Journal of Neurocytology

, Volume 30, Issue 8, pp 695–704 | Cite as

Lamination of spinal cells projecting to the zona incerta of rats

Article

Abstract

In this study, the lamination patterns of spinal cells projecting to the zona incerta (ZI), intralaminar nuclei and ventral posterior nucleus of the thalamus have been explored. Injections of cholera toxin subunit B or latex beads were made into the ZI, intralaminar and ventral posterior nuclei of Sprague Dawley rats. The brain and spinal cord were then aldehyde fixed and processed using standard methods. Our results show two major findings. First, after injections into the ZI, there is a distinct pattern of lamination of labelled cells in the spinal cord, a pattern that changes across the different levels. At cervical levels, labelled cells are located within the medial region of the deep dorsal horn, while at lumbar and sacral levels, they are found in the intermediate grey matter. These results are similar to those seen after injections into the intralaminar or ventral posterior nuclei, except that in the latter cases, more labelled cells are located in the superficial laminae of the dorsal horn, particularly from the ventral posterior nucleus. Second, the ZI is not associated uniformly with all spinal levels; labelling is heaviest at cervical and lightest at thoracic levels. From each thalamic injection site, labelling is noted on both sides of the spinal cord, with a clear contralateral predominance. In conclusion, the results indicate that the ZI receives a distinct set of spinal projections principally from the cervical level. The particular pattern of lamination of spinal cells projecting to the ZI suggests that the type of information relayed is from deep somatic and/or visceral structures, and probably nociceptive in nature.

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References

  1. Al-Chaer, E. D., Lawand, N. B., Westlund, K. N. & Willis, W. D. (1996) Visceral nociceptive input into the ventral posterolateral nucleus of the thalamus: A new function for the dorsal column pathway. Journal of Neurophysiology 76, 2661–2674.Google Scholar
  2. Al-Chaer, E. D., Lawand, N. B., Westlund, K. N. & Willis, W. D. (1997) Nucleus gracilis: An integrator for visceral and somatic information. Journal of Neurophysiology 78, 521–527.Google Scholar
  3. Angelucci, A., ClascÀ, F. & Sur, M. (1996) Anterograde axonal tracing with the subunit B of cholera toxin: A highly sensitive immunohistochemical protocol for revealing fine axonal morphology in adult and neonatal brains. Journal of Neuroscience Methods 65, 101–112.Google Scholar
  4. Apkarian, A. V. & Hodge, C. J. (1989) Primate spinothalamic pathways: III. Thalamic terminations of the dorsolateral and ventral spinothalamic pathways. Journal of Comparative Neurology 274, 493–511.Google Scholar
  5. Bosler, D., Hobbs, S., Chandler, M. J., Ammons, W., Brennan, T. & Foreman, R. (1991) Convergence of phrenic and cardiopulmonary spinal afferent information on cervical and thoracic spinothalamic tract neurons in the monkey: Implications for referred pain from diaphragm and heart. Journal of Neurophysiology 65, 1042–1054.Google Scholar
  6. Burstein, R., Dado, R. J. & Giesler, G. J. (1990) The cells of origin of the spinothalamic tract of the rat: A quantitative reexamination. Brain Research 511, 329–337.Google Scholar
  7. Cervero, F., Handwerker, H. O. & Laird, J. M. A. (1988) Prolonged noxious mechanical stimulation of the rat's tail: Responses and encoding properties of dorsal horn neurons. Journal of Physiology 404, 419–436.Google Scholar
  8. Chandler, M. J., Zhang, J. & Foreman, R. D. (1996) Vagal, sympathetic and somatic sensory to upper cervical (C1–C3) spinothalamic tract neurones in monkeys. Journal of Neurophysiology 76, 2555–2567.Google Scholar
  9. Clement, C. I., Keay, K. A., Podzebenko, K., Gordon, B. D. & Bandler, R. (2000) Spinal sources of noxious visceral and noxious deep somatic afferent drive onto the ventrolateral periaqueductal grey of the rat. Journal of Comparative Neurology 425, 323–344.Google Scholar
  10. Coleman, K. A. & Mitrofanis, J. (1996) Organisation of the visual reticular thalamic nucleus of rat. European Journal of Neuroscience 8, 388–404.Google Scholar
  11. Edwards, D. A. & Isaacs, S. (1991) Zona incerta lesion: Effects on copulation, partner preference and other sociosexual behaviours. Behavioural Brain Research 44, 145–150.Google Scholar
  12. Feng, Y., Cui, M., Al-Chaer, E. D. & Willis, W. D. (1998) Epigastric antinociception by cervical dorsal column lesion in rats. Journal of Anaesthesiology 89, 411–420.Google Scholar
  13. Fu, Q., Chandler, M. J., Mcneill, D. & Foreman, R. D. (1992) Vagal afferent fibres excite upper cervical neurones and inhibit activity of lumbar spinal cord neurons in the rat. Pain 51, 91–100.Google Scholar
  14. Giesler, G. J., MenetrÉy, D. & Basbaum, A. I. (1979) Differential origins of spinothalamic tract projections to medial and lateral thalamus in the rat. Journal of Comparative Neurology 184, 107–125.Google Scholar
  15. Jones, E. G. (1985) The Thalamus. New York: Plenum Press.Google Scholar
  16. Katz, L. C., Burkhalter, A. & Dreyer, W. D. (1984) Fluorescent latex microspheres as a retrograde neuronal marker in vivo and in vitro studies of visual cortex. Nature 310, 498–500.Google Scholar
  17. Keay, K. A., Feil, K., Gordon, B. D., Herbert, H. & Bandler, R. (1997) Spinal afferents to functionally distinct periaqueductal grey columns in the rat: An anterograde and retrograde tracing study. Journal of Comparative Neurology 385, 207–229.Google Scholar
  18. Kemplay, S. K. & Webster, K. E. (1986) A qualitative and quantitative analysis of the distributions of cells in the spinal cord and spinomedullary junction projecting to the thalamus of the rat. Neuroscience 17, 769–789.Google Scholar
  19. Kevetter, G. A. & Willis, W. D. (1982) Spinothalamic tract cells in the rat lumbar cord with collaterals to the medullary reticular formation. Brain Research 238, 181–185.Google Scholar
  20. Kim, U., Gregory, E. & Hall, W. C. (1992) Pathway from the zona incerta to the superior colliculus in the rat. Journal of Comparative Neurology 321, 555–575.Google Scholar
  21. Kohler, C., Hagland, L. & Swanson, L. W. (1984) A diffuse α-MSH-immunoreactive projection to the hippocampus and spinal cord from individual neurons in the lateral hypothalamic area and zona incerta. Journal of Comparative Neurology 223, 501–514Google Scholar
  22. Kolmac, C. I. & Mitrofanis, J. (1997) Organisation of the reticular thalamic projection to the intralaminar and midline nuclei in rats. Journal of Comparative Neurology 377, 165–178.Google Scholar
  23. Kolmac, C. I., Power, B. D. & Mitrofanis, J. (1998) Patterns of connections between zona incerta and brainstem in rats. Journal of Comparative Neurology 396, 544–555.Google Scholar
  24. Lechner, J., Leah, J. D. & Zimmerman, M. (1993) Brainstem peptidergic neurons projecting to the medial and lateral thalamus and zona incerta in the rat. Brain Research 603, 47–56.Google Scholar
  25. Luppi, P. H., Fort, P. & Jouvet, M. (1990) Iontophoretic application of conjugated cholera toxin B subunit (CTB) combined with immunohistochemistry of neurochemical substances: A method for transmitter identification of retrogradely labelled neurons. Brain Research 534, 209–224.Google Scholar
  26. Ma, W., Peschanski, M. & Besson, J. M. (1989) The overlap of spinothalamic and dorsal column nuclei projections in the ventrobasal complex of the rat thalamus: A double anterograde labelling study using light microscopy analysis. Journal of Comparative Neurology 245, 531–540.Google Scholar
  27. Maslany, S., Crockett, D. P. & Egger, M. D. (1992) Organisation of cutaneous primary afferents projecting to the dorsal horn in the rat: WGA-HRP versus B-HRP. Brain Research 569, 123–135.Google Scholar
  28. May, P. J., Sun, W. & Hall, W. C. (1997) Reciprocal connections between the zona incerta and the pretectum and superior colliculus of the cat. Neuroscience 77, 1091–1114.Google Scholar
  29. Mehle, W. R. (1969) Some neurological species differences. Annuals New York Academic of Science 167, 424–468.Google Scholar
  30. MenÉtrey, D., Roudier, F. & Besson, J. M. (1983) Pineal neurons reaching the lateral reticular nucleus as studied in the rat by retrograde transport of horseradish peroxidase. Journal of Comparative Neurology 220, 439–452.Google Scholar
  31. Mitrofanis, J. & Defonseka, R. (2001) Organisation of the connections between the zona incerta and the interposed nucleus. Anatomy of Embryology 204, 153–159.Google Scholar
  32. Mogenson, G. J., Swanson, L. W. & Wu, M. (1985) Evidence that projections from substantia innominata to the zona incerta and mesencephalic locomotor region contribute to locomotor activity. Brain Research 334, 65–76.Google Scholar
  33. Mok, D. & Mogenson, G. J. (1986) Convergence of signals in the zona incerta for angiotensin-mediated and osmotic thirst. American Journal of Physiology 251, 823–832.Google Scholar
  34. Molander, C. & Grant, G. (1995) The cytoarchitecture of the spinal cord. In: The Rat Nervous System (2nd Edn., edited by PAXINOS, G.), Sydney, Australia: Academic Press.Google Scholar
  35. Mouton, L. J. & Holstege, G. (2000) Segmental and laminar organisation of the spinal neurons projecting to the periaqueductal grey (PAG) in the cat suggests the existence of at least five separate clusters of spino PAG neurones. Journal of Comparative Neurology 428, 389–410.Google Scholar
  36. Nahin, R. L., Madsen, A. M. & Giesler, G. J. (1986) Functional location of the ascending axons of neurons adjacent to the spinal cord central canal in the rat. Brain Research 384, 367–372.Google Scholar
  37. Newman, H. M., Stevens, R. T. & Apkarian, A. V. (1996) Direct spinal projections to limbic and striatal areas: Anterograde transport studies from the upper cervical spinal cord and the cervical enlargement in the squirrel, monkey, and rat. Journal of Comparative Neurology 365, 640–658.Google Scholar
  38. Nicolelis, M. A., Chapin, J. K. & Lin, R. C. (1992) Somatotopic maps within the zona incerta relay parallel GABAergic somatosensory pathways to the neocortex, superior colliculus and brainstem. Brain Research 577, 134–141.Google Scholar
  39. Paxinos, G. & Watson, C. J. (1986) The rat brain in stereotaxic coordinates. (2nd Edn.) Academic Press.Google Scholar
  40. Peschanski, M., Manyth, P. W. & Besson, J. M. (1983) Spinal afferents to the ventrobasal thalamic complex in the rat: An anatomical study using wheat-germagglutinin conjugated to horseradish peroxidase Brain Research 278, 240–244.Google Scholar
  41. Pfaller, K. & Arvidsson, J. (1988) Central distribution of trigeminal and upper cervical afferents in the rat studied by anterograde transport of horseradish peroxidase conjugated to wheat germ agglutinin. Journal of Comparative Neurology 268, 91–108.Google Scholar
  42. Power, B. D., Kolmac, C. I. & Mitrofanis, J. (1999) Evidence for a large projection from the zona incerta to the dorsal thalamus. Journal of Comparative Neurology 404, 554–565.Google Scholar
  43. Power, B. D. & Mitrofanis, J. (1999a) Evidence for extensive interconnections within the zona incerta in rats. Neuroscience Letters 267, 9–12.Google Scholar
  44. Power, B. D. & Mitrofanis, J. (1999b) Specificity of projection among cells of the zona incerta. Journal of Neurocytology 28, 481–493.Google Scholar
  45. Qin, C., Chandler, M. J., Miller, K. E. & Foreman, R. D. (1999) Chemical activation of cervical cell bodies: Effects on responses to colorectal distension in lumbosacral spinal cord of rats. Journal of Neurophysiology 82, 4323–3433.Google Scholar
  46. Reardon, F. M. & Mitrofanis, J. (2000) Organisation of the amygdalothalamic pathways in rats. Anatomy and Embryology 201, 75–84.Google Scholar
  47. Ricardo, J. A. (1981) Efferent connections of the subthalamic region in the rat. II. The zona incerta. Brain Research 214, 43–60.Google Scholar
  48. Roger, M. & Cadusseau, J. (1985) Afferents to the zona incerta in the rat: A combined retrograde and anterograde study. Journal of Comparative Neurology 241, 480–492.Google Scholar
  49. Romanowski, C. A. J., Mitchell, I. J. & Crossman, A. R. (1985) The organisation of the efferent projections of the zona incerta. Journal of Anatomy 143, 75–95.Google Scholar
  50. Shammah-Lagnado, S. J., Negrao, N. & Ricardo, J. A. (1985) Afferent connections of the zona incerta: A horseradish peroxidase study in the rat. Neuroscience 15, 109–134.Google Scholar
  51. Shaw, V. E. & Mitrofanis, J. (2001) Body maps in the thalamus. Proceedings of Australian Neuroscience Society 12, 213.Google Scholar
  52. Shiosaka, S., Kawai, Y., shibasaki, T. & Tohyama, M. (1985) The descending ?MSHergic (?melanocyte stimulating hormonergic) projections from the zona incerta and lateral hypothalamic area to the inferior colliculus and spinal cord in the rat. Brain Research 338, 371–375.Google Scholar
  53. Tanaka, J. & Seto, K. (1988) Neurons in the lateral hypothalamic area and zona incerta with ascending projections to the subfornical organ area in the rat. Brain Research 456, 397–400.Google Scholar
  54. Tracey, D. J. (1995) Ascending and descending pathways in the spinal cord. In: The Rat Nervous System (2nd Edn., edited by PAXINOS, G.), Sydney, Australia: Academic Press.Google Scholar
  55. Tracey, D. J. & Waite, P. M. E. (1995) Somatosensory system. In: The Rat Nervous System (2nd Edn., edited by Paxinos, G.), Sydney, Australia: Academic Press.Google Scholar
  56. Vaccaro, T. & Mitrofanis, J. (1997) Does the reticular thalamic nucleus project to the midbrain? Journal of Neurocytology 26, 223–239.Google Scholar
  57. Wagner, C K., Eaton, M. J., Moore, K. E. & Lookingland, K. J. (1995) Efferent projections from the region of the medial zona incerta containing A13 dopaminergic neurones:APHAL anterograde tract tracing study in the rat. Brain Research 677, 229–237.Google Scholar
  58. Wall, P D. (1967) The laminar organisation of dorsal horn and effects of descending impulses. Journal of Physiology (London) 188, 403–423.Google Scholar
  59. Wang, C Willis, W. D. & Westlund, K. N. (1999) Ascending projections from the area around the spinal cord central canal: A Phaseolus vulgaris leucoagglutinin study in rats. Journal of Comparative Neurology 415, 341–367.Google Scholar
  60. Watanabe, K & Kawana, E. (1982) The cells of origin of incertofugal projections to the tectum, thalamus, tegmentum, and spinal cord in rat: A study using autoradiographic and horseradish peroxidase methods. Neuroscience 10, 2389–2406.Google Scholar
  61. Yen, C. T., Fu, T. S. & Chen, R. C. (1989) Distribution of thalamic nociceptive neurons activated from the tail of the rat. Brain Research 498, 118–122Google Scholar

Copyright information

© Kluwer Academic Publishers 2001

Authors and Affiliations

  1. 1.Department of Anatomy and HistologyUniversity of SydneyAustralia

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