Patterns of axonal branching of neurons of the substantia nigra pars reticulata and pars lateralis in the rat

Journal of Comparative Neurology

Volumn 492, Issue 3, 2005, Pages 349-369

  Cebrián, Carolina ^a   Parent, André ^b   Prensa, Lucía ^a  

^a UNIVERSITY OF NAVARRA   (Spain)

^b CENTRE DE RECHERCHE DE L INSTITUT UNIVERSITAIRE EN SANTÉ MENTALE DE QUÉBEC   (Canada)

Author keywords

Axonal collateralization; Basal ganglia; Nigrocollicular pathway; Nigrofugal projections; Nigrothalamic pathway; Single cell labeling

Indexed keywords

DEXTRAN;

ANIMAL TISSUE; ARTICLE; BASAL GANGLION; BIOTINYLATION; DIENCEPHALON; GABAERGIC TRANSMISSION; NERVE FIBER GROWTH; NERVE FIBER TRANSPORT; NONHUMAN; PATTERN RECOGNITION; PRIORITY JOURNAL; RAT; RETICULAR FORMATION; SUBSTANTIA NIGRA; SUPERIOR COLLICULUS; TARGET CELL; TISSUE SECTION;

ANIMALS; FEMALE; IMMUNOHISTOCHEMISTRY; IONTOPHORESIS; MALE; NEURAL PATHWAYS; NEURONS; RATS; RATS, WISTAR; STAINING AND LABELING; SUBSTANTIA NIGRA;

EID: 27544513864     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.20741     Document Type: Article

References (117)

1. Alexander GE, Crutcher MD. 1990. Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci 13:266-271.
2. Alexander GE, DeLong MR, Strick PL. 1986. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 9:357-381.
3. Anderson M, Yoshida M. 1977. Electrophysiological evidence for branching nigral projections to the thalamus and the superior colliculus. Brain Res 137:361-364.
4. Anderson ME, Yoshida M. 1980. Axonal branching patterns and location of nigrothalamic and nigrocollicular neurons in the cat. J Neurophysiol 43:883-895.
5. Appell PP, Behan M. 1990. Sources of subcortical GABAergic projections to the superior colliculus in the cat. J Comp Neurol 302:143-158.
6. Arnault P, Roger M. 1990. Ventral temporal cortex in the rat: connections of secondary auditory areas Te2 and Te3. J Comp Neurol 302:110-123.
7. Basso MA, Wurtz RH. 2002. Neuronal activity in substantia nigra pars reticulata during target selection. J Neurosci 22:1883-1894.
8. Beckstead RM. 1983. Long collateral branches of substantia nigra pars reticulata axons to thalamus, superior colliculus and reticular formation in monkey and cat. Multiple retrograde neuronal labeling with fluorescent dyes. Neuroscience 10:767-779.
9. Beckstead RM, Frankfurter A. 1982. The distribution and some morphological features of substantia nigra neurons that project to the thalamus, superior colliculus and pedunculopontine nucleus in the monkey. Neuroscience 7:2377-2388.
10. Beckstead RM, Domesick VB, Nauta WJ. 1979. Efferent connections of the substantia nigra and ventral tegmental area in the rat. Brain Res 175:191-217.
11. Beckstead RM, Edwards SB, Frankfurter A. 1981. A comparison of the intranigral distribution of nigrotectal neurons labeled with horseradish peroxidase in the monkey, cat, and rat. J Neurosci 1:121-125.
12. Bentivoglio M, van der Kooy D, Kuypers HG. 1979. The organization of the efferent projections of the substantia nigra in the rat. A retrograde fluorescent double labeling study. Brain Res 174:1-17.
13. Bunney BS, Chiodo LA, Grace AA. 1991. Midbrain dopamine system electrophysiological functioning: a review and new hypothesis. Synapse 9:79-94.
14. Büttner U, Büttner-Ennever JA. 1988. Present concepts of oculomotor organization. Rev Oculomot Res 2:3-32.
15. Cadusseau J, Roger M. 1985. Afferent projections to the superior colliculus in the rat, with special attention to the deep layers. J Hirnforsch 26:667-681.
16. Campbell KJ, Takada M. 1989. Bilateral tectal projection of single nigrostriatal dopamine cells in the rat. Neuroscience 33:311-321.
17. Carpenter MB, Nakano K, Kim R. 1976. Nigrothalamic projections in the monkey demonstrated by autoradiographic technics. J Comp Neurol 165:401-415.
18. Cebrián C, Parent A, Prensa L. 2003. Patterns of axonal branching of substantia nigra pars reticulata neurons in the rat. Program No. 601.11. 2003 Abstract Viewer/Itinerary Planner. Washington, DC: Society for Neuroscience Online.
19. Chevalier G, Deniau JM. 1984. Spatio-temporal organization of a branched tecto-spinal/tecto-diencephalic neuronal system. Neuroscience 12:427-439.
20. Chevalier G, Mana S. 2000. Honeycomb-like structure of the intermediate layers of the rat superior colliculus, with additional observations in several other mammals: AChE patterning. J Comp Neurol 419:137-153.
21. Chevalier G, Thierry AM, Shibazaki T, Feger J. 1981. Evidence for a GABAergic inhibitory nigrotectal pathway in the rat. Neurosci Lett 21:67-70.
22. Chevalier G, Vacher S, Deniau JM. 1984. Inhibitory nigral influence on tectospinal neurons, a possible implication of basal ganglia in orienting behavior. Exp Brain Res 53:320-326.
23. Chevalier G, Vacher S, Deniau JM, Desban M. 1985. Disinhibition as a basic process in the expression of striatal functions. I. The striatonigral influence on tecto-spinal/tecto-diencephalic neurons. Brain Res 334:215-226.
24. Clavier RM, Atmadja S, Fibiger HC. 1976. Nigrothalamic projections in the rat as demonstrated by orthograde and retrograde tracing techniques. Brain Res Bull 1:379-384.
25. Cowie RJ, Smith MK, Robinson DL. 1994. Subcortical contributions to head movements in macaques. II. Connections of a medial pontomedullary head-movement region. J Neurophysiol 72:2665-2682.
26. Dean P, Redgrave P, Westby GW. 1989. Event or emergency? Two response systems in the mammalian superior colliculus. Trends Neurosci 12:137-147.
27. Deniau JM, Chevalier G. 1992. The lamellar organization of the rat substantia nigra pars reticulata: distribution of projection neurons. Neuroscience 46:361-377.
28. Deniau JM, Hammond C, Riszk A, Feger J. 1978. Electrophysiological properties of identified output neurons of the rat substantia nigra (pars compacta and pars reticulata): evidences for the existence of branched neurons. Exp Brain Res 32:409-422.
29. Deniau JM, Menetrey A, Charpier S. 1996. The lamellar organization of the rat substantia nigra pars reticulata: segregated patterns of striatal afferents and relationship to the topography of corticostriatal projections. Neuroscience 73:761-781.
30. Deschênes M, Bourassa J, Doan VD, Parent A. 1996. A single-cell study of the axonal projections arising from the posterior intralaminar thalamic nuclei in the rat. Eur J Neurosci 8:329-343.
31. Di Chiara G, Porceddu ML, Morelli M, Mulas ML, Gessa GL. 1979. Substantia nigra as an output station for striatal dopaminergic responses: role of a GABA-mediated inhibition of pars reticulata neurons. Naunyn Schmiedebergs Arch Pharmacol 306:153-159.
32. Faull RL, Carman JB. 1968. Ascending projections of the substantia nigra in the rat. J Comp Neurol 132:73-92.
33. Faull RL, Mehler WR. 1978. The cells of origin of nigrotectal, nigrothalamic and nigrostriatal projections in the rat. Neuroscience 3:989-1002.
34. François C, Percheron G, Yelnik J. 1984. Localization of nigrostriatal, nigrothalamic and nigrotectal neurons in ventricular coordinates in macaques. Neuroscience 13:61-76.
35. Gerfen CR, Wilson CJ. 1996. The basal ganglia. In: Swanson LW, Bjorklund A, Hokfelt T, editors. Integrated system of the CNS, part III, handbook of chemical neuroanatomy, vol 12. Amsterdam: Elsevier, p 371-468.
36. Gerfen CR, Staines WA, Arbuthnott GW, Fibiger HC. 1982. Crossed connections of the substantia nigra in the rat. J Comp Neurol 207:283-303.
37. Gerfen CR, Baimbridge KG, Miller JJ. 1985. The neostriatal mosaic: compartmental distribution of calcium-binding protein and parvalbumin in the basal ganglia of the rat and monkey. Proc Natl Acad Sci U S A 82:8780-8784.
38. Gerfen CR, Baimbridge KG, Thibault J. 1987a. The neostriatal mosaic: III. Biochemical and developmental dissociation of patch-matrix mesostriatal systems. J Neurosci 7:3935-3944.
39. Gerfen CR, Herkenham M, Thibault J. 1987b. The neostriatal mosaic: II. Patch- and matrix-directed mesostriatal dopaminergic and non-dopaminergic systems. J Neurosci 7:3915-3934.
40. German DC, Manaye KF. 1993. Midbrain dopaminergic neurons (nuclei A8, A9, and A10): three-dimensional reconstruction in the rat. J Comp Neurol 331:297-309.
41. González-Hernández T, Rodríguez M. 2000. Compartmental organization and chemical profile of dopaminergic and GABAergic neurons in the substantia nigra of the rat. J Comp Neurol 421:107-135.
42. Grace AA, Bunney BS. 1984a. The control of firing pattern in nigral dopamine neurons: single spike firing. J Neurosci 4:2866-2876.
43. Grace AA, Bunney BS. 1984b. The control of firing pattern in nigral dopamine neurons: burst firing. J Neurosci 4:2877-2890.
44. Granata AR, Kitai ST. 1991. Inhibitory substantia nigra inputs to the pedunculopontine neurons. Exp Brain Res 86:459-466.
45. Grofova I, Deniau JM, Kitai ST. 1982. Morphology of the substantia nigra pars reticulata projection neurons intracellularly labeled with HRP. J Comp Neurol 208:352-368.
46. 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.
47. Harris LR. 1980. The superior colliculus and movements of the head and eyes in cats. J Physiol 300:367-391.
48. Hikosaka O, Wurtz RH. 1989. The basal ganglia. Rev Oculomot Res 3:257-281.
49. Hikosaka O, Takikawa Y, Kawagoe R. 2000. Role of the basal ganglia in the control of purposive saccadic eye movements. Physiol Rev 80:953-978.
50. Hökfelt T, Johansson O, Goldstein M. 1984. Chemical anatomy of the brain. Science 225:1326-1334.
51. Hontanilla B, Parent A, Gimenez-Amaya JM. 1997. Parvalbumin and calbindin D-28k in the entopeduncular nucleus, subthalamic nucleus, and substantia nigra of the rat as revealed by double-immunohistochemical methods. Synapse 25:359-367.
52. Hsu SM, Raine L, Fanger H. 1981. Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem 29:577-580.
53. Huerta MF, Van Lieshout DP, Harting JK. 1991. Nigrotectal projections in the primate Galago crassicaudatus. Exp Brain Res 87:389-401.
54. Illing RB. 1990. Choline acetyltransferase-like immunoreactivity in the superior colliculus of the cat and its relation to the pattern of acetylcholinesterase staining. J Comp Neurol 296:32-46.
55. Jackson A, Crossman AR. 1981. Basal ganglia and other afferent projections to the peribrachial region in the rat: a study using retrograde and anterograde transport of horseradish peroxidase. Neuroscience 6:1537-1549.
56. Jayaraman A, Batton RR, Carpenter MB. 1977. Nigrotectal projections in the monkey: an autoradiographic study. Brain Res 135:147-152.
57. 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.
58. Karabelas AB, Moschovakis AK. 1985. Nigral inhibitory termination on efferent neurons of the superior colliculus: an intracellular horseradish peroxidase study in the cat. J Comp Neurol 239:309-329.
59. Kelland MD, Asdourian D. 1989. Pedunculopontine tegmental nucleus-induced inhibition of muscle activity in the rat. Behav Brain Res 34:213-234.
60. Kernel ML, Desban M, Gauchy C, Glowinski J, Besson MJ. 1988. Topographical organization of efferent projections from the cat substantia nigra pars reticulata. Brain Res 455:307-323.
61. Kha HT, Finkelstein DI, Tomas D, Drago J, Pow DV, Home MK. 2001. Projections from the substantia nigra pars reticulata to the motor thalamus of the rat: single axon reconstructions and immunohistochemical study. J Comp Neurol 440:20-30.
62. Kultas-Ilinsky K, Ilinsky IA, Massopust LC, Young PA, Smith KR. 1978. Nigrothalamic pathway in the cat demonstrated by autoradiography and electron microscopy. Exp Brain Res 33:481-492.
63. Levey AI, Wainer BH, Mufson EJ, Mesulam MM. 1983. Co-localization of acetylcholinesterase and choline acetyltransferase in the rat cerebrum. Neuroscience 9:9-22.
64. Levey AI, Hallanger AE, Wainer BH. 1987. Choline acetyltransferase immunoreactivity in the rat thalamus. J Comp Neurol 257:317-332.
65. Mailly P, Charpier S, Menetrey A, Deniau JM. 2003. Three-dimensional organization of the recurrent axon collateral network of the substantia nigra pars reticulata neurons in the rat. J Neurosci 23:5247-5257.
66. McGeorge AJ, Faull RL. 1989. The organization of the projection from the cerebral cortex to the striatum in the rat. Neuroscience 29:503-537.
67. McHaffie JG, Stein BE. 1982. Eye movements evoked by electrical stimulation in the superior colliculus of rats and hamsters. Brain Res 247:243-253.
68. Mengual E, Velayos JL, Reinoso-Suarez F. 1993. Nicotinamide-adenine dinucleotide phosphate diaphorase activity matches acetylcholinesterase-rich patches in the medial thalamic nuclei of the cat. Brain Res 625:165-168.
69. Mengual E, Casanovas-Aguilar C, Perez-Clausell J, Gimenez-Amaya JM. 2001. Thalamic distribution of zinc-rich terminal fields and neurons of origin in the rat. Neuroscience 102:863-884.
70. Meredith GE, Wouterlood FG. 1990. Hippocampal and midline thalamic fibers and terminals in relation to the choline acetyltransferase-immunoreactive neurons in nucleus accumbens of the rat: a light and electron microscopic study. J Comp Neurol 296:204-221.
71. Mesulam MM, Mufson EJ, Levey AI, Wainer BH. 1984. Atlas of cholinergic neurons in the forebrain and upper brainstem of the macaque based on monoclonal choline acetyltransferase immunohistochemistry and acetylcholinesterase histochemistry. Neuroscience 12:669-686.
72. Middleton FA, Strick PL. 1996. Basal ganglia and cerebellar output influences non-motor function. Mol Psychiatry 1:429-433.
73. Middleton FA, Strick PL. 2002. Basal-ganglia "projections" to the prefrontal cortex of the primate. Cereb Cortex 12:926-935.
74. Moriizumi T, Leduc-Cross B, Wu JY, Hattori T. 1992. Separate neuronal populations of the rat substantia nigra pars lateralis with distinct projection sites and transmitter phenotypes. Neuroscience 46:711-720.
75. Muto N, Kakei S, Shinoda Y. 1996. Morphology of single axons of tectospinal neurons in the upper cervical spinal cord. J Comp Neurol 372:9-26.
76. Nakamura Y, Tokuno H, Moriizumi T, Kitao Y, Kudo M. 1989. Monosynaptic nigral inputs to the pedunculopontine tegmental nucleus neurons which send their axons to the medial reticular formation in the medulla oblongata. An electron microscopic study in the cat. Neurosci Lett 103:145-150.
77. Nelson EL, Liang CL, Sinton CM, German DC. 1996. Midbrain dopaminergic neurons in the mouse: computer-assisted mapping. J Comp Neurol 369:361-371.
78. Niijima K, Yoshida M. 1982. Electrophysiological evidence for branching nigral projections to pontine reticular formation, superior colliculus and thalamus. Brain Res 239:279-282.
79. Nishimura Y, Takada M, Mizuno N. 1997. Topographic distribution and collateral projections of the two major populations of nigrothalamic neurons. A retrograde labeling study in the rat. Neurosci Res 28:1-9.
80. Noda T, Oka H. 1984. Nigral inputs to the pedunculopontine region: intracellular analysis. Brain Res 322:332-336.
81. Northmore DP, Levine ES, Schneider GE. 1988. Behavior evoked by electrical stimulation of the hamster superior colliculus. Exp Brain Res 73:595-605.
82. Parent A. 1990. Extrinsic connections of the basal ganglia. Trends Neurosci. 13:254-258.
83. Parent A, Hazrati LN. 1995. Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop. Brain Res Brain Res Rev 20:91-127.
84. Parent A, Mackey A, Smith Y, Boucher R. 1983. The output organization of the substantia nigra in primate as revealed by a retrograde double labeling method. Brain Res Bull 10:529-537.
85. Paxinos G, Watson C. 1998. The rat brain in stereotaxic coordinates, 4th edition. New York: Academic Press.
86. Paxinos G, Kus L, Ashwell KWS, Watson C. 1999. Chemoarchitectonic atlas of the rat forebrain. New York: Academic Press.
87. Prensa L, Parent A. 2001. The nigrostriatal pathway in the rat: a single-axon study of the relationship between dorsal and ventral tier nigral neurons and the striosome/matrix striatal compartments. J Neurosci 21:7247-7260.
88. Price JL. 1994. Thalamus. In: Paxinos G, editor. The rat nervous system. New York: Elsevier, p 570-645.
89. Rajakumar N, Elisevich K, Flumerfelt BA. 1994. Parvalbumin-containing GABAergic neurons in the basal ganglia output system of the rat. J Comp Neurol 350:324-336.
90. Redgrave P, Odekunle A, Dean P. 1986. Tectal cells of origin of predorsal bundle in rat: location and segregation from ipsilateral descending pathway. Exp Brain Res 63:279-293.
91. Redgrave P, Marrow L, Dean P. 1992a. Topographical organization of the nigrotectal projection in rat: evidence for segregated channels. Neuroscience 50:571-595.
92. Redgrave P, Simkins M, Overton P, Dean P. 1992b. Anticonvulsant role of nigrotectal projection in the maximal electroshock model of epilepsy-I. Mapping of dorsal midbrain with bicuculline. Neuroscience 46:379-390.
93. Redgrave P, Marrow LP, Dean P. 1992c. Anticonvulsant role of nigrotectal projection in the maximal electroshock model of epilepsy-II. Pathways from substantia nigra pars lateralis and adjacent peripeduncular area to the dorsal midbrain. Neuroscience 46:391-406.
94. Reiner A, Anderson KD. 1993. Co-occurrence of gamma-aminobutyric acid, parvalbumin and the neurotensin-related neuropeptide LANT6 in pallidal, nigral and striatal neurons in pigeons and monkeys. Brain Res 624:317-325.
95. Rhoades RW, Kuo DC, Polcer JD, Fish SE, Voneida TJ. 1982. Indirect visual cortical input to the deep layers of the hamster's superior colliculus via the basal ganglia. J Comp Neurol 208:239-254.
96. Rinvik E. 1975. Demonstration of nigrothalamic connections in the cat by retrograde axonal transport of horseradish peroxidase. Brain Res 90:313-318.
97. Roger M, Arnault P. 1989. Anatomical study of the connections of the primary auditory area in the rat. J Comp Neurol 287:339-356.
98. Saitoh K, Hattori S, Song WJ, Isa T, Takakusaki K. 2003. Nigral GABAergic inhibition upon cholinergic neurons in the rat pedunculopontine tegmental nucleus. Eur J Neurosci 18:879-886.
99. Sakai ST, Grofova I, Bruce K. 1998. Nigrothalamic projections and nigrothalamocortical pathway to the medial agranular cortex in the rat: single- and double-labeling light and electron microscopic studies. J Comp Neurol 391:506-525.
100. Smith Y, Parent A, Seguela P, Descarries L. 1987. Distribution of GABA-immunoreactive neurons in the basal ganglia of the squirrel monkey (Saimiri sciureus). J Comp Neurol 259:50-64.
101. Spann BM, Grofova I. 1991. Nigropedunculopontine projection in the rat: an anterograde tracing study with Phaseolus vulgoris-leucoagglutinin (PHA-L). J Comp Neurol 311:375-388.
102. 3H]wheat germ agglutinin axonal transport study in the rat. Brain Res 196:228-236.
103. Steininger TL, Wainer BH, Rye DB. 1997. Ultrastructural study of cholinergic and noncholinergic neurons in the pars compacta of the rat pedunculopontine tegmental nucleus. J Comp Neurol 382:285-301.
104. Syka J, Radil-Weiss T. 1971. Electrical stimulation of the tectum in freely moving cats. Brain Res 28:567-572.
105. 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.
106. Tan MM, Harvey AR. 1989. The cholinergic innervation of normal and transplanted superior colliculus in the rat: an immunohistochemical study. Neuroscience 32:511-520.
107. Tsumori T, Yasui Y. 1997. Organization of the nigro-tecto-bulbar pathway to the parvicellular reticular formation: a light- and electron-microscopic study in the rat. Exp Brain Res 116:341-350.
108. Tsumori T, Yokota S, Ono K, Yasui Y. 2002. Synaptic organization of GABAergic projections from the substantia nigra pars reticulata and the reticular thalamic nucleus to the parafascicular thalamic nucleus in the rat. Brain Res 957:231-241.
109. Tsumori T, Yokota S, Ono K, Yasui Y. 2003. Nigrothalamostriatal and nigrothalamocortical pathways via the ventrolateral parafascicular nucleus. Neuroreport 14:81-86.
110. Ueki A. 1983. The mode of nigro-thalamic transmission investigated with intracellular recording in the cat. Exp Brain Res 49:116-124.
111. Williams MN, Faull RL. 1988. The nigrotectal projection and tectospinal neurons in the rat. A light and electron microscopic study demonstrating a monosynaptic nigral input to identified tectospinal neurons. Neuroscience 25:533-562.
112. Yamasaki DS, Krauthamer GM, Rhoades RW. 1986. Superior collicular projection to intralaminar thalamus in rat. Brain Res 378:223-233.
113. Yasui Y, Nakano K, Kayahara T, Mizuno N. 1991. Non-dopaminergic projections from the substantia nigra pars lateralis to the inferior colliculus in the rat. Brain Res 559:139-144.
114. Yasui Y, Nakano K, Nakagawa Y, Kayahara T, Shiroyama T, Mizuno N. 1992. Non-dopaminergic neurons in the substantia nigra project to the reticular formation around the trigeminal motor nucleus in the rat. Brain Res 585:361-366.
115. Yasui Y, Tsumori T, Ando A, Domoto T, Kayahara T, Nakano K. 1994. Descending projections from the superior colliculus to the reticular formation around the motor trigeminal nucleus and the parvicellular reticular formation of the medulla oblongata in the rat. Brain Res 656:420-426.
116. Yasui Y, Tsumori T, Ando A, Domoto T. 1995. Demonstration of axon collateral projections from the substantia nigra pars reticulata to the superior colliculus and the parvicellular reticular formation in the rat. Brain Res 674:122-126.
117. Yasui Y, Tsumori T, Ono K, Kishi T. 1997. Nigral axon terminals are in contact with parvicellular reticular neurons which project to the motor trigeminal nucleus in the rat. Brain Res 775:219-224.