Reduced GABA content in the motor thalamus during effective deep brain stimulation of the subthalamic nucleus

Frontiers in Systems Neuroscience

Volumn , Issue APRIL 2011, 2011, Pages

  Stefani, Alessandro ^a,b   Fedele, Ernesto ^c   Pierantozzi, Mariangela ^b   Galati, Salvatore ^d   Marzetti, Francesco ^b   Peppe, Antonella ^a   Pastore, Francesco Saverio ^b   Bernardi, Giorgio ^a,b   Stanzione, Paolo ^a,b  

^a IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^b UNIVERSITY OF ROME TOR VERGATA   (Italy)

^c UNIVERSITY OF GENOA   (Italy)

^d Neurocenter (EOC) of Southern Kingdom   (Switzerland)

Author keywords

Antero ventral thalamus; cGMP; GABA; Globus pallidus; Glutamate; Stereotactic neurosurgery; Subthalamus; UPDRS

Indexed keywords

4 AMINOBUTYRIC ACID; CYCLIC GMP;

ADULT; ANTERO VENTRAL THALAMUS; ARTICLE; BRAIN DEPTH STIMULATION; CLINICAL ARTICLE; GABAERGIC TRANSMISSION; GLOBUS PALLIDUS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; MICRODIALYSIS; NEUROSURGERY; NEUROTRANSMISSION; PARKINSON DISEASE; PUTAMEN; RADIOIMMUNOASSAY; SUBTHALAMIC NUCLEUS; THALAMUS;

EID: 82655175812     PISSN: 16625137     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnsys.2011.00017     Document Type: Article

References (46)

1. Agnesi, F., Tye, S. J., Bledsoe, J. M., Griessenauer, C. J., Kimble, C. J., Sieck, G. C., Bennet, K. E., Garris, P. A., Blaha, C. D., and Lee, K. H. (2009). Wireless instantaneous neurotransmitter concentration system-based amperomet-ric detection of dopamine, adenosine, and glutamate for intraoperative neu-rochemical monitoring. J. Neurosurg. 111, 701-711.
2. Albin, R. L., Young, A. B., and Penney, J. B. (1989). The functional anatomy of basal ganglia disorders. Trends Neurosci. 5, 366-375.
3. Anderson, M. E., Postupna, N., and Ruffo, M. (2003). Effects of high-frequency stimulation in the internal globus pallidus on the activity of thalamic neurons in the awake monkey. J. Neurophysiol. 89, 1150-1160.
4. Ashby, P., Paradiso, G., Saint-Cyr, J. A., Chen, R., Lang, A. E., and Lozano, A. M. (2001). Potentials recorded at the scalp by stimulation near the human subthalamic nucleus. Clin. Neurophysiol. 112, 431-437.
5. Benazzouz, A., Gao, D. M., Ni, Z. G., Piallat, B., Bouali-Benazzouz, R., and Benabid, A. L. (2000). Effect of high-frequency stimulation of the subthalamic nucleus on the neuronal activities of the sub-stantia nigra pars reticulata and vent-rolateral nucleus of the thalamus in the rat. Neuroscience 99, 289-295.
6. Blandini, F., Nappi, G., Tassorelli, C., and Martignoni, E. (2000). Functional changes of the basal ganglia circuitry in Parkinson's disease. Prog. Neurobiol. 62, 63-88.
7. Brown, P. (2003). Oscillatory nature of human basal ganglia activity: relationship to the pathophysiology of Parkinson's disease. Mov. Disord. 18, 357-363.
8. Covey, D. P., and Garris, P. A. (2009). Using fast-scan cyclic voltammetry to evaluate striatal dopamine release elicited by subthalamic nucleus stimulation. Conf. Proc. IEEE Eng. Med. Biol. Soc. 3306-3309.
9. DeLong, M. R. (1990). Primate models of movement disorders of basal ganglia origin. Trends Neurosci. 13, 281-285.
10. Ding, J. B., Guzman, J. N., Peterson, J. D., Goldberg, J. A., and Surmeier, D. J. (2010). Thalamic gating of corticostri-atal signaling by cholinergic interneu-rons. Neuron 67, 294-307.
11. Fedele, E., Mazzone, P., and Stefani, A. (2001). Microdialysis in Parkinsonian patient basal ganglia: acute apomor-phine-induced clinical and electro-physiological effects not paralleled by changes in the release of neuroac-tive amino acids. Exp. Neurol. 167, 356-365.
12. Fedele, E., and Raiteri, M. (1999). In vivo studies of the cerebral glutamate receptor/NO/cGMP pathway. Prog. Neurobiol. 58, 89-120.
13. Filali, M., Hutchison, W. D., Palter, V. N., Lozano, A. M., and Dostrovsky, J. O. (2004). Stimulation-induced inhibition of neuronal fring in human subthalamic nucleus. Exp. Brain Res. 156, 274-281.
14. Follett, K. A., Weaver, F. M., Stern, M., Hur, K., Harris, C. L., Luo, P., Marks, W. J., Rothlind, J., Sagher, O., Moy, C., Pahwa, R., Burchiel, K., Hogarth, P., Lai, E. C., Duda, J. E., Holloway, K., Samii, A., Horn, S., Bronstein, J. M., Stoner, G., Starr, P. A., Simpson, R., Baltuch, G., De Salles, A., Huang, G. D., and Reda, D. J. (2010). Pallidal versus subthalamic deep-brain stimulation for Parkinson's disease. N. Engl. J. Med. 362, 2077-2091.
15. Galati, S., D'Angelo, V., Olivola, E., Marzetti, F., Di Giovanni, G., Stanzione, P., and Stefani, A. (2010). Acute inactivation of the medial fore-brain bundle imposes oscillations in the SNr: a challenge for the 6-OHDA model? Exp. Neurol. 225, 294-301.
16. Galati, S., Mazzone, P., Fedele, E., Pisani, A., Peppe, A., and Pierantozzi, M. (2006). Biochemical and electrophysiological changes of substantia nigra pars reticu-lata driven by subthalamic stimulation in patients with Parkinson's disease. Eur. J. Neurosci. 23, 2923-2928.
17. Galati, S., Stanzione, P., D'Angelo, V., Fedele, E., Marzetti, F., Sancesario, G., Procopio, T., and Stefani, A. (2009). The pharmacological blockade of medial forebrain bundle induces an acute pathological synchronization of the cortico-subthalamic nucleus-globus pallidus pathway. J. Physiol. 587, 4405-4423.
18. Gradinaru, V., Mogri, M., Thompson K. R., Henderson, J. M., and Deisseroth, K. (2009). Optical deconstruction of Parkinsonian neural circuitry. Science 324, 354-359.
19. Guo, Y., Rubin, J. E., McIntyre, C. C., Vietk, J. L., and Terman, D. (2008). Thalamocortical relay fdelity varies across subthalamic nucleus deep brain stimulation protocols in a data-driven computational model. J. Neurophysiol. 99, 1477-1492.
20. Hahn, P. J., Russo, G. S., Hashimoto, T., Miocinovic, S., Xu, W., McIntyre, C. C., and Vitek, J. L. (2008). Pallidal burst activity during therapeutic deep brain stimulation. Exp. Neurol. 211, 243-251.
21. Hashimoto, T., Elder, C. M., Okun, M. S., Patrick, S. K., and Vitek, J. L. (2003). Stimulation of the subthalamic nucleus changes the firing pattern of pallidal neurons. J. Neurosci. 23, 1916-1923.
22. Hershey, T., Revilla, F. J., Wernle, A. R., McGee-Minnich, L., Antenor, J. V., and Videen, T. O. (2003). Cortical and subcortical blood fow effects of subthalamic nucleus stimulation in PD. Neurolog y 61, 816-821.
23. Hilker, R., Voges, J., Weisenbach, S., Kalbe, E., Burghaus, L., and Ghaemi, M. (2004). Subthalamic nucleus stimulation restores glucose metabolism in associative and limbic cortices and in cerebellum: evidence from a FDG-PET study in advanced Parkinson's disease. J. Cereb. Blood Flow Metab. 24, 7-16.
24. Hodaie, M., Cordella, R., Lozano, A. M., Wennberg, R., and Dostrovsky, J. O. (2006). Bursting activity of neurons in the human anterior thalamic nucleus. Brain Res. 1115, 1-8.
25. Johnson, M. D., Vitek, J. L., and McIntyre, C. C. (2009). Pallidal stimulation that improves Parkinsonian motor symptoms also modulates neuronal fring patterns in primary motor cortex in the MPTP-treated monkey. Exp. Neurol. 219, 359-362.
26. Kempf, F., Brücke, C., Salih, F., Trottenberg, T., Kupsch, A., and Schneider GH. (2009). Gamma activity and reactivity in human thalamic local feld potentials. Eur. J. Neurosci. 29, 943-953.
27. Kilpatrick, M., Church, E., Danish, S., Stiefel, M., Jaggi, J., and Halpern, C. (2010). Intracerebral microdialysis during deep brain stimulation surgery. J. Neurosci. Methods 190, 106-111.
28. Limousin, P., Greene, J., Pollak, P., Rothwell, J., Benabid, A. L., and Frackowiak, R. (1997). Changes in cerebral activity pattern due to sub-thalamic nucleus or internal pallidum stimulation in Parkinson's disease. Ann. Neurol. 42, 283-291.
29. Obeso, J. A., Rodríguez-Oroz, M. C., Benitez-Temino, B., Blesa, F. J., Guridi, J., and Marin, C. (2008). Functional organization of the basal ganglia: therapeutic implications for Parkinson's disease. Mov. Disord. 23, S548-S559.
30. Payoux, P., Remy, P., Damier, P., Miloudi, M., Loubinoux, I., Pidoux, B., Gaura, V., Rascol, O., Samson, Y., and Agid, Y. (2004). Subthalamic nucleus stimulation reduces abnormal motor cortical overactivity in Parkinson disease. Arch. Neurol. 61, 1307-1313.
31. Peppe, A., Pierantozzi, M., Bassi, A., Altibrandi, M. G., Brusa, L., Stefani, A., Stanzione, P., and Mazzone, P. (2004). Stimulation of the subtha-lamic nucleus compared with the globus pallidus internus in patients with Parkinson disease. J. Neurosurg. 101, 195-200.
32. Rubin, J. E., and Terman, D. (2004). High frequency stimulation of the subthalamic nucleus eliminates pathological tha-lamic rhythmicity in a computational model. J. Comput. Neurosci. 16, 211-235.
33. Shi, L. H., Luo, F., Woodward, D. J., and 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.
34. Stefani, A., Bassi, A., Mazzone, P., Pierantozzi, M., Gattoni, G., Altibrandi, M. G., Giacomini, P., Peppe, A., Bernardi, G., and Stanzione, P. (2002). Subdyskinetic apomorphine responses in globus pallidus and subthalamus of Parkinsonian patients: lack of clear evidence for the 'indirect pathway'. Clin. Neurophysiol. 113, 91-100.
35. Stefani, A., Fedele, E., Galati, S., Pepicelli, O., Frasca, S., and Pierantozzi, M. (2005). Subthalamic stimulation activates internal pallidus: evidence from cGMP microdialysis in PD patients. Ann. Neurol. 57, 448-452.
36. Stefani, A., Fedele, E., Galati, S., Raiteri, M., Pepicelli, O., and Brusa, L. (2006). Deep brain stimulation in Parkinson's disease patients: biochemical evidence. J. Neural Transm. 70, S401-S408.
37. Stefani, A., Fedele, E., Vitek, J., Pierantozzi, M., Galati, S., Marzetti, F., Peppe, A., Bernardi, G., and Stanzione, P. (2011). The clinical efficacy of l-dopa and STN-DBS share a common marker: reduced GABA content in the motor thalamus. Cell Death Dis. (in press).
38. Stefani, A., Lozano, A. M., Peppe, A., Stanzione, P., Galati, S., and Tropepi, D. (2007). Bilateral deep brain stimulation of the pedunculopontine and sub-thalamic nuclei in severe Parkinson's disease. Brain 130, 1596-1607.
39. Stefani, A., Mazzone, P., Bassi, A., Bernardi, G., Altibrandi, M. G., Peppe, A., Pierantozzi, M., and Stanzione, P. (1999). Electrophysiological and clinical desensitization to apomorphine administration in Parkinsonian patients undergoing stereotaxic neu-rosurgery. Exp. Neurol. 156, 209-213.
40. Stefani, A., Peppe, A., Pierantozzi, M., Galati, S., Moschella, V., and Stanzione, P. (2009). Multi-target strategy for Parkinsonian patients: the role of deep brain stimulation in the cen-tromedian-parafascicularis complex. Brain Res. Bull. 78, 113-118.
41. Stefani, A., Stanzione, P., Bassi, A., Mazzone, P., Vangelista, T., and Bernardi, G. (1997). Effects of increasing doses of apomorphine during stereotaxic neu-rosurgery in Parkinson's disease: clinical score and internal globus pallidus activity. J. Neural. Transm. 104, 895-904.
42. Urbano, F. J., Bisagno, V., Wikinski, S. I., Uchitel, O. D., and Llinás, R. R. (2009). Cocaine acute "binge" administration results in altered thalamocortical interactions in mice. Biol. Psychiatry 66, 769-776.
43. Van Gompel, J. J., Chang, S. Y., Goerss, S. J., Kim, I. Y., Kimble, C., Bennet, K. E., and Lee, K. H. (2010). Development of intraoperative electrochemical detection: wireless instantaneous neurochemical concentration sensor for deep brain stimulation feedback. Neurosurg. Focus 29, E6.
44. Windels, F., Bruet, N., Poupard, A., Feuerstein, C., Bertrand, A., and Savasta, M. (2003). Infuence of the frequency parameter on extracellular glutamate and gamma-aminobutyric acid in substantia nigra and globus pallidus during electrical stimulation of subthalamic nucleus in rats. J. Neurosci. Res. 72, 259-267.
45. Windels, F., Carcenac, C., Poupard, A., and Savasta, M. (2005). Pallidal origin of GABA release within the sub-stantia nigra pars reticulata during high-frequency stimulation of the subthalamic nucleus. J. Neurosci. 25, 5079-5086.
46. Xu, W., Russo, G. S., Hashimoto, T., Zhang, J., and Vitek, J. L. (2008). Subthalamic nucleus stimulation modulates tha-lamic neuronal activity. J. Neurosci. 28, 11916-11924.