10. Bosch, C., Degos, B., Deniau, J.-M. & Venance, L. (2011) Subthalamic nucleus high-frequency stimulation generates a concomitant synaptic excitation-inhibition in substantia nigra pars reticulata. J. Physiol., 589, 4189-4207.
11. Bruno, R.M. (2011) Synchrony in sensation. Curr. Opin. Neurobiol., 21, 701-708.
12. Bruno, R.M. & Sakmann, B. (2006) Cortex is driven by weak but synchronously active thalamocortical synapses. Science, 312, 1622-1627.
13. Deep Brain Stimulation for Parkinson's Disease Study Group (2001) Deep-brain stimulation of the subthalamic nucleus or the pars interna of the globus pallidus in Parkinson's disease. N. Engl. J. Med., 345, 956-963.
14. Deniau, J.M., Kitai, S.T., Donoghue, J.P. & Grofova, I. (1982) Neuronal interactions in the substantia nigra pars reticulata through axon collaterals of the projection neurons. An electrophysiological and morphological study. Exp. Brain Res., 47, 105-113.
15. Dorval, A.D., Kuncel, A.M., Birdno, M.J., Turner, D.A. & Grill, W.M. (2010) Deep brain stimulation alleviates parkinsonian bradykinesia by regularizing pallidal activity. J. Neurophysiol., 104, 911-921.
16. Ferron, J.-F., Kroeger, D., Chever, O. & Amzica, F. (2009) Cortical inhibition during burst suppression induced with isoflurane anesthesia. J. Neurosci., 29, 9850-9860.
17. Garcia, L., Audin, J., D'Alessandro, G., Bioulac, B. & Hammond, C. (2003) Dual effect of high-frequency stimulation on subthalamic neuron activity. J. Neurosci., 23, 8743-8751.
18. Garcia, L., D'Alessandro, G., Fernagut, P.-O., Bioulac, B. & Hammond, C. (2005) Impact of high-frequency stimulation parameters on the pattern of discharge of subthalamic neurons. J. Neurophysiol., 94, 3662-3669.
19. Gotz, T., Kraushaar, U., Geiger, J., Lubke, J., Berger, T. & Jonas, P. (1997) Functional properties of AMPA and NMDA receptors expressed in identified types of basal ganglia neurons. J. Neurosci., 17, 204-215.
20. Gradinaru, V., Mogri, M., Thompson, K.R., Henderson, J.M. & Deisseroth, K. (2009) Optical deconstruction of parkinsonian neural circuitry. Science, 324, 354-359.
21. Guo, Y., Rubin, J.E., McIntyre, C.C., Vitek, J.L. & Terman, D. (2008) Thalamocortical relay fidelity varies across subthalamic nucleus deep brain stimulation protocols in a data-driven computational model. J. Neurophysiol., 99, 1477-1492.
22. Gurney, K., Prescott, T.J. & Redgrave, P. (2001) A computational model of action selection in the basal ganglia I: a new functional anatomy. Biol. Cybern., 85, 401-410.
23. Hahn, P.J. & McIntyre, C.C. (2010) Modeling shifts in the rate and pattern of subthalamopallidal network activity during deep brain stimulation. J. Comput. Neurosci., 28, 425-441.
24. Hahn, P.J., Russo, G.S., Hashimoto, T., Miocinovic, S., Xu, W., McIntyre, C.C. & Vitek, J.L. (2008) Pallidal burst activity during therapeutic deep brain stimulation. Exp. Neurol., 211, 243-251.
25. Hammond, C., Bergman, H. & Brown, P. (2007) Pathological synchronization in Parkinson's disease: networks, models and treatments. Trends Neurosci., 30, 357-364.
26. Hashimoto, T., Elder, C.M., Okun, M.S., Patrick, S.K. & Vitek, J.L. (2003) Stimulation of the subthalamic nucleus changes the firing pattern of pallidal neurons. J. Neurosci., 23, 1916-1923.
27. Hikosaka, O., Takikawa, Y. & Kawagoe, R. (2000) Role of the basal ganglia in the control of purposive saccadic eye movements. Physiol. Rev., 80, 953-978.
28. Hoover, J.E. & Strick, P.L. (1993) Multiple output channels in the basal ganglia. Science, 259, 819-821.
29. Humphries, M.D. & Gurney, K.N. (2001) A pulsed neural network model of bursting in the basal ganglia. Neural Netw., 14, 845-863.
30. Humphries, M.D. & Gurney, K. (2007a) Deep brain stimulation of the subthalamic nucleus causes paradoxical inhibition of output in a computational model of the "parkinsonian" basal ganglia. In 2007 Neuroscience Meeting Planner Program No. 622.9. Society for Neuroscience, San Diego, CA, USA.
31. Humphries, M.D. & Gurney, K. (2007b) A means to an end: validating models by fitting experimental data. Neurocomputing, 70, 1892-1896.
32. Humphries, M.D., Stewart, R.D. & Gurney, K.N. (2006) A physiologically plausible model of action selection and oscillatory activity in the basal ganglia. J. Neurosci., 26, 12921-12942.
33. Kita, H., Tachibana, Y., Nambu, A. & Chiken, S. (2005) Balance of monosynaptic excitatory and disynaptic inhibitory responses of the globus pallidus induced after stimulation of the subthalamic nucleus in the monkey. J. Neurosci., 25, 8611-8619.
34. Krasowski, M.D. & Harrison, N.L. (1999) General anaesthetic actions on ligand-gated ion channels. Cell. Mol. Life Sci., 55, 1278-1303.
35. Leblois, A., Boraud, T., Meissner, W., Bergman, H. & Hansel, D. (2006a) Competition between feedback loops underlies normal and pathological dynamics in the basal ganglia. J. Neurosci., 26, 3567-3583.
36. Leblois, A., Meissner, W., Bezard, E., Bioulac, B., Gross, C.E. & Boraud, T. (2006b) Temporal and spatial alterations in GPi neuronal encoding might contribute to slow down movement in Parkinsonian monkeys. Eur. J. Neurosci., 24, 1201-1208.
37. Limousin, P., Pollak, P., Benazzouz, A., Hoffmann, D., Bas, J.F.L., Broussolle, E., Perret, J.E. & Benabid, A.L. (1995) Effect of parkinsonian signs and symptoms of bilateral subthalamic nucleus stimulation. Lancet, 345, 91-95.
38. Magill, P.J., Bolam, J.P. & Bevan, M.D. (2001) Dopamine regulates the impact of the cerebral cortex on the subthalamic nucleus-globus pallidus network. Neuroscience, 106, 313-330.
39. Mailly, P., Charpier, S., Menetrey, A. & Deniau, J.M. (2003) Three-dimensional organization of the recurrent axon collateral network of the substantia nigra pars reticulata neurons in the rat. J. Neurosci., 23, 5247-5257.
40. McIntyre, C.C. & Hahn, P.J. (2010) Network perspectives on the mechanisms of deep brain stimulation. Neurobiol. Dis., 38, 329-337.
41. McIntyre, C.C., Grill, W.M., Sherman, D.L. & Thakor, N.V. (2004) Cellular effects of deep brain stimulation: model-based analysis of activation and inhibition. J. Neurophysiol., 91, 1457-1469.
42. Mink, J.W. (1996) The basal ganglia: focused selection and inhibition of competing motor programs. Prog. Neurobiol., 50, 381-425.
43. Miocinovic, S., Parent, M., Butson, C.R., Hahn, P.J., Russo, G.S., Vitek, J.L. & McIntyre, C.C. (2006) Computational analysis of subthalamic nucleus and lenticular fasciculus activation during therapeutic deep brain stimulation. J. Neurophysiol., 96, 1569-1580.
44. Moran, A., Stein, E., Tischler, H., Belelovsky, K. & Bar-Gad, I. (2011) Dynamic stereotypic responses of basal ganglia neurons to subthalamic nucleus high-frequency stimulation in the parkinsonian primate. Front. Syst. Neurosci., 5, 21.
45. Nambu, A. (2008) Seven problems on the basal ganglia. Curr. Opin. Neurobiol., 18, 595-604.
46. Nisenbaum, E.S. & Wilson, C.J. (1995) Potassium currents responsible for inward and outward rectification in rat neostriatal spiny projection neurons. J. Neurosci., 15, 4449-4463.
47. Nowak, L.G. & Bullier, J. (1998) Axons, but not cell bodies, are activated by electrical stimulation in cortical gray matter. I. Evidence from chronaxie measurements. Exp. Brain Res., 118, 477-488.
48. Parent, M., Levesque, M. & Parent, A. (2001) Two types of projection neurons in the internal pallidum of primates: single-axon tracing and three-dimensional reconstruction. J. Comp. Neurol., 439, 162-175.
49. Perlmutter, J.S. & Mink, J.W. (2006) Deep brain stimulation. Annu. Rev. Neurosci., 29, 229-257.
50. Plenz, D. & Kitai, S.T. (1999) A basal ganglia pacemaker formed by the subthalamic nucleus and external globus pallidus. Nature, 400, 677-682.
51. Ranck, J.B. (1975) Which elements are excited in electrical stimulation of mammalian central nervous system: a review. Brain Res., 98, 417-440.
52. Rattay, F. (1999) The basic mechanism for the electrical stimulation of the nervous system. Neuroscience, 89, 335-346.
53. Redgrave, P., Prescott, T.J. & Gurney, K. (1999) The basal ganglia: a vertebrate solution to the selection problem? Neuroscience, 89, 1009-1023.
54. Reese, R., Leblois, A., Steigerwald, F., Pötter-Nerger, M., Herzog, J., Mehdorn, H.M., Deuschl, G., Meissner, W.G. & Volkmann, J. (2011) Subthalamic deep brain stimulation increases pallidal firing rate and regularity. Exp. Neurol., 229, 517-521.
55. Romanelli, P., Esposito, V., Schaal, D.W. & Heit, G. (2005) Somatotopy in the basal ganglia: experimental and clinical evidence for segregated sensorimotor channels. Brain Res. Brain Res. Rev., 48, 112-128.
56. Rubin, J.E. & Terman, D. (2004) High frequency stimulation of the subthalamic nucleus eliminates pathological thalamic rhythmicity in a computational model. J. Comput. Neurosci., 16, 211-235.
57. Rudolph, U. & Antkowiak, B. (2004) Molecular and neuronal substrates for general anaesthetics. Nat. Rev. Neurosci., 5, 709-720.
58. Shi, L.-H., Luo, F., Woodward, D.J. & Chang, J.-Y. (2006) Basal ganglia neural responses during behaviorally effective deep brain stimulation of the subthalamic nucleus in rats performing a treadmill locomotion test. Synapse, 59, 445-457.
59. Surmeier, D.J., Mercer, J.N. & Chan, C.S. (2005) Autonomous pacemakers in the basal ganglia: who needs excitatory synapses anyway? Curr. Opin. Neurobiol., 15, 312-318.
60. Tai, C.-H., Boraud, T., Bezard, E., Bioulac, B., Gross, C. & Benazzouz, A. (2003) Electrophysiological and metabolic evidence that high-frequency stimulation of the subthalamic nucleus bridles neuronal activity in the subthalamic nucleus and the substantia nigra reticulata. FASEB J., 17, 1820-1830.
61. Volkmann, J., Herzog, J., Kopper, F. & Deuschl, G. (2002) Introduction to the programming of deep brain stimulators. Mov. Disord., 17(Suppl 3), S181-S187.
62. Windels, F., Bruet, N., Poupard, A., Urbain, N., Chouvet, G., Feuerstein, C. & Savasta, M. (2000) Effects of high frequency stimulation of subthalamic nucleus on extracellular glutamate and GABA in substantia nigra and globus pallidus in the normal rat. Eur. J. Neurosci., 12, 4141-4146.
63. Yamakura, T. & Harris, R.A. (2000) Effects of gaseous anesthetics nitrous oxide and xenon on ligand-gated ion channels. Comparison with isoflurane and ethanol. Anesthesiology, 93, 1095-1101.
64. Zhang, T.C. & Grill, W.M. (2010) Modeling deep brain stimulation: point source approximation versus realistic representation of the electrode. J. Neural Eng., 7, 066009.