Skip to main content
SpringerLink
Log in

Evidence for sequential degeneration of the neurons in the intermediate zone of the spinal cord in amyotrophic lateral sclerosis: a topographic and quantitative investigation

  • Regular Papers
  • Published:
Acta Neuropathologica Aims and scope Submit manuscript

Summary

To elucidate the degenerating mechanism of the neurons in the intermediate zone of the spinal cord in classical amyotrophic lateral sclerosis (ALS), the spinal neurons in a patient with ALS, whose muscular strength was fairly well preserved up to death, were examined quantitatively and topographically, and compared with the data of advanced ALS patients and age-matched control subjects reported previously. In advanced ALS patients, anterior horn cells completely disappeared and the medium-sized (nuclear area; 71–150 μm2) and large (nuclear area; greater than 151 μm2) neurons in the intermediate zone were severely reduced. In the present case, however, the loss of anterior horn cells was severe but the degree was not equal to that of advanced ALS patients, and the neurons in the intermediate zone were quite well preserved. The finding indicates that the primary degeneration may occur in the anterior horn cells and the neurons in the intermediae zone degenerate sequentially in the spinal gray matter in ALS.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Barilari MG, Kuypers HGJM (1969) Propriospinal fibers interconnecting the spinal enlargements in the cat. Brain Res 14:321–330

    Google Scholar 

  2. Brownell B, Oppenheimer DR, Hughes JT (1970) The central nervous system in motor neurone disease. J Neurol Neurosurg Psychiatry 33:338–357

    Google Scholar 

  3. Burton H, Locwy AD (1977) Projections to the spinal cord from medullary somatosensory relay nuclei. J Comp Neurol 173:773–792

    Google Scholar 

  4. Carpenter MB, Sutin J (1983) Spinal cord: gross anatomy and internal structure. In: Human neuroanatomy, 8th edn. Williams & Wilkins, Baltimore, pp 232–264

    Google Scholar 

  5. Carstens E, Trevino DL (1978) Laminar origins of spinothalamic projections in the cat as determined by the retrograde transport of horseradish peroxidase. J Comp Neurol 182:151–166

    Google Scholar 

  6. Chaouch A, Menetrey D, Binder D, Besson JM (1983) Neurons at the origin of the medial component of the bulbopontine spinoreticular tract in the rat: an anatomical study using horseradish peroxidase retrograde transport. J Comp Neurol 214:309–320

    Google Scholar 

  7. Cruz AR, Lison L (1963) Nucleocytoplasmic allometric relation in some nerve cells. Z Mikrosk Anat Forsch 70:139–167

    Google Scholar 

  8. Holmes G (1909) The pathology of amyotrophic lateral sclerosis. Rev Neurol Psychiatry 7:693–725

    Google Scholar 

  9. Ikuta F, Makifuchi T, Ichikawa T (1979) Comparative studies of tract degeneration in ALS and other disorders. In: Tsubaki T, Toyokura Y (eds) Amyotrophic lateral sclerosis. University of Tokyo Press, Tokyo, pp 177–200

    Google Scholar 

  10. Ikuta F, Makifuchi T, Ohama E, Takeda S, Oyanagi K, Nakashima S, Motegi T (1982) Tract degeneration of the human spinal cord: some observations on ALS and hemispherectomized humans. Shinkei Kenkyu no Shimpo 26:710–736

    Google Scholar 

  11. Itahara K, Konno H, Yamamoto T, Iwasaki Y (1984) Somatic motor and internuncial neurons in the spinal anterior horn in Shy-Drager syndrome and amyotrophic lateral sclerosis. In: Annual report of the research committee of CNS degenerative diseases. The Ministry of Health and Welfare of Japan, Tokyo, pp 169–174

    Google Scholar 

  12. Iwata M, Hirano A (1979) Current problems in the pathology of amyotrophic lateral sclerosis. Prog Neuropathol 4: 277–298

    Google Scholar 

  13. Jankowska E, Padel Y, Tanaka R (1975) Projections of pyramidal tract cells to α-motoneurones innervating hind-limb muscles in the monkey. J Physiol (London) 249:637–667

    Google Scholar 

  14. Kanemitsu A (1977) Etude quantitative de la cytoarchitecture de la moelle épinière chez la chat et le poulet. Proc Jpn Acad 53B:183–188

    Google Scholar 

  15. Kanemitsu A (1979) Quantitative study of spinal neurons in cases of ALS. In: Annual report of the Ministry of Education, Science and Culture. The Intractable Disease Research Committee, Japan, Tokyo, pp 142–146

    Google Scholar 

  16. Kanemitsu A (1980) The number and sizes of the neurons in the cervical enlargement in ALS. In: Annual report of the Ministry of Education, Science and Culture. The Intractable Disease Research Committee, Japan, Tokyo, pp 131–134

    Google Scholar 

  17. Kanemitsu A, Ikuta F (1977) Etude quantitative des neurones dans la moelle cervical chez un cas de l'hémisphérectomie cérébrale. Proc Jpn Acad 53B:189–193

    Google Scholar 

  18. Kato T, Hirano A, Kurland LT (1987) Asymmetric involvement of the spinal cord involving both large and small anterior horn cells in a case of familial amyotrophic lateral sclerosis. Clin Neuropathol 6:67–70

    Google Scholar 

  19. Kusuma A, en Donkelaar HJ (1980) Propriospinal fibers interconnecting the spinal enlargements in some quadrupedal reptiles. J Comp Neurol 193:871–891

    Google Scholar 

  20. Lawrence DG, Porter R, Redman SJ (1985) Corticomotoneuronal synapses in the monkey: light microscopic localization upon motoneurons of intrinsic muscles of the hand. J Comp Neurol 232:499–510

    Google Scholar 

  21. Lawyer T Jr, Netsky MG (1953) Amyotrophic lateral sclerosis. A clinicoanatomic study of fifty-three cases. Arch Neurol Psychiatry 69:171–192

    Google Scholar 

  22. Liu RPC (1983) Laminar origins of spinal projection neurons to the periaqueductal gray of the rat. Brain Res 264:118–122

    Google Scholar 

  23. Loewy AD, Schader RE (1977) A quantitative study of retrograde neuronal changes in Clarke's column. J Comp Neurol 171:65–82

    Google Scholar 

  24. Mann DMA, Yates PO (1974) Motor neuron disease: the nature of the pathogenic mechanism. J Neurol Neurosurg Psychiatry 37:1036–1046

    Google Scholar 

  25. Mannen H (1966) Contribution to the quantitative study of the nervous tissue: a new method for measurement of the volume and surface area of neurons. J Comp Neurol 126:75–90

    Google Scholar 

  26. Martin GF, Humbertson AO Jr, Laxson LC, Panneton WM, Tschismadia I (1979) Spinal projections from the mesencephalic and pontine reticular formation in the north American opossum: a study using axonal transport techniques. J Comp Neurol 187:373–400

    Google Scholar 

  27. Matsushita M (1969) Some aspects of the interneuronal connections in cat's spinal gray matter. J Comp Neurol 136:57–80

    Google Scholar 

  28. Matsushita M, Hosoya Y, Ikeda M (1979) Anatomical organization of the spinocerebellar system in the cat, as studied by retrograde transport of horseradish peroxidase. J Comp Neurol 184:81–106

    Google Scholar 

  29. Matsushita M, Ikeda M, Hosoya Y (1979) The location of spinal neurons with long descending axons (long descending propriospinal tract neurons) in the cat: a study with the horseradish peroxidase technique. J Comp Neurol 184:63–80

    Google Scholar 

  30. Matthews MR, Cowan WM, Powell TPS (1960) Transneuronal cell degeneration in the lateral geniculate nucleus of the macaque monkey. J Anat 94:145–169

    Google Scholar 

  31. Mizusawa H, Hirano A, Shintaku M (1987) Involvement of small neurons in anterior horn of the spinal cord in amyotrophic lateral sclerosis. Neurol Med (Tokyo) 27: 331–336

    Google Scholar 

  32. Molenaar I, Kuypers HGJM (1978) Cells of origin of propriospinal fibers and of fibers ascending to supraspinal levels. A HRP study in cat and rhesus monkey. Brain Res 152:429–450

    Google Scholar 

  33. Molinari HH (1984) Ascending somatosensory projections to the dorsal accessory olive: an anatomical study in cats. J Comp Neurol 223:110–123

    Google Scholar 

  34. Nyberg-Hansen R (1965) Sites and mode of termination of reticulo-spinal fibers in the cat. An experimental study with silver impregnation methods. J Comp Neurol 124:71–100

    Google Scholar 

  35. Oppenheimer DR (1984) Diseases of motor neurons and pyramidal tracts. In: Adams JH, Corsellis JAN, Duchen LW (eds) Greenfield's neuropathology, 4th edn. Edward Arnold, London, pp 726–747

    Google Scholar 

  36. Oyanagi K (1980) Amyotrophic lateral sclerosis: a quantitative study of nuclear sizes and localization of the neurons in the spinal gray matter. Shinkei Kenkyu no Shimpo 24:1212–1225

    Google Scholar 

  37. Oyanagi K, Ikuta F (1987) A morphometric reevaluation of Huntington's chorea with special reference to the large neurons in the neostriatum. Clin Neuropathol 6:71–79

    Google Scholar 

  38. Oyanagi K, Makifuchi T, Ikuta F (1983) A topographic and quantitative study of neurons in human spinal gray matter, with special reference to their changes in amyotrophic lateral sclerosis. Biomed Res 4:211–224

    Google Scholar 

  39. Oyanagi K, Takahashi H, Wakabayashi K, Ikuta F (1987) Selective involvement of large neurons in the neostriatum of Alzheimer's disease and senile dementia: a morphometric investigation. Brain Res 411:205–211

    Google Scholar 

  40. Oyanagi K, Takahashi H, Wakabayashi K, Ikuta F (1988) Selective decrease of large neurons in the neostriatum in progressive supranuclear palsy Brain Res 458:218–223

    Google Scholar 

  41. Ralston DD, Ralston HJ III (1985) The terminations of corticospinal tract axons in the macaque monkey. J Comp Neurol 242:325–337

    Google Scholar 

  42. Rexed B (1952) The cytoarchitectonic organization of the spinal cord in the cat. J Comp Neurol 96:415–496

    Google Scholar 

  43. Rexed B (1954) A cytoarchitectonic atlas of the spinal cord in the cat. J Comp Neurol 100:297–379

    Google Scholar 

  44. Scheibel ME, Scheibel AB (1966) Terminal axonal patterns in cat spinal cord. I. The lateral corticospinal tract. Brain Res 2:333–350

    Google Scholar 

  45. Schoen JHR (1964) Comparative aspects of the descending fibre systems in the spinal cord. Prog Brain Res 11:203–222

    Google Scholar 

  46. Skinner RD, Coulter JD, Adams RJ, Remmel RS (1979) Cells of origin of long descending propriospinal fibers connecting the spinal enlargement in cat and monkey determined by horseradish peroxidase and electrophysiological techniques. J Comp Neurol 188:443–454

    Google Scholar 

  47. Sobue G, Sahashi K, Takahashi A, Matsuoka Y, Muroga T, Sobue I (1983) Degenerating compartment and functioning compartment of motor neurons in ALS: possible process of motor neuron loss. Neurology 33:654–657

    Google Scholar 

  48. Swash M, Leader M, Brown A, Swettenham KW (1986) Focal loss of anterior horn cells in the cervical cord in motor neuron disease. Brain 109:939–952

    Google Scholar 

  49. Tsukagoshi H, Yanagisawa N, Oguchi K, Nagashima K, Murakami T (1979) Morphometric quantification of the cervical limb motor cells in controls and in amyotrophic lateral sclerosis. J Neurol Sci 41:287–297

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. The Center for Materials of Brain Diseases, Brain Research Institute, Niigata University, Asahimachi 1, 951, Niigata, Japan

    K. Oyanagi

  2. Department of Pathology; Brain Research Institute, Niigata University, Asahimachi 1, 951, Niigata, Japan

    F. Ikuta

  3. Department of Neurology, Shinrakuen Hospital, Nishi-Ariakemachi 1-27, 950-21, Niigata, Japan

    Y. Horikawa

Authors
  1. K. Oyanagi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. F. Ikuta
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Y. Horikawa
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Supported in part by a Grant-in-Aid for Scientific Research (A) No. 60440046 from the Ministry of Education, Science and Culture, Japan

Rights and permissions

Reprints and permissions

About this article

Cite this article

Oyanagi, K., Ikuta, F. & Horikawa, Y. Evidence for sequential degeneration of the neurons in the intermediate zone of the spinal cord in amyotrophic lateral sclerosis: a topographic and quantitative investigation. Acta Neuropathol 77, 343–349 (1989). https://doi.org/10.1007/BF00687368

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00687368

Key words

Search

Navigation