Neuronal interactions in the substantia nigra pars reticulata through axon collaterals of the projection neurons

An electrophysiological and morphological study

Summary

Substantia nigra pars reticulata (SNr) neurons, antidromically activated following stimulation of the dorsal thalamus and/or superior colliculus were intracellularly stained with HRP. Light microscopic analysis revealed that the labeled SNr neurons have axon collaterals arborizing within SNr. Axon collaterals of SNr neurons partially overlapped with the dendritic fields of their parent cells and also extended beyond the parent dendritic fields. The labeled axon terminals did not closely appose the parent cell processes, suggesting that the collaterals most likely terminate on neurons other than the parent cell.

Electrical stimulation of either the thalamus or the superior colliculus induced monosynaptic and polysynaptic IPSPs in SNr cells. The polysynaptic IPSPs evoked from thalamic stimulation disappeared following hemitransection of the brain just rostral to the thalamus while the monosynaptic IPSPs remained the same. Since there are no known afferents from either thalamus or superior colliculus to SNr, we consider that these monosynaptic IPSPs are due to activation of the recurrent collaterals of SNr projection cells. The results of this study indicate that projection neurons of SNr also have an inhibitory role within the SNr.

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References

  1. Adams JC (1977) Technical considerations on the use of horseradish peroxidase as a neuronal marker. Neuroscience 2: 141–145

    Google Scholar 

  2. Beckstead RM, Domesick VB, Nauta WJH (1979) Efferent connections of the substantia nigra and ventral tegmental area in the rat. Brain Res 175: 191–217

    Google Scholar 

  3. Bentivoglio M, Van Der Kooy D, Kuypers HGJM (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

    Google Scholar 

  4. Bunny BS, Aghajanian GK (1976) The precise localization of nigral afferents in the rat as determined by a retrograde tracing technique. Brain Res 117: 423–435

    Google Scholar 

  5. Carpenter MB, Nakaro K, Kim R (1976) Nigrothalamic projections in the monkey demonstrated by autoradiographic technics. J Comp Neurol 165: 401–416

    Google Scholar 

  6. Chevalier G, Thierry AM, Shibazaki T, Feger J (1981) Evidence for a GABAergic inhibitory nigrotectal pathway in the rat. Neurosci Lett 21: 67–70

    Google Scholar 

  7. Deniau JM, Feger J, de Guyader C (1976) Striatal evoked inhibition of indentified nigro-thalamic neurons. Brain Res 104: 152–156

    Google Scholar 

  8. Deniau JM, Lockner D, Feger J (1978a) Effect of substantia nigra stimulation on identified neurons in the VL-VA thalamic complex: Comparison between intact and chronically decorticated cats. Brain Res 145: 27–36

    Google Scholar 

  9. Deniau JM, Chevalier G, Feger J (1978b) Electrophysiological study of the nigro-tectal pathway in the rat. Neurosci Lett 10: 215–220

    Google Scholar 

  10. DiChiara G, Porcedau ML, Mulas ML, Gessa GL (1979) Evidence for a GABAergic projection from the substantia nigra to the ventromedial thalamus and to the superior colliculus of the rat. Brain Res 176: 273–284

    Google Scholar 

  11. Dray A, Gonye TJ, Oakley NR, Tanner T (1976) Evidence for existence of a raphe projection to the substantia nigra in rat. Brain Res 113: 45–57

    Google Scholar 

  12. Faull RLM, Mehler WR (1978) The cells of origin of nigrotectal, nigrothalamic and nigrostriatal projections in the rat. Neuroscience 3: 989–1002

    Google Scholar 

  13. Francois C, Percheron G, Yelnik J, Heyner S (1979) Demonstration of the existence of small local circuit neurons in the Golgi-stained primate substantia nigra. Brain Res 172: 160–164

    Google Scholar 

  14. Grofova I (1975) The identification of striatal and pallidal neurons projecting to substantia nigra. An experimental study by means of retrograde axonal transport of horseradish peroxidase. Brain Res 91: 286–291

    Google Scholar 

  15. Grofova I, Rinvik E (1970) An experimental electron microscopic study on the striatonigral projection in the cat. Exp Brain Res 11: 249–262

    Google Scholar 

  16. Grofova I, Deniau JM, Kitai ST (1982) Morphology of the substantia nigra pars reticulata projection neurons intracellularly labeled with HRP. J Comp Neurol (in press)

  17. Gulley RI, Wood RL (1971) The fine structure of the neurons in the rat substantia nigra. Tissue Cell 3: 675–690

    Google Scholar 

  18. Hattori T, McGeer P, Fibiger HC, McGeer EG (1973) On the source of GAB A-containing terminals in the substantia nigra. Electron microscopic autoradiographic and biochemical studies. Brain Res 54: 103–114

    Google Scholar 

  19. Herkenham M (1979) The afferent and efferent connections of the ventromedial thalamic nucleus in the rat. J Comp Neurol 183: 487–518

    Google Scholar 

  20. Herkenham M, Nauta WJH (1979) Efferent connections of the habenular nuclei in the rat. J Comp Neurol 187: 19–48

    Google Scholar 

  21. Juraska JM, Wilson CJ, Groves PM (1977) The substantia nigra of the rat: A Golgi study. J Comp Neurol 172: 585–600

    Google Scholar 

  22. Kanazawa I, Marshall GR, Kelly JS (1976) Afferents to the rat substantia nigra studied with horseradish peroxidase with special reference to fibers from the subthalamic nucleus. Brain Res 11: 485–491

    Google Scholar 

  23. Karabelas A, Purpura D (1980) Evidence for autapses in the substantia nigra. Brain Res 200: 467–473

    Google Scholar 

  24. Kultas-Ilinsky K, Ilinsky IA, Massopust LC, Young PA, Smith KR (1978) Nigrothalmic pathway in the cat demonstrated by autoradiography and electron microscopy. Exp Brain Res 33: 481–492

    Google Scholar 

  25. MacLeod NK, James TA, Kilpatrick IC, Starr MS (1980) Evidence for a GABAergic nigrothalamic pathway in the rat. II. Electrophysiological studies. Exp Brain Res 40: 55–61

    Google Scholar 

  26. Miller JJ, Richardson TL, Fibiger HC, McLennan H (1975) Anatomical and electrophysiologica identification of a projection from the mesencephalic raphe to the caudate putamen in the rat. Brain Res 97: 133–138

    Google Scholar 

  27. Moore RY, Halaris AE, Jones BE (1978) Serotonin neuron of midbrain raphe: Ascending projections. J Comp Neurol 180: 417–438

    Google Scholar 

  28. Nakamura S, Iwama K (1975) Antidromic activation of the rat locus coeruleus neurons from hippocampus, cerebral and cerebellar cortices. Brain Res 99: 372–376

    Google Scholar 

  29. Nauta HJW, Kaiserman-Abramof IR, Lasek RJ (1975) Electron microscopic observations of horseradish peroxidase transported from the caudatoputamen to the substantia nigra in the rat: Possible involvement of the agranular reticulum. Brain Res 85: 373–384

    Google Scholar 

  30. Niimi K, Ikeda T, Kawamura S, Inoshita H (1970) Efferent projections of the head of the caudate nucleus in the cat. Brain Res 21: 327–343

    Google Scholar 

  31. Park MR, Lighthall JW, Kitai ST (1980) Recurrent inhibition in the rat neostriatum. Brain Res 194: 359–369

    Google Scholar 

  32. Ramon y Cajal S (1955) Histologie du systeme nerveux de l'homme et des vertebres. Tome II. Instituto Ramon y Cajal, Madrid, pp 275–278

    Google Scholar 

  33. Ribak CE, Vaughn JE, Roberts E (1980) Gabaergic nerve terminals decrease in the substantia nigra following hemitransections of the striatonigral and pallidonigral pathways. Brain Res 192: 413–420

    Google Scholar 

  34. Rinvik E (1975) Demonstration of nigrothalamic connections in the cat by retrograde axonal transport of horseradish peroxidase. Brain Res 90: 313–318

    Google Scholar 

  35. Rinvik E, Grofova I (1970) Observations on the fine structure of the substantia nigra in the cat. Exp Brain Res 11: 229–248

    Google Scholar 

  36. Rinvik E, Grofova I, Ottersen OP (1976) Demonstration of nigrotectal and nigroreticular projections in the cat by axonal transport of proteins. Brain Res 112: 388–394

    Google Scholar 

  37. Schwyn RC, Fox CA (1974) The primate substantia nigra: A Golgi and electron microscopic study. J Hirnforsch 15: 95–126

    Google Scholar 

  38. Steindler DA, Deniau JM (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

    Google Scholar 

  39. Szabo J (1962) Topical distribution of the striatal efferents in the monkey. Exp Neurol 5: 21–36

    Google Scholar 

  40. Szabo J (1967) The efferent projections of the putamen in the monkey. Exp Neurol 19: 463–476

    Google Scholar 

  41. Ueki A, Uno M, Anderson M, Yoshida M (1977) Monosynaptic inhibition of thalamic neurons produced by stimulation of substantia nigra. Experientia 33: 1480–1481

    Google Scholar 

  42. Van der Kooy D, Hattori T (1980) Single subthalamic nucleus neurons project to both the globus pallidus and substantia nigra in rat. J Comp Neurol 192: 751–768

    Google Scholar 

  43. Vincent ST, Hattori T, McGeer EG (1978) The nigro-tectal projection: A biochemical and ultrastructural characterization. Brain Res 151: 159–164

    Google Scholar 

  44. Voneida TJ (1960) An experimental study of the course and destination of fibers arising in the head of the caudate nucleus in the cat and monkey. J Comp Neurol 115: 75–87

    Google Scholar 

  45. Wilson CJ, Groves PM (1979) A simple and rapid section embedding technique for sequential light and electron microscopic examination of individually stained central neurons. J Neurosci Meth 1: 383–391

    Google Scholar 

  46. Yoshida M, Omata S (1979) Blocking by picrotoxin of nigra evoked inhibition of neurons of ventromedial nucleus of the thalamus. Experientia 35: 794

    Google Scholar 

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Correspondence to Prof. S. T. Kitai.

Additional information

Supported by USPHS NIH Grant NS 14866 to S.T. Kitai and F32 NS 06249 to J.P. Donoghue. Foundation Simone el Cino del Duca, Paris, France, furnished travel funds to J.M. Deniau

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Deniau, J.M., Kitai, S.T., Donoghue, J.P. et al. Neuronal interactions in the substantia nigra pars reticulata through axon collaterals of the projection neurons. Exp Brain Res 47, 105–113 (1982). https://doi.org/10.1007/BF00235891

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Key words

  • Substantia nigra
  • Nigra projection neurons
  • Axon collaterals
  • Antidromic activation
  • Collateral inhibition