The pedunculopontine tegmental nucleus: Implications for a role in modulating spinal cord motoneuron excitability

Journal of Neural Transmission

Volumn 118, Issue 10, 2011, Pages 1409-1421

  Scarnati, Eugenio ^a   Florio, Tiziana ^a   Capozzo, Annamaria ^a   Confalone, Giuseppina ^a   Mazzone, Paolo ^b  

^a UNIVERSITY OF L'AQUILA   (Italy)

^b CTO Hospital ASL Roma C   (Italy)

Author keywords

Deep brain stimulation; Dorsal root; H reflex; Parkinson's disease; Reticulospinal pathways; Superior colliculus; Ventral root

Indexed keywords

GLUCOSE;

ARTICLE; AUDITORY STIMULATION; BRAIN DEPTH STIMULATION; BRAIN MAPPING; BRAIN NUCLEUS; BRAIN STEM RESPONSE; CELL COUNT; CELL LOSS; CELLULAR DISTRIBUTION; CHOLINERGIC NERVE CELL; CHOLINERGIC TRANSMISSION; DORSAL ROOT; EVOKED MUSCLE RESPONSE; GLUCOSE BRAIN LEVEL; HINDLIMB; HOFFMANN REFLEX; HUMAN; MEDIAL LONGITUDINAL FASCICULUS; MUSCLE CONTRACTION; MUSCLE EXCITATION; NERVE CELL EXCITABILITY; NERVE STIMULATION; NEUROANATOMY; NEUROMODULATION; NISSL SUBSTANCE; NONHUMAN; PARKINSON DISEASE; PEDUNCULOPONTINE TEGMENTAL NUCLEUS; PERIPHERAL NERVE; PRIORITY JOURNAL; SPINAL CORD MOTONEURON; STRIATONIGRAL DEGENERATION; SUBNUCLEUS COMPACTUS; SUBNUCLEUS DISSIPATUS; VENTRAL ROOT; VOLUNTARY MOVEMENT;

ANIMALS; BRAIN MAPPING; DOPAMINE; ELECTRIC STIMULATION; H-REFLEX; HINDLIMB; HUMANS; NEURAL PATHWAYS; NEURONS; PEDUNCULOPONTINE TEGMENTAL NUCLEUS; SPINAL CORD;

EID: 80755163595     PISSN: 03009564     EISSN: 14351463     Source Type: Journal    
DOI: 10.1007/s00702-010-0532-2     Document Type: Article

References (93)

1. Alstermark B, Pinter MJ, Sasaki S (1992a) Descending pathways mediating disynaptic excitation of dorsal neck motoneurones in the cat: brain stem relay. Neurosci Res 15:42-57.
2. Alstermark B, Pinter MJ, Sasaki S (1992b) Tectal and tegmental excitation in dorsal neck motoneurones of the cat. J Physiol 454:517-532.
3. Ammari R, Lopez C, Bioulac B, Garcia L, Hammond C (2010) Subthalamic nucleus evokes similar long lasting glutamatergic excitations in pallidal, entopeduncular and nigral neurons in the basal ganglia slice. Neuroscience 166:808-818.
4. Angel RW, Hofmann WW(1963) The H reflex in normal, spastic, and rigid subjects. Arch Neurol 8:591-596.
5. Anglade P, Tsuji S, Agid Y, Hirsch EC (1995) Neuronal plasticity and Parkinson disease. Mol Chem Neuropathol 24:251-255.
6. Atsuta Y, Abraham P, Iwahara T, Garcia-Rill E, Skinner RD (1991) Control of locomotion in vitro: II. Chemical stimulation. Somatosens. Mot Res 8:55-63.
7. Baldissera F, Lundberg A, Udo M (1972) Activity evoked from the mesencephalic tegmentum in descending pathways other than the rubrospinal tract. Exp Brain Res 15:133-150.
8. Baldissera F, Di Loreto S, Florio T, Scarnati E (1994) Short-latency excitation of hindlimb motoneurons induced by electrical stimulation of the pontomesencephalic tegmentum in the rat. Neurosci Lett 169:13-16. (Pubitemid 24108852)
9. Bevan MD, Bolam JP (1995) Cholinergic, GABAergic, and glutamate- enriched inputs from the mesopontine tegmentum to the subthalamic nucleus in the rat. J Neurosci 15:7105-7120.
10. Bohnen NI, Muller ML, Koeppe RA, Studenski SA, Kilbourn MA, Frey KA, Albin RL (2009) History of falls in Parkinson disease is associated with reduced cholinergic activity. Neurology 73:1670-1676.
11. Braak H, Del Tredici K (2008) Cortico-basal ganglia-cortical circuitry in Parkinson's disease reconsidered. Exp Neurol 212:226-229.
12. Breit S, Bouali-Benazzouz R, Benabid AL, Benazzouz A (2001) 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 14:1833-1842. (Pubitemid 35469167)
13. Carlson JD, Pearlstein RD, Buchholz J, Iacono RP, Maeda G (1999) Regional metabolic changes in the pedunculopontine nucleus of unilateral 6-hydroxydopamine Parkinson's model rats. Brain Res 828:12-19. (Pubitemid 29236470)
14. Chung KA, Lobb BM, Nutt JG, Horak FB (2010) Effects of a central cholinesterase inhibitor on reducing falls in Parkinson disease. Neurology 75:1263-1269.
15. Delwaide PJ, Pepin JL, De Pasqua V, de Noordhout AM (2000) Projections from basal ganglia to tegmentum: a subcortical route for explaining the pathophysiology of Parkinson's disease signs? J Neurol 247(Suppl 2):II75-II81.
16. Ebert U, Koch M (1992) Glutamate receptors mediate acoustic input to the reticular brain stem. Neuroreport 3:429-432.
17. Ebert U, Ostwald J (1991) The mesencephalic locomotor region is activated during the auditory startle response of the unrestrained rat. Brain Res 565:209-217.
18. Edwards SB (1975) Autoradiographic studies of the projections of the midbrain reticular formation: descending projections of nucleus cuneiformis. J Comp Neurol 161:341-358.
19. Ferraye MU, Debu B, Fraix V, Goetz L, Ardouin C, Yelnik J, Henry- Lagrange C, Seigneuret E, Piallat B, Krack P, Le Bas JF, Benabid AL, Chabardes S, Pollak P (2010) Effects of pedunculopontine nucleus area stimulation on gait disorders in Parkinson's disease. Brain 133:205-214.
20. Florio T, Scarnati E, Confalone G, Minchella D, Galati S, Stanzione P, Stefani A, Mazzone P (2007) 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 25:1174-1186.
21. Futami T, Takakusaki K, Kitai ST (1995) Glutamatergic and cholinergic inputs from the pedunculopontine tegmental nucleus to dopamine neurons in the substantia nigra pars compacta. Neurosci Res 21:331-342.
22. Galati S, Scarnati E, Mazzone P, Stanzione P, Stefani A (2008) Deep brain stimulation promotes excitation and inhibition in subthalamic nucleus in Parkinson's disease. Neuroreport 19:661-666. (Pubitemid 351489364)
23. Garcia-Rill E, Skinner RD, Fitzgerald JA (1985) Chemical activation of the mesencephalic locomotor region. Brain Res 330:43-54. (Pubitemid 15143640)
24. Garcia-Rill E, Houser CR, Skinner RD, Smith W, Woodward DJ (1987) Locomotion-inducing sites in the vicinity of the pedunculopontine nucleus. Brain Res Bull 18:731-738. (Pubitemid 17118375)
25. Garcia-Rill E, Kinjo N, Atsuta Y, Ishikawa Y, Webber M, Skinner RD (1990) Posterior midbrain-induced locomotion. Brain Res Bull 24:499-508. (Pubitemid 20119439)
26. Garcia-Rill E, Skinner RD, Miyazato H, Homma Y (2001) Pedunculopontine stimulation induces prolonged activation of pontine reticular neurons. Neuroscience 104:455-465. (Pubitemid 32493736)
27. Goldsmith M, van der Kooy D (1988) Separate non-cholinergic descending projections and cholinergic ascending projections from the nucleus tegmenti pedunculopontinus. Brain Res 445:386-391. (Pubitemid 18085460)
28. Gomez-Gallego M, Fernandez-Villalba E, Fernandez-Barreiro A, Herrero MT (2007) 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 114:319-326. (Pubitemid 46328652)
29. Grantyn A, Grantyn R (1982) Axonal patterns and sites of termination of cat superior colliculus neurons projecting in the tecto-bulbospinal tract. Exp Brain Res 46:243-256. (Pubitemid 12092922)
30. Grillner S, Lund S (1968) The origin of a descending pathway with monosynaptic action on flexor motoneurones. Acta Physiol Scand 74:274-284.
31. Grofova I, Keane S (1991) Descending brainstem projections of the pedunculopontine tegmental nucleus in the rat. Anat Embryol (Berl) 184:275-290.
32. Hawkes CH, Del Tredici K, Braak H (2010) A timeline for Parkinson's disease. Parkinsonism Relat Disord 16:79-84.
33. Hiraoka K, Matuo Y, Iwata A, Onishi T, Abe K (2006) The effects of external cues on ankle control during gait initiation in Parkinson's disease. Parkinsonism Relat Disord 12:97-102. (Pubitemid 43234310)
34. Hirsch EC, Graybiel AM, Duyckaerts C, Javoy-Agid F (1987) Neuronal loss in the pedunculopontine tegmental nucleus in Parkinson disease and in progressive supranuclear palsy. Proc Natl Acad Sci USA 84:5976-5980. (Pubitemid 17135731)
35. Hoffmann P (1922) Untersuchungen uber die eigenreflexe (sehnenreflexe) menschlicher muskeln. Julius Springer, Berlin
36. Holstege JC, Kuypers HG (1982) Brain stem projections to spinal motoneuronal cell groups in rat studied by means of electron microscopy autoradiography. Prog Brain Res 57:177-183.
37. Homma Y, Skinner RD, Garcia-Rill E (2002) Effects of pedunculopontine nucleus (PPN) stimulation on caudal pontine reticular formation (PnC) neurons in vitro. J Neurophysiol 87:3033-3047. (Pubitemid 34670683)
38. Huerta MF, Harting JK (1982) Projections of the superior colliculus to the supraspinal nucleus and the cervical spinal cord gray of the cat. Brain Res 242:326-331. (Pubitemid 12048652)
39. Iwamoto Y (1990) Disynaptic tectal and pyramidal excitation of hindlimb motoneurons mediated by pontine reticulospinal neurons in the cat. Exp Brain Res 79:175-186. (Pubitemid 20040427)
40. Jellinger K (1988) The pedunculopontine nucleus in Parkinson's disease, progressive supranuclear palsy and Alzheimer's disease. J Neurol Neurosurg Psychiatry 51:540-543.
41. Jenkinson N, Nandi D, Oram R, Stein JF, Aziz TZ (2006) Pedunculopontine nucleus electric stimulation alleviates akinesia independently of dopaminergic mechanisms. Neuroreport 17:639-641.
42. Kang Y, Kitai ST (1990) Electrophysiological properties of pedunculopontine neurons and their postsynaptic responses following stimulation of substantia nigra reticulata. Brain Res 535:79-95.
43. Kelland MD, Asdourian D (1989) Pedunculopontine tegmental nucleus-induced inhibition of muscle activity in the rat. Behav Brain Res 34:213-234. (Pubitemid 19214769)
44. Kobayashi Y, Okada K (2009) Reward processing of the basal ganglia:reward function of pedunculopontine tegmental nucleus. Brain Nerve 61:397-404.
45. Kushnir M, Klein C, Rabey JM (2000) H reflex behavior in Parkinson's disease patients. Effect of stimulus duration. Parkinsonism Relat Disord 6:243-246. (Pubitemid 30438784)
46. Lavoie B, Parent A (1994) Pedunculopontine nucleus in the squirrel monkey: cholinergic and glutamatergic projections to the substantia nigra. J Comp Neurol 344:232-241. (Pubitemid 24151191)
47. Manaye KF, Zweig R, Wu D, Hersh LB, De Lacalle S, Saper CB, German DC (1999) Quantification of cholinergic and select noncholinergic mesopontine neuronal populations in the human brain. Neuroscience 89:759-770. (Pubitemid 29071002)
48. Mazzone P, Insola A, Sposato S, Scarnati E (2009) The deep brain stimulation of the pedunculopontine tegmental nucleus. Neuromodulation 12:191-204.
49. Mena-Segovia J, Sims HM, Magill PJ, Bolam JP (2008) Cholinergic brainstem neurons modulate cortical gamma activity during slow oscillations. J Physiol 586:2947-2960. (Pubitemid 351837287)
50. Mesulam MM, Mufson EJ, Wainer BH, Levey AI (1983) Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1-Ch6). Neuroscience 10:1185-1201. (Pubitemid 14178569)
51. Meunier S, Pol S, Houeto JL, Vidailhet M (2000) Abnormal reciprocal inhibition between antagonist muscles in Parkinson's disease. Brain 123(Pt 5):1017-1026. (Pubitemid 30224197)
52. Mitchell IJ, Clarke CE, Boyce S, Robertson RG, Peggs D, Sambrook MA, Crossman AR (1989) Neural mechanisms underlying parkinsonian symptoms based upon regional uptake of 2-deoxyglucose in monkeys exposed to 1-methyl-4-phenyl-1,2, 3,6-tetrahydropyridine. Neuroscience 32:213-226. (Pubitemid 19284718)
53. Miyazato H, Skinner RD, Reese NB, Mukawa J, Garcia-Rill E (1996) Midlatency auditory evoked potentials and the startle response in the rat. Neuroscience 75:289-300. (Pubitemid 26344621)
54. Moro E, Hamani C, Poon YY, Al Khairallah T, Dostrovsky JO, Hutchison WD, Lozano AM (2010) Unilateral pedunculopontine stimulation improves falls in Parkinson's disease. Brain 133:215-224.
55. Newmann DB (1985) Distinguishing rat brainstem reticulospinal nuclei and their morphology. II. Pontine and mesencephalic nuclei. J Hirnforsch 26:385-418.
56. Okada K, Kobayashi Y (2009) Characterization of oculomotor and visual activities in the primate pedunculopontine tegmental nucleus during visually guided saccade tasks. Eur J Neurosci 30:2211-2223.
57. Okada K, Toyama K, Inoue Y, Isa T, Kobayashi Y (2009) Different pedunculopontine tegmental neurons signal predicted and actual task rewards. J Neurosci 29:4858-4870.
58. Olszewski J, Baxter D (1982) Cytoarchitecture of the Human Brain Stem. Karger, Basel
59. Orieux G, Francois C, Feger J, Yelnik J, Vila M, Ruberg M, Agid Y, Hirsch EC (2000) Metabolic activity of excitatory parafascicular and pedunculopontine inputs to the subthalamic nucleus in a rat model of Parkinson's disease. Neuroscience 97:79-88. (Pubitemid 30195878)
60. Palombo E, Porrino LJ, Bankiewicz KS, Crane AM, Sokoloff L, Kopin IJ (1990) Local cerebral glucose utilization in monkeys with hemiparkinsonism induced by intracarotid infusion of the neurotoxin MPTP. J Neurosci 10:860-869. (Pubitemid 20104784)
61. Paxinos G, Huang XF (1995) Atlas of the human brainstem. Academic Press, San Diego
62. Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates, 2nd edn. Academic Press, Sydney
63. Peterson BW, Pitts NG, Fukushima K (1979) Reticulospinal connections with limb and axial motoneurons. Exp Brain Res 36:1-20. (Pubitemid 9215698)
64. Pierantozzi M, Palmieri MG, Galati S, Stanzione P, Peppe A, Tropepi D, Brusa L, Pisani A, Moschella V, Marciani MG, Mazzone P, Stefani A (2008) Pedunculopontine nucleus deep brain stimulation changes spinal cord excitability in Parkinson's disease patients. J Neural Transm 115:731-735.
65. Plenz D, Kital ST (1999) A basal ganglia pacemaker formed by the subthalamic nucleus and external globus pallidus. Nature 400:677-682.
66. Ransmayr G, Faucheux B, Nowakowski C, Kubis N, Federspiel S, Kaufmann W, Henin D, Hauw JJ, Agid Y, Hirsch EC (2000) Age-related changes of neuronal counts in the human pedunculopontine nucleus. Neurosci Lett 288:195-198. (Pubitemid 30411913)
67. Redgrave P, Dean P, Mitchell IJ, Odekunle A, Clark A (1988) The projection from superior colliculus to cuneiform area in the rat. I. Anatomical studies. Exp Brain Res 72:611-625.
68. Rinne JO, Ma SY, Lee MS, Collan Y, Roytta M (2008) Loss of cholinergic neurons in the pedunculopontine nucleus in Parkinson's disease is related to disability of the patients. Parkinsonism Relat Disord 14:553-557.
69. Robbins A, Schwartz-Giblin S, Pfaff DW (1990) Ascending and descending projections to medullary reticular formation sites which activate deep lumbar back muscles in the rat. Exp Brain Res 80:463-474. (Pubitemid 20197345)
70. Rye DB, Saper CB, Lee HJ, Wainer BH (1987) Pedunculopontine tegmental nucleus of the rat: cytoarchitecture, cytochemistry, and some extrapyramidal connections of the mesopontine tegmentum. J Comp Neurol 259:483-528. (Pubitemid 17076551)
71. Rye DB, Lee HJ, Saper CB, Wainer BH (1988) Medullary and spinal efferents of the pedunculopontine tegmental nucleus and adjacent mesopontine tegmentum in the rat. J Comp Neurol 269:315-341. (Pubitemid 18090001)
72. Satoh K (1979) The origin of reticulospinal fibers in the rat: a HRP study. J Hirnforsch 20:313-332. (Pubitemid 10211394)
73. Scarnati E, Campana E, Pacitti C (1984) Pedunculopontine-evoked excitation of substantia nigra neurons in the rat. Brain Res 304:351-361. (Pubitemid 14079943)
74. Schieppati M (1987) The Hofmann reflex: a mean of assessing spinal reflex excitability and its descending control in man. Prog Neurobiol 28:345-376.
75. Shammah-Lagnado SJ, Negrao N, Silva BA, Ricardo JA (1987) Afferent connections of the nuclei reticularis pontis oralis and caudalis: a horseradish peroxidase study in the rat. Neuroscience 20:961-989.
76. Shimamoto SA, Larson PS, Ostrem JL, Glass GA, Turner RS, Starr PA (2010) Physiological identification of the human pedunculopontine nucleus. J Neurol Neurosurg Psychiatry 81:80-86.
77. Simon C, Kezunovic N, Ye M, Hyde JR, Hayar A, Williams DK, Garcia-Rill E (2010) Gamma band unit activity and population responses in the pedunculopontine nucleus (PPN). J Neurophysiol 104:463-474.
78. Simonetta MM, Meunier S, Vidailhet M, Pol S, Galitzky M, Rascol O (2002) Transmission of group II heteronymous pathways is enhanced in rigid lower limb of de novo patients with Parkinson's disease. Brain 125:2125-2133.
79. Skinner RD, Kinjo N, Henderson V, Garcia-Rill E (1990a) Locomotor projections from the pedunculopontine nucleus to the spinal cord. Neuroreport 1:183-186.
80. Skinner RD, Kinjo N, Ishikawa Y, Biedermann JA, Garcia-Rill E (1990b) Locomotor projections from the pedunculopontine nucleus to the medioventral medulla. Neuroreport 1:207-210.
81. Spann BM, Grofova I (1989) Origin of ascending and spinal pathways from the nucleus tegmenti pedunculopontinus in the rat. J Comp Neurol 283:13-27. (Pubitemid 19130531)
82. Struppler A (1974) Elektromyographie der zentralen innervationsstorungen. In: Hops HC, Struppler A (eds) Reflexuntersuchungen. Thieme, Stuttgart, pp 166-200.
83. Takakusaki K, Shiroyama T, Yamamoto T, Kitai ST (1996) Cholinergic and noncholinergic tegmental pedunculopontine projection neurons in rats revealed by intracellular labeling. J Comp Neurol 371:345-361. (Pubitemid 26286587)
84. Takakusaki K, Shiroyama T, Kitai ST (1997) Two types of cholinergic neurons in the rat tegmental pedunculopontine nucleus: electrophysiological and morphological characterization. Neuroscience 79:1089-1109. (Pubitemid 27293760)
85. Takakusaki K, Habaguchi T, Ohtinata-Sugimoto J, Saitoh K, Sakamoto T (2003) Basal ganglia efferents to the brainstem centers controlling postural muscle tone and locomotion: a new concept for understanding motor disorders in basal ganglia dysfunction. Neuroscience 119:293-308. (Pubitemid 36577431)
86. Takakusaki K, Habaguchi T, Saitoh K, Kohyama J (2004) Changes in the excitability of hindlimb motoneurons during muscular atonia induced by stimulating the pedunculopontine tegmental nucleus in cats. Neuroscience 124:467-480. (Pubitemid 38229666)
87. Valls-Sole J (2000) Neurophysiological characterization of parkinsonian syndromes. Neurophysiol Clin 30:352-367. (Pubitemid 32009984)
88. Vincent SR, Satoh K, Armstrong DM, Fibiger HC (1983) NADPHdiaphorase: a selective histochemical marker for the cholinergic neurons of the pontine reticular formation. Neurosci Lett 43:31-36. (Pubitemid 14224425)
89. Wang HL, Morales M (2009) Pedunculopontine and laterodorsal tegmental nuclei contain distinct populations of cholinergic, glutamatergic and GABAergic neurons in the rat. Eur J Neurosci 29:340-358.
90. Weinberger M, Hamani C, Hutchison WD, Moro E, Lozano AM, Dostrovsky JO (2008) Pedunculopontine nucleus microelectrode recordings in movement disorder patients. Exp Brain Res 188:165-174.
91. Wichmann T, DeLong MR (1998) Models of basal ganglia function and pathophysiology of movement disorders. Neurosurg Clin N Am 9:223-236. (Pubitemid 28169298)
92. Woolf NJ, Butcher LL (1989) Cholinergic systems in the rat brain: IV. Descending projections of the pontomesencephalic tegmentum. Brain Res Bull 23:519-540. (Pubitemid 20035317)
93. Zweig RM, Jankel WR, Hedreen JC, Mayeux R, Price DL (1989) The pedunculopontine nucleus in Parkinson's disease. Ann Neurol 26:41-46. (Pubitemid 19190041)