Glutamatergic and cholinergic pedunculopontine neurons innervate the thalamic parafascicular nucleus in rats: Changes following experimental parkinsonism

Brain Structure and Function

Volumn 216, Issue 4, 2011, Pages 319-330

  Barroso Chinea, Pedro ^a   Rico, Alberto J ^a   Conte Perales, Lorena ^a   Gómez Bautista, Virginia ^a   Luquin, Natasha ^a   Sierra, Salvador ^a   Roda, Elvira ^a   Lanciego, José L ^a  

^a UNIVERSITY OF NAVARRA   (Spain)

Author keywords

Basal ganglia; ChA.T.; Glut; Glutamate; Parkinson's disease; PPTg

Indexed keywords

VESICULAR GLUTAMATE TRANSPORTER 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; DENERVATION; DOPAMINERGIC SYSTEM; GENE EXPRESSION; GLUTAMATERGIC NERVE CELL; INNERVATION; MALE; NERVE CELL; NERVE PROJECTION; NEUROTRANSMISSION; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; NUCLEOTIDE SEQUENCE; PARKINSONISM; PEDUNCULOPONTINE TEGMENTAL NUCLEUS; PRIORITY JOURNAL; RAT; SENSORY NERVE; THALAMUS PARAFASCICULAR NUCLEUS;

ANIMALS; CHOLINERGIC NEURONS; DNA PRIMERS; GLUTAMIC ACID; HISTOLOGICAL TECHNIQUES; IMMUNOENZYME TECHNIQUES; IN SITU HYBRIDIZATION, FLUORESCENCE; INTRALAMINAR THALAMIC NUCLEI; MICRODISSECTION; NEURONS, EFFERENT; PARKINSONIAN DISORDERS; PEDUNCULOPONTINE TEGMENTAL NUCLEUS; POLYMERASE CHAIN REACTION; RATS; RNA, MESSENGER; STILBAMIDINES; VESICULAR GLUTAMATE TRANSPORT PROTEIN 2;

PARKINSONIA; RATTUS;

EID: 84655176491     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-011-0317-x     Document Type: Article

References (66)

1. Albin RL, Young AB, Penney JB (1989) The functional anatomy of basal ganglia disorders. Trends Neurosci 12:366-375 (Pubitemid 19238787)
2. Aymerich MS, Barroso-Chinea P, Pérez-Manso M, Muñoz- Patiño AM, Moreno-Igoa M, González-Hernández T, Lanciego JL (2006) Consequences of unilateral nigrostriatal denervation on the thalamostriatal pathway in rats. Eur J Neurosci 23:2009-2108
3. Aziz TZ, Davies L, Stein J, France S (1998) The role of descending basal ganglia connections to the brain stem in parkinsonian akinesia. Br J Neurosurg 12:245-249 (Pubitemid 28287242)
4. Bacci JJ, Kachidian P, Kerkerian-Le Goff L, Salin P (2004) Intralaminar thalamic nuclei lesions: Widespread impact on dopamine denervation-mediated cellular defects in the rat basal ganglia. J Neuropathol Exp Neurol 63:20-31 (Pubitemid 38030230)
5. Blanco-Lezcano L, Rocha-Arrieta LL, Alvarez-González L, Martí- nez-Martí L, Pavón-Fuentes N, González- Fraguela ME, Bauzá- Calderín Y, Coro-Grave de Peralta Y (2005) The effects of lesions in the compact parto f the substantia nigra on glutamate and GABA release in the pedunculopontine nucleus. Rev Neurol 40:23-29 (Pubitemid 41295373)
6. Breit S, Bouali-Benazzouz R, Benabid AL, Benazzouz A (2001) Unilateral lesion of the nigrostriatal pathway induces an increase on 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)
7. Breit S, Lessmann L, Unterbrink D, Popa RC, Gasser T, Schulz JB (2006) Lesion of the pedunculopontine nucleus reverseshyperactivity of the subthalamic nucleus and substantia nigra pars reticulata in a 6-hydroxydopamine rat model. Eur J Neurosci 24:2275-2282 (Pubitemid 44622348)
8. Breit S, Martin A, Lessmann L, Cerkez D, Gasser T, Schulz JB (2008) Bilateral changes in neuronal activity of the basal ganglia in the unilateral 6-hydroxydopamine rat model. J Neurosci Res 86:1388-1396 (Pubitemid 351571913)
9. Caparrós-Lefebvre D, Ruchoux MM, Blond D, Petit H, Percheron G (1994) Long-term thalamic stimulation in Parkinson's disease: Postmortem anatomoclinical study. Neurology 44:1856-1860 (Pubitemid 24319210)
10. Caparrós-Lefebvre D, Blond S, Feltin MP, Pollak P, Benabid AL (1999) Improvement of levodopa induced dyskinesias by thalamic deep brain stimulation is related to slight variations in electrode placement: Possible involvement of the centre median parafascicularis complex. J Neurol Neurosurg Pshychiatr 67:308-314 (Pubitemid 29392589)
11. Capozzo A, Florio T, Cellini R, Moriconi U, Scarnati E (2003) The pedunculopontine nucleus projectin to the parafascicular nucleus of the thalamus: An electrophysiological investigation in the rat. J Neural Transm 110:733-747 (Pubitemid 36783227)
12. Carlson JD, Pearlstein RD, Bucholz J, Iacono RP, Maoda G (1999) Regional metabolic changes in the pedunculopontine nucleus of unilateral 6-hydroxydopamine Parkinson's model rats. Brain Res 828:12-19 (Pubitemid 29236470)
13. Clements JR, Grant S (1990) Glutamate-like immunoreactivity in neurons of the laterodorsal tegmental and pedunculopontine nuclei in the rat. Neurosci Lett 120:70-73
14. Cornwall J, Phillipson OT (1988) Afferent projections to the parafascicular thalamic nucleus of the rat, as shown by the retrograde transport of wheat germ agglutinin. Brain Res Bull 20:139-150 (Pubitemid 19017199)
15. Crossman AR (1987) Primate models of dyskinesia: The experimental approach in the study of basal ganglia-related involuntary movement disorders. Neuroscience 21:1-40 (Pubitemid 17076862)
16. DeLong MR (1990) Primate models of movement disorders of basal ganglia origin. Trends Neurosci 13:266-271
17. Dun NJ, Dun SL, Hwang LL, Fostermann U (1995) Infrequent coexistence of nitric oxide synthase and parvalbumin, calbindin and calretinin immunoreactivity in rat pontine neurons. Neurosci Lett 191:165-168
18. Erro E, Lanciego JL, Giménez-Amaya JM (1999) Relationships between thalamostriatal neurons and pedunculopontine projections to the thalamus: A neuroanatomical tract-tracing study in the rat. Exp Brain Res 127:162-170 (Pubitemid 29313128)
19. Ford B, Holmes CJ, Mainville L, Jones BE (1995) GABAergic neurons in the rat pontomesencephalic tegmentum: Codistribution with cholinergic and other tegmental neurons projecting to the posterior lateral hypothalamus. J Comp Neurol 363:177-196
20. García-Rill E, Biedermann JA, Chambers T, Skinner RD, Mrak RE, Husain M, Karson CN (1995) Mesopontine neurons in schizophrenia. Neuroscience 66:321-335
21. Geula C, Schatz CR, Mesulam MM (1993) Differential localization of NADPH-diaphorase and calbindin-D28 k within the cholinergic neurons in the basal forebrain, striatum and brainstem in the rat, monkey, baboon and human. Neuroscience 54:461-476 (Pubitemid 23153755)
22. Gonzalo N, Lanciego JL, Castle M, Vázquez A, Erro E, Obeso JA (2002) The parafascicular thalamic complex and basal ganglia circuitry: Further complexity to the basal ganglia model. Thalamus Relat Sys 1:341-348 (Pubitemid 351479957)
23. Groenewegen HJ, Berendse HW, Haber SN (1993) Organization of the output of the ventral striatopallidal system in the rat: Ventral pallidal efferents. Neuroscience 57:113-142 (Pubitemid 23325638)
24. Hallanger AE, Wainer BH (1988) Ascending projections from the pedunculopontine tegmental nucleus and the adjacent mesopontine tegmentum in the rat. J Comp Neurol 274:483-515
25. Hallanger AE, Levey AI, Lee HJ, Rye DB, Wainer BH (1987) The origins of cholinergic and other subcortical afferents to the thalamus in the rat. J Comp Neurol 262:105-124 (Pubitemid 17106949)
26. Isaacson LG, Tanaka D Jr (1986) Cholinergic and non-cholinergic projections from the canine pontomesencephalic tegmentum (Ch5 area) to the caudal intralaminar nuclei. Exp Brain Res 62:179-188 (Pubitemid 16162074)
27. Jackson A, Crossman AR (1983) Nucleus tegmenti pedunculopontininus: Efferent connections with special referente to the basal ganglia, studied in the rat by anterograde and retrograde transporto f horseradish peroxidase. Neuroscience 10:725-765 (Pubitemid 14097182)
28. Jenkinson N, Nandi D, Miall RC, Stein JF, Aziz TZ (2004) Pedunculopontine nucleus stimulation improves akinesia in a parkinsonian monkey. NeuroReport 15:2621-2624 (Pubitemid 40053949)
29. Jenkinson N, Nandi D, Aziz TZ, Stein JF (2005) Pedunculopontine nucleus: A new target for deep brain stimulation for akinesia. NeuroReport 16:1875-1876 (Pubitemid 41653505)
30. Jia HG, Yamuy J, Sampogna S, Morales FR, Chase MH (2003) Colocalization of gamma-aminobutyric acid and acetylcholine in neurons in the laterodorsal and pedunculopontine tegmental nuclei in the cat: A Light and electron microscopic study. Brain Res 992:205-219 (Pubitemid 37415103)
31. Jones EG (1991) Paradoxical sleep and its chemical/structural substrates in the brain. Neuroscience 40:637-656
32. Kobayashi S, Nakamura Y (2003) Synaptic organization of the rat parafascicular nucleus, with special reference to its afferents from the superior colliculus and the pedunculopontine tegmental nucleus. Brain Res 980:80-91 (Pubitemid 36836116)
33. Kobayashi S, Hoshino K, Homma S, Takagi S, Norita M (2007) A possible monosynaptic pathways links the pedunculopontine nucleus to thalamostriatal neurons in the hooded rat. Arch Histol Cytol 70:207-214 (Pubitemid 350224156)
34. Kojima J, Yamaji Y, Matsumara M, Nambu A, Inase M, Tokuno H, Takada M, Imai H (1997) Excitotoxic lesions of the pedunculopontine tegmental nucleus produce contralatral hemiparkinsonism in the monkey. Neurosci Lett 226:111-114 (Pubitemid 27190418)
35. Krauss JK, Pohle T, Weigel R, Burgunder JM (2002) Deep brain stimulation of the centre median-parafascicular complex in patients with movement disorders. J Neurol Neurosurg Psychiatr 72:546-548
36. Krout KE, Belzer RE, Loewy AD (2002) Brainstem projections to midline and intralaminar thalamic nuclei of the rat. J Comp Neurol 448:53-101 (Pubitemid 34507499)
37. Lanciego JL, Rodríguez-Oroz MC, Blesa FJ, Alvarez-Erviti L, Guridi J, Barroso-Chinea P, Smith Y, Obeso JA (2008) Lesion of the centromedian thalamic nucleus in MPTP-treated primates. Mov Disord 23:708-715
38. Lavoie B, Parent A (1994) Pedunculopontine nucleus in the squirrel monkey: Projections to the basal ganglia as revealed by anterograde tract-tracing methods. J Comp Neurol 344:210-231 (Pubitemid 24151190)
39. Martínez-González C, Bolam JP, Mena-Segovia J (2011) Topographical organization of the pedunculopontine nucleus. Frontiers Neuroanat. doi:10.3389/fnana.2011.00022
40. Mazzone P, Lozano A, Stnzione P, Galati S, Scarnati E, Peppe A, Stefani A (2005) Implantation of human pedunculopontine nucleus: A safe and clinically relevant target in Parkinson's disease. NeuroReport 16:1877-1881 (Pubitemid 41653506)
41. Mena-Segovia J, Micklem BR, Nair-Roberts RG, Ungless MA, Bolam JP (2009) GABAergic neuron distribution in the pedunculopontine nucleus defines functional subterritories. J Comp Neurol 515:397-408
42. Mesulam MM, Mufson EJ, Wainer BH, Levey AI (1983) Central cholinergic pathways in the rat: An overview based on alternative nomenclature (Ch1-Ch6). Neuroscience 10:1185-1201 (Pubitemid 14178569)
43. Moriizumi T, Hattori T (1992) Separate neuronal populations of the rat globus pallidus projecting to the subthalamic nucleus, auditory cortex and pedunculopontine tegmental area. Neuroscience 46:701-710
44. Munro-Davis LE, Winter J, Aziz TZ, Stein JF (1999) The role of the pedunculopontine region in basal-ganglia mechanisms of akinesia. Exp Brain Res 129:511-517
45. Nandi D, Aziz TZ, Giladi N, Winter J, Stein JF (2002a) Reversal of akinesia in experimental parkinsonism by GABA antagonist microinjections in the pedunculopontine nucleus. Brain 125:2418-2430 (Pubitemid 35303502)
46. Nandi D, Liu X, Winter JL, Aziz TZ, Stein JF (2002b) Deep brain stimulation of the pedunculopontine region in the normal nonhuman primate. J Clin Neurosci 9:170-174 (Pubitemid 34464589)
47. Oakman SA, Faris PL, Cozzari C, Hartman BK (1999) Characterization of the extent of pontomesencephalic cholinergic neurons' projections to the thalamus: Comparison with projections to midbrain dopaminergic groups. Neuroscience 94:529-547 (Pubitemid 29436079)
48. Orieux G, François C, Féger J, Yelnik J, Vila M, Ruberg G, 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)
49. Pahapill PA, Lozano AM (2000) The pedunculopontine nucleus and Parkinson's disease. Brain 123:1767-1783 (Pubitemid 30664282)
50. Parent M, Descarries L (2008) Acetylcholine innervation of the adult rat thalamus: Distribution and ultrastructural features in dorsolateral geniculate, parafascicular and reticular thalamic nuclei. J Comp Neurol 511:678-691
51. Paxinos G, Watson C (2007) The rat brain in stereotaxic coordinates. Academic Press, San Diego
52. Plaha P, Gill SS (2005) Bilateral deep brain stimulation of the pedunculopontine nucleus for Parkinson's disease. NeuroReport 16:1883-1887 (Pubitemid 41653507)
53. Rosene DL, Roy NJ, Davis BJ (1986) A cryoprotection method that facilitates cutting frozen sections of whole monkeys brain for histological and histochemical processing without freezing artifact. J Histochem Cytochem 34:1301-1316
54. Saper CB, Loewy AD (1982) Projections of the pedunculopontine tegmental nucleus in the rat: Evidence for additional extrapyramidal circuitry. Brain Res 252:367-372 (Pubitemid 13238954)
55. Semba K, Fibiger HC (1992) 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 323:387-410
56. Semba K, Reiner PB, Fibiger HC (1990) Single cholinergic mesopontine tegmental neurons project to both the pontine reticular formation and the thalamus in the rat. Neuroscience 38:643-654 (Pubitemid 20383201)
57. Sofroniew MV, Priestley JV, Consolazione A, Eckenstein F, Cuello AC (1985) Cholinergic projections from the midbrain and pons to the thalamus in the rat, identified by combined retrograde tracing and choline acetyltransferase immunohistochemistry. Brain Res 329:213-223 (Pubitemid 15142236)
58. Stefani A, Lozano AM, Peppe A, Stanzione P, Galati S, Tropepi D, Pierantozzi M, Brusa L, Scarnati E, Mazzone P (2007) Bilateral deep brain stimulation of the pedunculopontine and subthalamic nuclei in severe Parkinson's disease. Brain 130:1596-1607 (Pubitemid 47355911)
59. Steininger TL, Rye DB, Wainer BH (1992) Afferent projections to the cholinergic pedunculopontine tegmental nucleus and adjacent midbrain extrapyramidal area in the albino rat. J Comp Neurol 321:515-543
60. Steriade M, Datta S, Pare D, Oakson G, Curro Dossi RC (1990) Neuronal activities in brainstem cholinergic nuclei related to tonic activation processes in thalamocortical systems. J Neurosci 10:2541-2559
61. Stornetta RL, Sevigny CP, Schreihofer AM, Rosin DL, Guyenet PG (2002) Vesicular glutamate transporter DNPI/VGLUT2 is expressed by both C1 adrenergic and non-aminergic vasomotor neurons of the rat medulla. J Comp Neurol 444:207-220 (Pubitemid 34117086)
62. Sugimoto T, Hattori T (1984) Organization of efferent projections of nucleus tegmenti pedunculopontinus pars compacta with special reference to its cholinergic aspects. Neuroscience 11:931-946 (Pubitemid 14111183)
63. Vila M, Périer C, Féger J, Yelnik J, Faucheux B, Ruberg M, Raisman- Vozari R, Agid Y, Hirsch EC (2000) Evolution of changes in neuronal activity in the subthalamic nucleus of rats with unilateral lesion of the substantia nigra assessed by the metabolic and electrophysiological measurements. Eur J Neurosci 12:337-344 (Pubitemid 30068438)
64. Vincent SR (2000) The ascending reticular activating system: From aminergic neurons to nitric oxide. J Chem Neuroanat 18:23-30 (Pubitemid 30120013)
65. 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)
66. Wang H-L, 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