The lamellar organization of the rat substantia nigra pars reticulata: Segregated patterns of striatal afferents and relationship to the topography of corticostriatal projections

Neuroscience

Volumn 73, Issue 3, 1996, Pages 761-781

  Deniau, J M ^a   Menetrey, A ^a   Charpier, S ^a  

^a SORBONNE UNIVERSITÉ   (France)

Author keywords

axonal tracing; basal ganglia; parallel processing; striatum; substantia nigra pars reticulata

Indexed keywords

HORSERADISH PEROXIDASE; WHEAT GERM AGGLUTININ;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; CORPUS STRIATUM; MALE; MICROIONTOPHORESIS; NERVE PROJECTION; NONHUMAN; NUCLEUS ACCUMBENS; OLFACTORY CORTEX; PRIORITY JOURNAL; RAT; RETROGRADE NERVE FIBER TRANSPORT; SENSORY NERVE; SUBSTANTIA NIGRA;

EID: 0030218002     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/0306-4522(96)00088-7     Document Type: Article

References (80)

1. 1. Alexander G. E. and Crutcher M. D. (1990) Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci. 13, 266-271.
2. 2. Alexander G. E. and Crutcher M. D. (1991) Reply. Trends Neurosci. 14, 56-58.
3. 3. Alexander G. E., Crutcher M. D. and DeLong M. R. (1990) Basal ganglia thalamocortical circuits: parallel substrates for motor, oculomotor, prefrontal and limbic functions. Prog. Brain Res. 85, 119-146.
4. 4. Anderson M. and Yoshida M. (1980) Axonal branching patterns and location of nigrothalamic and nigrocollicular neurons in the cat. J. Neurophysiol. 43, 883-895.
5. 5. Arbuthnott G. W., MacLeod N. K., Maxwell D. J. and Wright A. K. (1990) Distribution and synaptic contacts of the cortical terminals arising from neurons in the rat ventral medial thalamic nucleus. Neuroscience 38, 47-60.
6. 6. Arnault P. and Roger M. (1990) Ventral temporal cortex in the rat. Connections of secondary auditory areas Te2 and Te3. J. comp. Neurol. 302, 110-123.
7. 7. Barth T. M., Jones T. A. and Schauert T. (1990) Functional subdivisions of the rat sensorimotor cortex. Behav. Brain Res. 39, 73-95.
8. 8. Beckstead R. M. (1979) Long collateral branches of substantia nigra pars reticulata axons to thalamus, superior colliculus and reticular formation in monkey and cat. Multiple retrograde neuronal labelling with fluorescent dyes. Neuroscience 10, 767-779.
9. 9. Berendse H. W., Galis de Graaf Y. and Groenewegen H. J. (1992) Topographical organization and relationship with ventral striatal compartments of prefrontal corticostriatal projections in the rat. J. comp. Neurol. 316, 314-347.
10. 10. Brog J. S., Salapongse A., Deutch A. and Zahm D. S. (1993) The patterns of afferent innervation of the core and shell in the "accumbens" part of the ventral striatum. J. comp. Neurol. 338, 255-278.
11. 11. Cospito J. A. and Kultas-Ilinsky (1981) Synaptic organization of motor corticostriatal projections in the rat. Expl Neurol. 72, 257-266.
12. 12. Cowan R. L. and Wilson C. J. (1994) Spontaneous firing patterns and axonal projections of single corticostriatal neurons in the rat medial agranular cortex. J. Neurophysiol. 71, 17-32.
13. 13. Deniau J. M. and Chevalier G. (1992) The lamellar organization of the rat substantia nigra pars reticulata: distribution of projection neurons. Neuroscience 46, 361-377.
14. 14. Deniau J. M. and Chevalier G. (1994) Functional architecture of the rodent substantia nigra pars reticulata: evidence for segregated channels. In The Basal Ganglia IV-New ideas on Structure and Function (eds Percheron G., McKenzie J. S. and Feger J.), Advances in Behavioral Biology, vol 41, pp. 63-70. Plenum Press, New York.
15. 15. Deniau J. M., Hammond C., Riszk A. and 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. Expl Brain Res. 32, 409-422.
16. 16. Desban M., Gauchy C., Glowinski J. and Kernel M. L. (1995) Heterogeneous topographical distribution of the striatonigral and striatopallidal neurons in the matrix compartment of the cat caudate nucleus. J. comp. Neurol. 352, 117-133.
17. 17. Dinopoulos A., Karamanlidis A. N., Papadopoulos G., Antonopoulos J. and Michaloudi H. (1985) Thalamic projections to motor, prefrontal and somatosensory cortex in the sheep studied by means of the horseradish peroxidase retrograde transport method. J. comp. Neurol. 241, 63-81.
18. 18. Domesick V. B. (1969) Projections from the cingulate cortex in the rat. Brain Res. 12, 296-320.
19. 19. Domesick V. B. (1977) The topographical organization of the striatonigral connection in the rat. Anat. Rec. 187, 567.
20. 20. Donoghue J. P. and Herkenham M. (1986) Neostriatal projections from individual cortical fields conform to histochemically distinct striatal compartments in the rat. Brain Res. 365, 397-403.
21. 21. Donoghue J. P. and Wise S. P. (1982) The motor cortex of the rat: cytoarchitecture and microstimulation mapping. J. comp. Neurol. 212, 76-88.
22. 22. Ebrahimi A., Pochet R. and Roger M. (1992) Topographical organization of the projections from physiologically identified areas of the motor cortex to the striatum in the rat. Neurosci. Res. 14, 39-60.
23. 23. Faull R. L. M., Nauta W. J. H. and Domesick V. B. (1986) The visual cortico-striato-nigral pathway in the rat. Neuroscience 19, 1119-1132.
24. 24. Flaherty A. W. and Graybiel A. M. (1991) Corticostriatal transformations in the primate somatosensory system. Projections from physiologically mapped body part representations. J. Neurophysiol. 66, 1249-1263.
25. 25. François C., Yelnik J. and Percheron G. (1987) Golgi study of the primate substantia nigra. II Spatial organization of dendritic arborizations in relation to the cyto-architectonic boundaries and to the striatonigral bundle. J. comp. Neurol. 265, 473-493.
26. 26. Gerfen C. R. (1985) The neostriatal mosaic I Compartmental organization of projections from the neostriatum to the substantia nigra in the rat. J. comp. Neurol. 236, 454-476.
27. 27. Glenn L. L., Hada J., Roy J. P., Deschênes M. and Steriade M. (1982) Anterograde tracer and field potential analysis of the neocortical layer I projection from the nucleus ventralis medialis of the thalamus in the cat. Neuroscience 7, 1861-1878.
28. 28. Goldman-Rakic P. S. and Selemon L. D. (1990) New frontiers in basal ganglia research. Trends Neurosci. 13, 241-244.
29. 29. Groenewegen H. J. (1988) Organization of the afferent connections of the mediodorsal thalamic nucleus in the rat, related to the mediodorsal-prefrontal topography. Neuroscience 24, 379-431.
30. 30. Groenewegen H. J., Berendse H. W., Wolters J. G. and Lohman A. H. M. (1990) The anatomical relationship of the prefrontal cortex with the striatopallidal system, the thalamus and the amygdala: evidence for a parallel organization. In Prog. Brain Res. (eds Uylings H. B. M., Van Eden C. G., De Bruin M. A., Corner M. A. and Feenestra M. G. P.), vol. 85, pp. 95-118. Elsevier, Amsterdam.
31. 31. Grofova I., Deniau J. M. and Kitai S. T. (1982) Morphology of the substantia nigra pars reticulata projection neurons intracellularly labeled with HRP. J. comp. Neurol. 208, 352-368.
32. 32. Hall R. D. and Lindholm E. P. (1974) Organization of motor and somatosensory neocortex of the albino rat. Brain Res. 66, 23-38.
33. 33. Hedreen J. C. and DeLong M. R. (1991) Organization of striatopallidal, striatonigral and nigrostriatal projections in the macaque. J. comp. Neurol. 304, 569-595.
34. 34. Herkenham M. (1979) The afferent and efferent connections of the ventromedial thalamic nucleus in the rat. J. comp. Neurol. 183, 487-518.
35. 35. Höhl-Abrahao J. C. and Creutzfeldt O. D. (1991) Topographical mapping of the thalamocortical projections in rodents and comparison with that in primates. Expl Brain Res. 87, 283-294.
36. 36. Hontanilla B., De la Heras S. and Gimenéz-Amaya J. M. (1994) Organization of the striatal projections from the rostral caudate nucleus to the globus pallidus, the entopeduncular nucleus and the pars reticulata of the substantia nigra in the cat. Anat Rec. 238, 114-124.
37. 37. Ilinsky I. A., Jouandet M. L. and Goldman-Rakic P. S. (1985) Organization of the nigrothalamocortical system in the rhesus monkey. J. comp. Neurol. 236, 315-330.
38. 38. Juraska J. M., Wilson C. J. and Groves P. M. (1977) The substantia nigra of the rat: a Golgi study. J. comp. Neurol. 172, 585-600.
39. 39. Katayama T., Niimi K. and Matsuoka H. (I986) Thalamic projections to the motor and premotor areas in the cat traced with horseradish peroxidase. J. Hirnforsch. 27, 45-60.
40. 40. Kelley A. E. and Domesick V. B. (1982) The distribution of the projection from the hippocampal formation to the nucleus accumbens in the rat: an anterograde and retrograde horseradish peroxidase study. Neuroscience 7, 2321-2335.
41. 41. Krettek J. E. and Price J. L. (1977) The cortical projections of the mediodorsal nucleus and adjacent thalamic nuclei in the rat. Brain Res. 88, 243-261.
42. 42. LeDoux J. E., Farb C. R. and Romanski L. M. (1991) Overlapping projections to the amygdala and striatum from auditory processing areas of the thalamus and cortex. Neurosci. Lett. 134, 139-144.
43. 43. Lynd-Balta E. and Haber S. N. (1994) Primate striatonigral projections: a comparison of the sensorimotor-related striatum and the ventral striatum. J. comp. Neurol. 345, 562-578.
44. 44. McGeorge A. J. and Faull R. L. M. (1989) The organization of the projection from the cerebral cortex to the striatum in the rat. Neuroscience 29, 503-537.
45. 45. Mesulam M. M. (1978) Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: a non-carcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents. J. Histochem. Cytochem. 26, 106-117.
46. 46. Miyashita E. and Tamai Y. (1989) Subcortical connections of frontal 'oculomotor' areas in the cat. Brain Res. 502, 75-87.
47. 47. Montaron M. F., Deniau J. M., Menetry A., Glowinski J. and Thierry A. M. (1996) Prefrontal cortex inputs of the nucleus accumbens nigro-thalamic circuit Neuroscience (in press).
48. 48. Musil S. Y. and Olson C. R. (1988) Organization of cortical and subcortical projections to medial prefrontal cortex in the cat. J. comp. Neurol. 272, 219-241.
49. 49. Nauta W. J. H., Smith G. P., Faull R. L. M. and Domesick V. B. (1978) Efferent connections and nigral afferents of the nucleus accumbens septi in the rat. Neuroscience 3, 385-401.
50. 50. Niijima K. and Yoshida M. (1982) Electrophysiological evidence for branching nigral projections to pontine reticular formation, superior colliculus and thalamus. Brain Res. 239, 279-282.
51. 51. Parent P. (1990) Extrinsic connections of the basal ganglia. Trends Neurosci. 13, 254-258.
52. 52. Parent A. and Hazrati L. N. (1993) Anatomical aspects of information processing in primate basal ganglia. Trends Neurosci. 16, 111-116.
53. 53. Parent A. and Hazrati L. N. (1994) Multiple striatal representation in primate substantia nigra. J. comp. Neurol. 344, 305-320.
54. 54. Parent A., MacKey A., Smith Y. and Boucher R. (1983) The output organization of the substantia nigra in primate as revealed by retrograde double labeling method. Brain Res. Bull. 10, 529-538.
55. 55. Paxinos G. and Watson C. (1982) The Rat Brain in Stereotaxic Coordinates. Academic Press, New York.
56. 56. Pennartz C. M. A., Groenewegen H. J. and Lopez Da Silva F. H. (1994) The nucleus accumbens as a complex of functionally distinct neuronal esembles: an integration of behavioural, electrophysiological and anatomical data. Prog. Neurobiol. 42, 719-761.
57. 57. Percheron G. and Filion M. (1991) Parallel processing in the basal ganglia: up to a point. Trends Neurosci. 14, 55-56.
58. 58. Percheron G., Yelnik J. and François C. (1984) The primate striato-pallido-nigral system. An integrative system for cortical information. In Basal Ganglia: Structure and Function (eds McKenzie J. S., Kemm R. E. and Wilcock L. N.), pp. 87-105. Plenum Press, New York.
59. 59. Redgrave P., Marrow L. and Dean P. (1992) Topographical organization of the nigrotectal projection in rat: evidence for segregated channels. Neuroscience 80, 571-595.
60. 60. Reep R. L., Corwin J. W., Hashimoto A. and Watson R. T. (1987) Efferent connections of the rostral portion of medial agranular cortex in rats. Brain Res. Bull. 19, 203-221.
61. 61. Rhoades R. W., Kuo D. C., Polcer J. D., Fish S. E. and Voneida T. J. (1982) Indirect visual cortical input to the hamster's deep layers of the superior colliculus via the basal ganglia. J. comp. Neurol. 205, 8-29.
62. 62. Roger M. and Arnault P. (1989) Anatomical study of the connections of the primary auditory area in the rat. J. comp. Neurol. 287, 339-356.
63. 63. Roy J. P. and Price J. L. (1992) The organization of the thalamocortical connections of the mediodorsal thalamic nucleus in the rat, related to the ventral forebrain-prefrontal cortex topography. J. comp. Neurol. 323, 167-197.
64. 64. Royce G. J. and Mourey R. J. (1985) Efferent connections of the centromedian and parafascicular thalamic nuclei: an autoradiographic investigation in the cat. J. comp. Neurol. 235, 277-300.
65. 65. Saavedra H., Motles E., Infante C. and Leiva J. (1987) Evidence for a nigro-pulvinar-lateralis posterior complex projection in the cat using horseradish peroxidase neuronal retrograde technique. Archs. ital. Biol. 125, 59-70.
66. 66. Selemon S. and Goldman Rakic P. S. (1985) Longitudinal topography and interdigitation of corticostriatal projections in the rhesus monkey. J. Neurosci. 5, 776-794.
67. 67. Sesack S. R., Deutch A. Y., Roth R. H. and Bunney B. S. (1989) Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: an anterograde tracing study with PHAL. J. comp. Neurol. 290, 213-242.
68. 68. Smith Y. and Parent A. (1986) Differential connections of caudata nucleus and putamen in the squirrel monkey (Saimiri sciureus). Neuroscience 18, 347-371.
69. 69. Sripanidkulchai K. and Wyss J. M. (1986) Thalamic projections to retrosplenial cortex in the rat. J. comp. Neurol. 254, 143-165.
70. 70. Steindler D. A. and Deniau J. M. (1980) Anatomical evidence for collateral branching of substantia nigra neurons: a combined horseradish peroxidase and (3H) wheat germ agglutinin axonal transport study in the rat. Brain Res. 196, 228-236.
71. 71. Takada M. (1992) The lateroposterior thalamic nucleus and substantia nigra pars lateralis: origin of dual innervation over the visual system and basal ganglia. Neurosci. Lett. 139, 153-156.
72. 72. Tokuno H., Takada M., Kondo Y. and Mizuno (1993) Laminar organization of the substantia nigra pars reticulata in the macaque monkey, with special reference to the caudato-nigral tectal link. Expl Brain Res. 92, 545-548.
73. 73. Veening J. G., Cornelissen F. M. and Lieven P. A. J. M. (1980) The topical organization of the afferents to the caudatoputamen of the rat. A horseradish peroxidase study. Neuroscience 5, 1253-1268.
74. 74. Webster K. E. (1961) Cortico-striate interrelations in the albino rat. J. Anal. 95, 532-544.
75. 75. Wise S. P. and Jones E. G. (1977) Cells of origin and terminal distribution of descending projections of the rat somatic sensory cortex. J. comp. Neurol. 175, 129-158.
76. 76. Yasui Y., Nakano K., Kayahara T. and Mizuno N. (1991) Non dopaminergic projection from the substantia nigra pars lateralis to the inferior colliculus in the rat. Brain Res. 559, 139-144.
77. 77. Yeterian E. H. and Van Hoesen G. W. (1978) Cortico-striate projections in the rhesus monkey: the organization of certain cortico-caudate connections. Brain Res. 139, 43-63.
78. 78. Zahm D. S. and Brog J. S. (1992) On the significance of subterritories in the "accumbens" part of the rat ventral striatum. Neuroscience 50, 751-767.
79. 79. Zahm D. S. and Heimer J. S. (1993) Specificity in the efferent projections of the nucleus accumbens in the rat: comparison of the rostral pole projection patterns with those of the core and shell. J. comp. Neurol. 327, 220-232.
80. 80. Ziles K. (1985) The Cortex of the Rat. A Stereotaxic Atlas. Springer-Verlag, Berlin, Heidelberg, New York and Tokyo.