The zona incerta modulates spontaneous spike-wave discharges in the rat

Journal of Neurophysiology

Volumn 109, Issue 10, 2013, Pages 2505-2516

  Shaw, Fu Zen ^a,b   Liao, Yi Fang ^c   Chen, Ruei Feng ^d   Huang, Yu Hsing ^a   Lin, Rick C S ^e  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^b NATIONAL CHIAO TUNG UNIVERSITY   (Taiwan)

^c TZU CHI UNIVERSITY   (Taiwan)

^d NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^e UNIVERSITY OF MISSISSIPPI MEDICAL CENTER   (United States)

Author keywords

Absence seizure; Deep brain stimulation; Spike wave discharge; Tremor; Zona incerta

Indexed keywords

LIDOCAINE; MUSCIMOL;

ANIMAL EXPERIMENT; ARTICLE; BRAIN DEPTH STIMULATION; CONTROLLED STUDY; FEMALE; MALE; MUSCLE CONTRACTION; NEUROMODULATION; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; RAT; SPIKE WAVE; VIBRISSA; ZONA INCERTA;

ABSENCE SEIZURE; DEEP BRAIN STIMULATION; SPIKE-WAVE DISCHARGE; TREMOR; ZONA INCERTA;

ACTION POTENTIALS; ANESTHETICS, LOCAL; ANIMALS; CEREBRAL CORTEX; ELECTRIC STIMULATION; GABA-A RECEPTOR AGONISTS; LIDOCAINE; MUSCIMOL; MUSCLE CONTRACTION; MUSCLE, SKELETAL; RATS; RATS, LONG-EVANS; SUBTHALAMUS; VIBRISSAE;

EID: 84878551549     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00750.2011     Document Type: Article

References (59)

1. Bai X, Guo J, Killory B, Vestal M, Berman R, Negishi M, Danielson N, Novotny EJ, Constable RT, Blumenfeld H. Resting functional connectivity between the hemispheres in childhood absence epilepsy. Neurology 76: 1960-1967, 2011.
2. Bartho P, Freund TF, Acsady L. Selective GABAergic innervation of thalamic nuclei from zona incerta. Eur J Neurosci 16: 999-1014, 2002.
3. Bartho P, Slezia A, Varga V, Bokor H, Pinault D, Buzsaki G, Acsady L. Cortical control of zona incerta. J Neurosci 27: 1670-1681, 2007.
4. Blumenfeld H. Cellular and network mechanisms of spike-wave seizures. Epilepsia 46(Suppl 9): 21-33, 2005.
5. Blumenfeld H, Klein JP, Schridde U, Vestal M, Rice T, Khera DS, Bashyal C, Giblin K, Paul-Laughinghouse C, Wang F, Phadke A, Mission J, Agarwal RK, Englot DJ, Motelow J, Nersesyan H, Waxman SG, Levin AR. Early treatment suppresses the development of spike-wave epilepsy in a rat model. Epilepsia 49: 400-409, 2008.
6. Bogacz J, Bogacz D, Bogacz A. Oculomotor phenomena in petit-mal. Clin Neurophysiol 111: 959-963, 2000.
7. Brudzynski SM, Cruickshank JW, McLachlan RS. Cholinergic mechanisms in generalized seizures: importance of the zona incerta. Can J Neurol Sci 22: 116-120, 1995.
8. Chen SD, Yeh KH, Huang YH, Shaw FZ. Effects of intracranial administration of ethosuximide in rats with spontaneous or pentylenetetrazol-induced spike-wave discharges. Epilepsia 52: 1311-1318, 2011.
9. Danober L, Deransart C, Depaulis A, Vergnes M, Marescaux C. Patho-physiological mechanisms of genetic absence epilepsy in the rat. Prog Neurobiol 55: 27-57, 1998.
10. Dybdal D, Gale K. Postural and anticonvulsant effects of inhibition of the rat subthalamic nucleus. J Neurosci 20: 6728-6733, 2000.
11. Fanselow EE, Sameshima K, Baccala A, Nicolelis MA. Thalamic bursting in rats during different awake behavioral states. Proc Natl Acad Sci USA 98: 15330-15335, 2001.
12. Fontanini A, Katz DB. 7 to 12 Hz activity in rat gustatory cortex reflects disengagement from a fluid self-administration task. J Neurophysiol 93: 2832-2840, 2005.
13. Garcia L, D'Alessandro G, Bioulac B, Hammond C. High-frequency stimulation in Parkinson's disease: more or less? Trends Neurosci 28: 209-216, 2005.
14. Guehl D, Vital A, Cuny E, Spampinato U, Rougier A, Bioulac B, Burbaud P. Postmortem proof of effectiveness of zona incerta stimulation in Parkinson disease. Neurology 70: 1489-1490, 2008.
15. Hamani C, Sakabe S, Bortolotto ZA, Cavalheiro EA, Mello LE. Inhibitory role of the zona incerta in the pilocarpine model of epilepsy. Epilepsy Res 49: 73-80, 2002.
16. Holmes MD, Brown M, Tucker DM. Are "generalized" seizures truly generalized? Evidence of localized mesial frontal and frontopolar discharges in absence. Epilepsia 45: 1568-1579, 2004.
17. Huang HY, Lee HW, Chen SD, Shaw FZ. Lamotrigine ameliorates seizures and psychiatric comorbidity in a rat model of spontaneous absence epilepsy. Epilepsia 53: 2005-2014, 2012.
18. Kim U, Gregory E, Hall WC. Pathway from zona incerta to the superior colliculus. J Comp Neurol 321: 555-575, 1992.
19. Lavallee P, Urbain N, Dufresne C, Bokor H, Acsady L, Deschenes M. Feedforward inhibitory control of sensory information in higher-order thalamic nuclei. J Neurosci 25: 7489-7498, 2005.
20. Liang SF, Liao YC, Shaw FZ, Chang DW, Young CP, Chiueh H. Closed-loop seizure control on epileptic rat models. J Neural Eng 8: 045001, 2011.
21. Lin CS, Nicolelis MA, Schneider JS, Chapin JK. A major direct GABAergic pathway from zona incerta to neocortex. Science 248: 1553-1556, 1990.
22. Liu Y, Postupna N, Falkenberg J, Anderson ME. High frequency deep brain stimulation: what are the therapeutic mechanisms? Neurosci Biobehav Rev 32: 343-351, 2008.
23. Manning JP, Richards DA, Leresche N, Crunelli V, Bowery NG. Cortical-area specific block of genetically determined absence seizures by ethosuximide. Neuroscience 123: 5-9, 2004.
24. Masri R, Quiton RL, Lucas JM, Murray PD, Thompson SM, Keller A. Zona incerta: a role in central pain. J Neurophysiol 102: 181-191, 2009.
25. Meeren HK, Pijn JP, Van Luijtelaar EL, Coenen AM, Lopes da Silva FH. Cortical focus drives widespread corticothalamic networks during spontaneous absence seizures in rats. J Neurosci 22: 1480-1495, 2002.
26. Mitrofanis J. Some certainty for the "zone of uncertainty"? Exploring the function of the zona incerta. Neuroscience 130: 1-15, 2005.
27. Nandi D, Chir M, Liu X, Bain P, Parkin S, Joint C, Winter J, Stein J, Scott R, Gregory R, Aziz T. Electrophysiological confirmation of the zona incerta as a target for surgical treatment of disabling involuntary arm movements in multiple sclerosis: use of local field potentials. J Clin Neurosci 9: 64-68, 2002.
28. Nicolelis MA, Baccala LA, Lin RC, Chapin JK. Sensorimotor encoding by synchronous neural ensemble activity at multiple levels of the somatosensory system. Science 268: 1353-1358, 1995.
29. Nicolelis MA, Chapin JK, Lin RC. Somatotopic maps within the zona incerta relay parallel GABAergic somatosensory pathways to the neocortex, superior colliculus, and brain stem. Brain Res 577: 134-141, 1992.
30. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates (2nd ed.). New York: Academic, 1986.
31. Périer C, Tremblay L, Féger J, Hirsch EC. Behavioral consequences of bicuculline injection in the subthalamic nucleus and the zona incerta in rat. J Neurosci 22: 8711-8719, 2002.
32. Pfurtscheller G. Induced oscillations in the alpha band: functional meaning. Epilepsia 44: 2-8, 2003.
33. Pinault D, Slezia A, Acsady L. Corticothalamic 5-9 Hz oscillations are more pro-epileptogenic than sleep spindles in rats. J Physiol 574: 209-227, 2006.
34. Plaha P, Ben-Shlomo Y, Patel NK, Gill SS. Stimulation of the caudal zona incerta is superior to stimulation of the subthalamic nucleus in improving contralateral parkinsonism. Brain 129: 1732-1747, 2006.
35. Polack PO, Charpier S. Intracellular activity of cortical and thalamic neurons during high-voltage rhythmic spike discharge in Long-Evans rats in vivo. J Physiol 571: 461-476, 2006.
36. Polack PO, Guillemain I, Hu E, Deransart C, Depaulis A, Charpier S. Deep layer somatosensory cortical neurons initiate spike-and-wave discharges in a genetic model of absence seizures. J Neurosci 27: 6590-6599, 2007.
37. Richards DA, Manning JP, Barnes D, Romdola L, Bowery NG, Caccia S, Leresche N, Crunelli V. Targeting thalamic nuclei is not sufficient for the full anti-absence action of ethosuximide in a rat model of absence epilepsy. Epilepsy Res 54: 97-107, 2003.
38. Semba K, Komisaruk BR. Neural substrates of two different rhythmical vibrissal movements in the rat. Neuroscience 12: 761-774, 1984.
39. Shaw FZ. 7-12 Hz high-voltage rhythmic spike discharges in rats evaluated by antiepileptic drugs and flicker stimulation. J Neurophysiol 97: 238-247, 2007.
40. Shaw FZ. Is spontaneous high-voltage rhythmic spike discharge in Long Evans rats an absence-like seizure activity? J Neurophysiol 91: 63-77, 2004.
41. Shaw FZ, Chuang SH, Shieh KR, Wang YJ. Depression-and anxiety-like behaviors of a rat model with absence epileptic discharges. Neuroscience 160: 382-393, 2009.
42. Shaw FZ, Lai CJ, Chiu TH. A low-noise flexible integrated system for recording and analysis of multiple electrical signals during sleep-wake states in rats. J Neurosci Methods 118: 77-87, 2002.
43. Shaw FZ, Lee SY, Chiu TH. Modulation of somatosensory evoked potential during wake-sleep states and spike-wave discharge in the rat. Sleep 29: 285-293, 2006.
44. Shaw FZ, Liao YF. Relation between activities of the cortex and vibrissae muscle during high-voltage rhythmic spike discharges in rats. J Neurophysiol 93: 2435-2448, 2005.
45. Shaw FZ, Yen CT, Chen RF. A simple and effective process for noise reduction of multichannel cortical field potential recordings in freely moving rats. J Neurosci Methods 124: 167-174, 2003.
46. Snead OC 3rd, Depaulis A, Vergnes M, Marescaux C. Absence epilepsy: advances in experimental animal models. Adv Neurol 79: 253-278, 1999.
47. Steriade M, Parent A, Ropert N, Kitsikis A. Zona incerta and lateral hypothalamic afferents to the midbrain reticular core of cat-HRP and electrophysiological study. Brain Res 238: 13-28, 1982.
48. Supko DE, Uretsky NJ, Wallace LJ. Activation of AMPA/kanic acid glutamate receptors in the zona incerta stimulates locomotor activity. Brain Res 564: 159-163, 1991.
49. Supko DE, Uretsky NJ, Wallace LJ. AMPA/kanic acid glutamate receptor antagonism in the zona incerta dorsal to the subthalamic nucleus inhibits amphetamine-induced stereotypy but not locomotor activity. Brain Res 576: 89-96, 1992.
50. Theodore WH, Fisher RS. Brain stimulation for epilepsy. Lancet Neurol 3: 111-118, 2004.
51. Timofeev I, Steriade M. Neocortical seizures: initiation, development and cessation. Neuroscience 123: 299-336, 2004.
52. Tort AB, Fontanini A, Kramer MA, Jones-Lush LM, Kopell NJ. Cortical networks produce three distinct 7-12 Hz rhythms during single sensory responses in the awake rat. J Neurosci 30: 4315-4324, 2010.
53. Urbain N, Deschenes M. Motor cortex gates vibrissal responses in a thalamo-cortical projection pathway. Neuron 56: 714-725, 2007.
54. van Luijtelaar G, Sitnikova E. Global and focal aspects of absence epilepsy: the contribution of genetic models. Neurosci Biobehav Rev 30: 983-1003, 2006.
55. Vercueil L, Benazzouz A, Deransart C, Bressand K, Marescaux C, Depaulis A, Benabid AL. High-frequency stimulation of the sub-thalamic nucleus suppresses absence seizures in the rat: comparison with neurotoxic lesions. Epilepsy Res 31: 39-46, 1998.
56. Voges J, Volkmann J, Allert N, Lehrke R, Koulousakis A, Freund HJ, Sturm V. Bilateral high-frequency stimulation in the subthalamic nucleus for the treatment of Parkinson disease: correlation of therapeutic effect with anatomical electrode position. J Neurosurg 96: 269-279, 2002.
57. Westmijse I, Ossenblok P, Gunning B, van Luijtelaar G. Onset and propagation of spike and slow wave discharges in human absence epilepsy: a MEG study. Epilepsia 50: 2538-2548, 2009.
58. Wiest MC, Nicolelis MA. Behavioral detection of tactile stimuli during 7-12 Hz cortical oscillations in awake rats. Nat Neurosci 6: 913-914, 2003.
59. Young CP, Liang SF, Chang DW, Liao YC, Shaw FZ, Hsieh CH. A portable wireless on-line closed-loop seizure controller in freely moving rats. IEEE Trans Instrum Meas 60: 513-521, 2011.