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Stimulation for the compact parts of pedunculopontine nucleus: An available therapeutic approach in intractable epilepsy

2013; Elsevier BV; Volume: 29; Issue: 1 Linguagem: Inglês

10.1016/j.yebeh.2013.06.033

1525-5069

Taotao Liu, Jueping Feng, Huilian Bu, Cheng Liu, Xue-Hai Guan, Hong‐Bing Xiang,

EEG and Brain-Computer Interfaces

Many studies have shown that susceptibility to epilepsy is increased during nonrapid eye movement (NREM, slow-wave) sleep whereas rapid eye movement (REM) sleep suppresses seizure occurrence. Therefore, it is postulated that rapid eye movement sleep is a natural antiepileptogenic system in the body during the human wake–sleep cycle [1Jaseja H. Purpose of REM sleep: endogenous anti-epileptogenesis in man — a hypothesis.Med Hypotheses. 2004; 62: 546-548Abstract Full Text Full Text PDF PubMed Scopus (20) Google Scholar, 2Jaseja H. Pedunculopontine nucleus stimulation: a novel adjunctive therapeutic approach in intractable epilepsy.Epilepsy Behav. 2013; 27: 279Abstract Full Text Full Text PDF PubMed Scopus (11) Google Scholar, 3Matos G. Andersen M.L. do Valle A.C. Tufik S. The relationship between sleep and epilepsy: evidence from clinical trials and animal models.J Neurol Sci. 2010; 295: 1-7Abstract Full Text Full Text PDF PubMed Scopus (59) Google Scholar]. Because it is demonstrated that stimulation of the pedunculopontine tegmental nucleus (PPTg) can enhance REM sleep successfully [[4]Lim A.S. Moro E. Lozano A.M. Hamani C. Dostrovsky J.O. Hutchison W.D. et al.Selective enhancement of rapid eye movement sleep by deep brain stimulation of the human pons.Ann Neurol. 2009; 66: 110-114Crossref PubMed Scopus (89) Google Scholar], PPTg has been highlighted as a target for deep brain stimulation for seizure treatment of intractable epilepsy [2Jaseja H. Pedunculopontine nucleus stimulation: a novel adjunctive therapeutic approach in intractable epilepsy.Epilepsy Behav. 2013; 27: 279Abstract Full Text Full Text PDF PubMed Scopus (11) Google Scholar, 5Jaseja H. Pedunculopontine nucleus stimulation: potent therapeutic role in intractable epilepsy.Epilepsy Behav. 2013; 27: 280Abstract Full Text Full Text PDF PubMed Scopus (7) Google Scholar, 6Jaseja H. Pedunculopontine nucleus stimulation in intractable epilepsy: simulation of nature's antiepileptic role and mechanism.Epilepsy Behav. 2013; 27: 507Abstract Full Text Full Text PDF PubMed Scopus (9) Google Scholar]; however, the exact location of the optimal brain site for stimulation is not fully understood [7Lim S.N. Lee S.T. Tsai Y.T. Chen I.A. Tu P.H. Chen J.L. et al.Electrical stimulation of the anterior nucleus of the thalamus for intractable epilepsy: a long-term follow-up study.Epilepsia. 2007; 48: 342-347Crossref PubMed Scopus (172) Google Scholar, 8Vesper J. Steinhoff B. Rona S. Wille C. Bilic S. Nikkhah G. et al.Chronic high-frequency deep brain stimulation of the STN/SNr for progressive myoclonic epilepsy.Epilepsia. 2007; 48: 1984-1989Crossref PubMed Scopus (79) Google Scholar]. Recently, some studies have suggested that the neurons innervating motor structures are predominantly situated in the caudal parts of the PPTg, which divide into the dissipated part (dp) and compact part (cp) of the PPTg [9Geisler S. Derst C. Veh R.W. Zahm D.S. Glutamatergic afferents of the ventral tegmental area in the rat.J Neurosci. 2007; 27: 5730-5743Crossref PubMed Scopus (357) Google Scholar, 10Liu C. Ye D.W. Guan X.H. Li R.C. Xiang H.B. Zhu W.Z. Stimulation of the pedunculopontine tegmental nucleus may affect renal function by melanocortinergic signaling.Med Hypotheses. 2013; 81: 114-116Abstract Full Text Full Text PDF PubMed Scopus (23) Google Scholar, 11Xiang H.B. Liu C. Guo Q.Q. Li R.C. Ye D.W. Deep brain stimulation of the pedunculopontine tegmental nucleus may influence renal function.Med Hypotheses. 2011; 77: 1135-1138Abstract Full Text Full Text PDF PubMed Scopus (28) Google Scholar]. Nevertheless, it is still unclear whether cpPPTg or dpPPTg is tightly linked to motor projections. There is unequivocal agreement on the high and specific value of neurotropic pseudorabies virus (PRV) tracing for synaptic connectivity and neuroanatomical pathways in CNS by propagating retrogradely through chains of functionally connected neurons [11Xiang H.B. Liu C. Guo Q.Q. Li R.C. Ye D.W. Deep brain stimulation of the pedunculopontine tegmental nucleus may influence renal function.Med Hypotheses. 2011; 77: 1135-1138Abstract Full Text Full Text PDF PubMed Scopus (28) Google Scholar, 12Jovanovic K. Pastor A.M. O'Donovan M.J. The use of PRV-Bartha to define premotor inputs to lumbar motoneurons in the neonatal spinal cord of the mouse.PLoS One. 2010; 5: e11743Crossref PubMed Scopus (30) Google Scholar, 13Duale H. Hou S. Derbenev A.V. Smith B.N. Rabchevsky A.G. 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It is well known that PRV can provide a highly specific method of mapping the motor and sympathetic pathways innervating a variety of targets [12Jovanovic K. Pastor A.M. O'Donovan M.J. The use of PRV-Bartha to define premotor inputs to lumbar motoneurons in the neonatal spinal cord of the mouse.PLoS One. 2010; 5: e11743Crossref PubMed Scopus (30) Google Scholar, 17Stanley S. Pinto S. Segal J. Perez C.A. Viale A. DeFalco J. et al.Identification of neuronal subpopulations that project from hypothalamus to both liver and adipose tissue polysynaptically.Proc Natl Acad Sci U S A. 2010; 107: 7024-7029Crossref PubMed Scopus (133) Google Scholar, 18Lee T.K. Lois J.H. Troupe J.H. Wilson T.D. Yates B.J. Transneuronal tracing of neural pathways that regulate hindlimb muscle blood flow.Am J Physiol Regul Integr Comp Physiol. 2007; 292: R1532-R1541Crossref PubMed Scopus (40) Google Scholar, 19Xiang H.B. Zhu W.Z. Guan X.H. Ye D.W. 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Brainstem substrates of sympatho-motor circuitry identified using trans-synaptic tracing with pseudorabies virus recombinants.J Neurosci. 2003; 23: 4657-4666PubMed Google Scholar] mice by using retrograde tracing techniques of PRV-614, expressing a novel monomeric red fluorescent protein (mRFP1) under control of the cytomegalovirus immediate early promoter for direct visualization with the fluorescence microscope [22Glatzer N.R. Derbenev A.V. Banfield B.W. Smith B.N. Endomorphin-1 modulates intrinsic inhibition in the dorsal vagal complex.J Neurophysiol. 2007; 98: 1591-1599Crossref PubMed Scopus (44) Google Scholar, 23Willhite D.C. Nguyen K.T. Masurkar A.V. Greer C.A. Shepherd G.M. Chen W.R. Viral tracing identifies distributed columnar organization in the olfactory bulb.Proc Natl Acad Sci U S A. 2006; 103: 12592-12597Crossref PubMed Scopus (144) Google Scholar, 24Zhang Y. Kerman I.A. Laque A. Nguyen P. Faouzi M. Louis G.W. et al.Leptin-receptor-expressing neurons in the dorsomedial hypothalamus and median preoptic area regulate sympathetic brown adipose tissue circuits.J Neurosci. 2011; 31: 1873-1884Crossref PubMed Scopus (186) Google Scholar]. We found that injections of PRV-614 into the left gastrocnemius muscle labeled neurons in the cpPPTg and dpPPTg (Fig. 1), which was in line with a previous report showing that the PPTg control of the lumbar epaxial muscle produced a special posture by transneuronal tracer PRV-Bartha [[25]Daniels D. Miselis R.R. Flanagan-Cato L.M. Central neuronal circuit innervating the lordosis-producing muscles defined by transneuronal transport of pseudorabies virus.J Neurosci. 1999; 19: 2823-2833PubMed Google Scholar], suggesting that a direct neuronal circuit from the cpPPTg and dpPPTg to gastrocnemius muscle exists via the motor pathway. Otherwise, PRV-614/tyrosine hydroxylase (TH) and PRV-614/tryptophan hydroxylase (TPH) double-labeled neurons were detected in the dpPPTg and not in the cpPPTg (Fig. 1), which was in agreement with our previous immunohistochemical study in investigating that PRV-614/tryptophan hydroxylase and PRV-614/tyrosine hydroxylase double-labeled neurons in the cpPPTg were not detected after PRV-614 injection to the kidney [[11]Xiang H.B. Liu C. Guo Q.Q. Li R.C. Ye D.W. Deep brain stimulation of the pedunculopontine tegmental nucleus may influence renal function.Med Hypotheses. 2011; 77: 1135-1138Abstract Full Text Full Text PDF PubMed Scopus (28) Google Scholar], suggesting different neuronal populations present between the cpPPTg and the dpPPTg, and the functional integrity of synapses in the cpPPTg is not essential to serotonergic and catecholaminergic pathways. Because a subset of neurons that participate in regulating sympathetic outflow include serotonergic and catecholaminergic cells [17Stanley S. Pinto S. Segal J. Perez C.A. Viale A. DeFalco J. et al.Identification of neuronal subpopulations that project from hypothalamus to both liver and adipose tissue polysynaptically.Proc Natl Acad Sci U S A. 2010; 107: 7024-7029Crossref PubMed Scopus (133) Google Scholar, 26Xiang H.B. Zhu W.Z. Guan X.H. Ye D.W. Possible mechanism of deep brain stimulation for pedunculopontine nucleus-induced urinary incontinence: a virally mediated transsynaptic tracing study in a transgenic mouse model.Acta Neurochir. 2013; ([in press])Google Scholar], our data also provided a better understanding of the cpPPTg neural circuits involving ascending and descending motor projections. Based on these studies, the functional integrity of synapses in the cpPPTg is essential to motor projections. Therefore, this study highlights the potential use of exploring the compact parts of pedunculopontine nucleus stimulation as an available therapeutic approach in intractable epilepsy. Further investigation into the value of cpPPTg stimulation for intractable epilepsy is warranted. The work is original, and there is no conflict of interest to disclose. This work was supported by grants from the National Natural Science Foundation of PR China (No. 81271766 to H.X.), Special Fund of Fundamental Scientific Research Business Expense for Higher School of Central Government ( 2012 TS060 to H.X.), and 2010 Clinical Key Disciplines Construction Grant from the Ministry of Health of PR China .