C-Fos expression after deep brain stimulation of the pedunculopontine tegmental nucleus in the rat 6-hydroxydopamine Parkinson model

Journal of Chemical Neuroanatomy

Volumn 42, Issue 3, 2011, Pages 210-217

  Saryyeva, Assel ^a   Nakamura, Makoto ^a   Krauss, Joachim K ^a   Schwabe, Kerstin ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

Basal ganglia; Central gray; Motor activity

Indexed keywords

OXIDOPAMINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASAL GANGLION; BRAIN DEPTH STIMULATION; CENTRAL GRAY MATTER; CONTROLLED STUDY; DISEASE MODEL; ELECTRODE; GENE EXPRESSION; MALE; NERVE CELL; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; ONCOGENE C FOS; PARKINSON DISEASE; PEDUNCULOPONTINE TEGMENTAL NUCLEUS; PRIORITY JOURNAL; RAT; SHAM PROCEDURE; SPRAGUE DAWLEY RAT;

ANIMALS; BASAL GANGLIA; DEEP BRAIN STIMULATION; DISEASE MODELS, ANIMAL; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MOTOR ACTIVITY; NEURONS; OXIDOPAMINE; PARKINSONIAN DISORDERS; PEDUNCULOPONTINE TEGMENTAL NUCLEUS; PERIAQUEDUCTAL GRAY; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 80053132640     PISSN: 08910618     EISSN: 18736300     Source Type: Journal    
DOI: 10.1016/j.jchemneu.2011.08.003     Document Type: Article

References (76)

1. Alam M., Schwabe K., Krauss J.K. The pedunculopontine nucleus area: critical evaluation of interspecies differences relevant for its use as a target for deep brain stimulation. Brain 2011, 134:11-23.
2. Ainge J.A., Jenkins T.A., Winn P. Induction of c-fos in specific thalamic nuclei following stimulation of the pedunculopontine tegmental nucleus. Eur. J. Neurosci. 2004, 20:1827-1837.
3. Alderson H.L., Latimer M.P., Winn P. A functional dissociation of the anterior and posterior pedunculopontine tegmental nucleus: excitotoxic lesions have differential effects on locomotion and the response to nicotine. Brain Struct. Funct. 2008, 213:247-253.
4. Aravamuthan B.R., Bergstrom D.A., French R.A., Taylor J.J., Parr-Brownlie L.C., Walters J.R. Altered neuronal activity relationships between the pedunculopontine nucleus and motor cortex in a rodent model of Parkinson's disease. Exp. Neurol. 2008, 213:268-280.
5. Aziz T.Z., Stein J.F. Brainstem mechanisms of akinesia in the primate. J. Neurol. Neurosurg. Psychiatry 1997, 63-131.
6. Aziz T.Z., Davies L., Stein J., France S. The role of descending basal ganglia connections to the brain stem in parkinsonian akinesia. Br. J. Neurosurg. 1998, 12:245-249.
7. Ballanger B., Lozano A.M., Moro E., van E.T., Hamani C., Chen R., Cilia R., Houle S., Poon Y.Y., Lang A.E., Strafella A.P. Cerebral blood flow changes induced by pedunculopontine nucleus stimulation in patients with advanced Parkinson's disease: A [(15)O] H(2)O PET study. Hum. Brain Mapp. 2009.
8. Bandler R., Depaulis A., Vergnes M. Identification of midbrain neurones mediating defensive behaviour in the rat by microinjections of excitatory amino acids. Behav. Brain Res. 1985, 15:107-119.
9. Bandler R., Keay K.A., Floyd N., Price J. Central circuits mediating patterned autonomic activity during active vs. passive emotional coping. Brain Res. Bull. 2000, 53:95-104.
10. Benabid A.L., Chabardes S., Torres N., Piallat B., Krack P., Fraix V., Pollak P. Functional neurosurgery for movement disorders: a historical perspective. Prog. Brain Res. 2009, 175:379-391.
11. Boshuisen M.L., Ter Horst G.J., Paans A.M., Reinders A.A., den Boer J.A. rCBF differences between panic disorder patients and control subjects during anticipatory anxiety and rest. Biol. Psychiatry 2002, 52:126-135.
12. Brandao M.L., Cardoso S.H., Melo L.L., Motta V., Coimbra N.C. Neural substrate of defensive behavior in the midbrain tectum. Neurosci. Biobehav. Rev. 1994, 18:339-346.
13. Breit S., Bouali-Benazzouz R., Benabid A.L., Benazzouz A. Unilateral lesion of the nigrostriatal pathway induces an increase of neuronal activity of the pedunculopontine nucleus, which is reversed by the lesion of the subthalamic nucleus in the rat. Eur. J. Neurosci. 2001, 14:1833-1842.
14. Breit S., Lessmann L., Benazzouz A., Schulz J.B. Unilateral lesion of the pedunculopontine nucleus induces hyperactivity in the subthalamic nucleus and substantia nigra in the rat. Eur. J. Neurosci. 2005, 22:2283-2294.
15. Breit S., Lessmann L., Unterbrink D., Popa R.C., Gasser T., Schulz J.B. Lesion of the pedunculopontine nucleus reverses hyperactivity of the subthalamic nucleus and substantia nigra pars reticulata in a 6-hydroxydopamine rat model. Eur. J. Neurosci. 2006, 24:2275-2282.
16. Brown P. Bad oscillations in Parkinson's disease. J. Neural Transm. Suppl. 2006, 27-30.
17. Carrive P. The periaqueductal gray and defensive behavior: functional representation and neuronal organization. Behav. Brain Res. 1993, 58:27-47.
18. Dellu F., Mayo W., Cherkaoui J., Le M.M., Simon H. Learning disturbances following excitotoxic lesion of cholinergic pedunculo-pontine nucleus in the rat. Brain Res. 1991, 544:126-132.
19. Delong M.R., Wichmann T. Circuits and circuit disorders of the basal ganglia. Arch. Neurol. 2007, 64:20-24.
20. 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.
21. DeVito J.L., Anderson M.E., Walsh K.E. A horseradish peroxidase study of afferent connections of the globus pallidus in Macaca mulatta. Exp. Brain Res. 1980, 38:65-73.
22. Dragunov M., Faull R. The use of c-fos as a metabolic marker in neuronal pathway tracing. J. Neurosci. Methods 1989, 29:261-265.
23. Dybdal D., Gale K. Postural and anticonvulsant effects of inhibition of the rat subthalamic nucleus. J. Neurosci. 2000, 20:6728-6733.
24. Edley S.M., Graybiel A.M. The afferent and efferent connections of the feline nucleus tegmenti pedunculopontinus, pars compacta. J. Comp. Neurol. 1983, 217:187-215.
25. Ferraye M.U., Dbu B., Fraix V., Goetz L., Ardouin C., Henry-Lagrange C., Seigneuret E., Piallat B., Krack P., Le Bas J.F., Benabid A.L., Chabardes S., Pollak P. Effects of pedunculopontine nucleus area stimulation on gait disorders in Parkinson's disease. Brain 2010, 133:205-214.
26. Florio T., Scarnati E., Confalone G., Minchella D., Galati S., Stanzione P., Stefani A., Mazzone P. High-frequency stimulation of the subthalamic nucleus modulates the activity of pedunculopontine neurons through direct activation of excitatory fibres as well as through indirect activation of inhibitory pallidal fibres in the rat. Eur. J. Neurosci. 2007, 25:1174-1186.
27. Garcia-Rill E., Skinner R.D., Miyazato H., Homma Y. Pedunculopontine stimulation induces prolonged activation of pontine reticular neurons. Neuroscience 2001, 104:455-465.
28. Gerfen C.R., Staines W.A., Arbuthnott G.W., Fibiger H.C. Crossed connections of the substantia nigra in the rat. J. Comp. Neurol. 1982, 207:283-303.
29. Gomez-Gallego M., Fernandez-Villalba E., Fernandez-Barreiro A., Herrero M.T. Changes in the neuronal activity in the pedunculopontine nucleus in chronic MPTP-treated primates: an in situ hybridization study of cytochrome oxidase subunit I, choline acetyl transferase and substance P mRNA expression. J. Neural Transm. 2007, 114:319-326.
30. Graeff F.G. Neuroanatomy and neurotransmitter regulation of defensive behaviors and related emotions in mammals. Braz. J. Med. Biol. Res. 1994, 27:811-829.
31. Graeff F.G. Serotonin, the periaqueductal gray and panic. Neurosci. Biobehav. Rev. 2004, 28:239-259.
32. Gubellini P., Eusebio A., Ouselati A., Melin C., Kerkerian-Le Goff, Salin P. Chronic high-frequency stimulation of the subthalamic nucleus and L-DOPA treatment in experimental parkinsonism: effects on motor behaviour and striatal transmission. Eur. J. Neurosci. 2006, 24:1801-1814.
33. Gubellini P., Salin P., Kerkerian-Le Goff, Baunez C. Deep brain stimulation in neurological diseases and experimental models: from molecule to complex behaviour. Prog. Neurobiol. 2009, 89:79-123.
34. Hashimoto T., Elder C.M., Okun M.S., Patrick S.K., Vitek J.L. Stimulation of the subthalamic nucleus changes the firing pattern of pallidal neurons. J. Neurosci. 2003, 23:1916-1923.
35. Heise C.E., Mitrofanis J. Fos immunoreactivity in some locomotor neural centres of 6OHDA-lesioned rats. Anat. Embryol. (Berl) 2006, 211:659-671.
36. Herdegen T., Leah J.D. Inducible and constitutive transcription factors in the mammalian nervous system: control of gene expression by Jun, Fos and Krox, and CREB/ATF proteins. Brain Res. Brain Res. Rev. 1998, 28:370-490.
37. Hirsch E.C., Graybiel A.M., Duyckaerts C., Javoy-Agid F. Neuronal loss in the pedunculopontine tegmental nucleus in Parkinson disease and in progressive supranuclear palsy. Proc. Natl. Acad. Sci. U.S.A. 1987, 84:5976-5980.
38. Homs-Ormo S., Coll-Andreu M., Satorra-Marin N., revalo-Garcia R., Morgado-Bernal I. Effects of pedunculopontine tegmental nucleus lesions on emotional reactivity and locomotion in rats. Brain Res. Bull. 2003, 59:495-503.
39. Inglis W.L., Winn P. The pedunculopontine tegmental nucleus: where the striatum meets the reticular formation. Prog. Neurobiol. 1995, 47:1-29.
40. Jellinger K. The pedunculopontine nucleus in Parkinson's disease, progressive supranuclear palsy and Alzheimer's disease. J. Neurol. Neurosurg. Psychiatry 1988, 51:540-543.
41. Jenkinson N., Nandi D., Miall R.C., Stein J.F., Aziz T.Z. Pedunculopontine nucleus stimulation improves akinesia in a Parkinsonian monkey. Neuroreport 2004, 15:2621-2624.
42. Jeon M.F., Ha Y., Cho Y.H., Lee B.H., Park Y.G., Chang J.W. Effect of ipsilateral subthalamic nucleus lesioning in a rat parkinsonian model: study of behavior correlated with neuronal activity in the pedunculopontine nucleus. J. Neurosurg. 2003, 99:762-767.
43. Koch M., Kungel M., Herbert H. Cholinergic neurons in the pedunculopontine tegmental nucleus are involved in the mediation of prepulse inhibition of the acoustic startle response in the rat. Exp. Brain Res. 1993, 97:71-82.
44. Kovacs K.J. c-Fos as a transcription factor: a stressful (re) review from a functional map. Neurochem. Int. 1998, 33:287-297.
45. Kojima J., Yamaji Y., Matsumura M., Nambu A., Inase M., Tokuno H., Takada M., Imai H. Excitotoxic lesions of the pedunculopontine tegmental nucleus produce contralateral hemiparkinsonism in the monkey. Neurosci. Lett. 1997, 226:111-114.
46. Lee M.S., Rinne J.O., Marsden C.D. The pedunculopontine nucleus: its role in the genesis of movement disorders. Yonsei Med. J. 2000, 41:167-184.
47. Loher T.J., Burgunder J.M., Pohle T., Weber S., Sommerhalder R., Krauss J.K. Long-term pallidal deep brain stimulation in patients with advanced Parkinson disease: 1-year follow-up study. J. Neurosurg. 2002, 96:844-853.
48. Lozano A.M., Dostrovsky J., Chen R., Ashby P. Deep brain stimulation for Parkinson's disease: disrupting the disruption. Lancet Neurol. 2002, 1:225-231.
49. Matsumura M., Kojima J. The role of the pedunculopontine tegmental nucleus in experimental parkinsonism in primates. Stereotact. Funct. Neurosurg. 2001, 77:108-115.
50. Matsumura M., Nambu A., Yamaji Y., Watanabe K., Imai H., Inase M., Tokuno H., Takada M. Organization of somatic motor inputs from the frontal lobe to the pedunculopontine tegmental nucleus in the macaque monkey. Neuroscience 2000, 98:97-110.
51. Moro E., Hamani C., Poon Y.Y., Al-Khairrallah T., Dostrovsky J.O., Hutchison W.D., Lozano A.M. Unilateral pedunculopontine stimulation improves falls in Parkinson's disease. Brain 2010, 133:215-224.
52. Munro-Davies L.E., Winter J., Aziz T.Z., Stein J.F. The role of the pedunculopontine region in basal-ganglia mechanisms of akinesia. Exp. Brain Res. 1999, 129:511-517.
53. Murer M.G., Pazo J.H. Circling behaviour induced by activation of GABAA receptors in the subthalamic nucleus. Neuroreport 1993, 4:1219-1222.
54. Nandi D., Aziz T.Z., Giladi N., Winter J., Stein J.F. Reversal of akinesia in experimental parkinsonism by GABA antagonist microinjections in the pedunculopontine nucleus. Brain 2002, 125:2418-2430.
55. Nandi D., Jenkinson N., Stein J., Aziz T. The pedunculopontine nucleus in Parkinson's disease: primate studies. Br. J. Neurosurg. 2008, 22(Suppl. 1):S4-S8.
56. Oakman S.A., Faris P.L., Kerr P.E., Cozzari C., Hartmann B.K. Distribution of pontomesencephalic cholinergic neurons projecting to substantia nigra differs significantly from those projecting to ventral tegmental area. J. Neurosci. 1995, 15:5859-5869.
57. Olmstead M.C., Franklin K.B. Lesions of the pedunculopontine tegmental nucleus abolish catalepsy and locomotor depression induced by morphine. Brain Res. 1994, 662:134-140.
58. Pahapill P.A., Lozano A.M. The pedunculopontine nucleus and Parkinson's disease. Brain 2000, 123(Pt 9):1767-1783.
59. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 1998, Academic Press, San Diego, USA. 4th ed.
60. Plaha P., Gill S.S. Bilateral deep brain stimulation of the pedunculopontine nucleus for Parkinson's disease. Neuroreport 2005, 16:1883-1887.
61. Rauch F., Schwabe K., Krauss J.K. Effect of deep brain stimulation in the pedunculopontine nucleus on motor function in the rat 6-hydroxydopamine Parkinson model. Behav. Brain Res. 2010, 210:46-53.
62. Rinne J.O., Ma S.Y., Lee M.S., Collan Y., Roytta M. Loss of cholinergic neurons in the pedunculopontine nucleus in Parkinson's disease is related to disability of the patients. Parkinsonism. Relat. Disord. 2008, 14:553-557.
63. Rodriguez-Oroz M.C., Obeso J.A., Lang A.E., Houeto J.L., Pollak P., Rehncrona S., Kulisevsky J., Albanese A., Volkmann J., Hariz M.I., Quinn N.P., Speelman J.D., Guridi J., Zamarbide I., Gironell A., Molet J., Pascual-Sedano B., Pidoux B., Bonnet A.M., Agid Y., Xie J., Benabid A.L., Lozano A.M., Saint-Cyr J., Romito L., Contarino M.F., Scerrati M., Fraix V., Van B.N. Bilateral deep brain stimulation in Parkinson's disease: a multicentre study with 4 years follow-up. Brain 2005, 128:2240-2249.
64. Scarnati E., Di L.S., Proia A., Gallie G. The functional role of the pedunculopontine nucleus in the regulation of the electrical activity of entopeduncular neurons in the rat. Arch. Ital. Biol. 1988, 126:145-163.
65. Schenberg L.C., Bittencourt A.S., Sudre E.C., Vargas L.C. Modeling panic attacks. Neurosci. Biobehav. Rev. 2001, 25:647-659.
66. Schulte T., Brecht S., Herdegen T., Illert M., Mehdorn H.M., Hamel W. Induction of immediate early gene expression by high-frequency stimulation of the subthalamic nucleus in rats. Neuroscience 2006, 138:1377-1385.
67. Semba K., Fibiger H.C. Afferent connections of the laterodorsal and the pedunculopontine tegmental nuclei in the rat: a retro- and antero-grade transport and immunohistochemical study. J. Comp. Neurol. 1992, 323:387-410.
68. Stefani A., Lozano A.M., Peppe A., Stanzione P., Galati S., Tropepi D., Pierantozzi M., Brusa L., Scarnati E., Mazzone P. Bilateral deep brain stimulation of the pedunculopontine and subthalamic nuclei in severe Parkinson's disease. Brain 2007, 130:1596-1607.
69. Steiniger B., Kretschmer B.D. Effects of ibotenate pedunculopontine tegmental nucleus lesions on exploratory behaviour in the open field. Behav. Brain Res. 2004, 151:17-23.
70. Steininger T.L., Rye D.B., Wainer B.H. Afferent projections to the cholinergic pedunculopontine tegmental nucleus and adjacent midbrain extrapyramidal area in the albino rat. I. Retrograde tracing studies. J. Comp. Neurol. 1992, 321:515-543.
71. Takakusaki K., Oohinata-Sugimoto J., Saitoh K., Habaguchi T. Role of basal ganglia-brainstem systems in the control of postural muscle tone and locomotion. Prog. Brain Res. 2004, 143:231-237.
72. Takakusaki K., Tomita N., Yano M. Substrates for normal gait and pathophysiology of gait disturbances with respect to the basal ganglia dysfunction. J. Neurol. 2008, 255(Suppl. 4):19-29.
73. Temel Y., Visser Vanderwalle V., van der Wolf M., Spincemaille G.H., Desbonnet L., Hoogland G., Steinbusch H.W. Monopolar versus bipolar high frequency stimulation in the rat subthalamic nucleus: differences in histological damage. Neurosci. Lett. 2004, 367:92-96.
74. Trottenberg T., Kupsch A., Schneider G.H., Brown P., Kuhn A.A. Frequency-dependent distribution of local field potential activity within the subthalamic nucleus in Parkinson's disease. Exp. Neurol. 2007, 205:287-291.
75. Vitek J.L. Mechanisms of deep brain stimulation: excitation of inhibition. Mov. Disord. 2002, 17:69-72.
76. Zweig R.M., Jankel W.R., Hedreen J.C., Mayeux R., Price D.L. The pedunculopontine nucleus in Parkinson's disease. Ann. Neurol. 1989, 26:41-46.