Loss of primary sensory neurons in the very old rat: Neuron number estimates using the disector method and confocal optical sectioning

Journal of Comparative Neurology

Volumn 396, Issue 2, 1998, Pages 211-222

  Bergman, E ^a   Ulfhake, B ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Aging; Dorsal root ganglia; Optical disector; Spinal cord; Stereology

Indexed keywords

NEUROFILAMENT PROTEIN;

AGED; AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR DISORDER; CELL COUNT; CELL LOSS; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; FEMALE; MALE; MUSCLE SPINDLE AFFERENT NERVE; MYELINATED NERVE; NONHUMAN; NONMYELINATED NERVE; PRIORITY JOURNAL; RAT; SPINAL GANGLION; STEREOLOGY;

ANIMALS; CELL COUNT; CELL SIZE; DISSECTION; FEMALE; GANGLIA, SPINAL; IMMUNOHISTOCHEMISTRY; MALE; MICROSCOPY, CONFOCAL; MICROTOMY; MOLECULAR WEIGHT; NEURONS, AFFERENT; OPTICS; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY;

EID: 0032577980     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19980629)396:2<211::AID-CNE6>3.0.CO;2-3     Document Type: Article

References (92)

1. Abdel-Rahman, T.A. and T. Cowen (1993) Neurodegeneration in sweat glands and skin of aged rats. J. Autonom. Nerv. Syst. 46:55-63.
2. Ahmad, A. and P.D. Spear (1993) Effects of aging on the size, density, and number of rhesus monkey lateral geniculate neurons. J. Comp. Neurol. 334:631-643.
3. Algeri, S., G. Calderini, G. Toffano, and F. Ponzio (1983) Neurotransmittor alterations in aging rats. In D. Samuel (ed): Aging of the Brain. New York: Raven Press, pp. 227-243.
4. Arvidsson, J., J. Ygge, and G. Grant (1986) Cell loss in lumbar dorsal root ganglia and transganglionic degeneration after sciatic nerve resection in the rat. Brain Res. 373:15-21.
5. Berg, B.N., A. Wolf, and H.S. Simms (1962) Degenerative lesions of spinal roots and peripheral nerves in aging rats. Gerontologia (Basel). 6: 72-80.
6. Bergman, E., H. Johnson, X. Zhang, T. Hökfelt, and B. Ulfhake (1996) Neuropeptides and neurotrophin receptor mRNAs in primary sensory neurons of aged rats. J. Comp. Neurol. 375:303-320.
7. Bolton, C.F., R.K. Winkelmann, and P.J. Dyck (1966) A quantitative study of Meissner's corpuscles in man. Neurology 16:1-9.
8. Bondok, A.A. and F.M. Sansone (1984) Retrograde and transganglionic degeneration of sensory neurons after a peripheral nerve lesion at birth. Exp. Neurol. 86:322-330.
9. Burek, J.D. and C.F. Hollander (1980) Experimental Gerontology. The Laboratory Rat, Vol. II. New York: Academic Press, pp. 149-159.
10. Burek, J.D., A.J. van der Kogel, and C.F. Hollander (1976) Degenerative myelopathy in three strains of aging rats. Vet. Pathol. 13:321-331.
11. Cauna, N. (1965) The effects of aging on the receptor organs of the human dermis. In W. Montagna (ed): Advances in Biology of the Skin. New York: Pergamon Press, pp. 63-96.
12. Cavanagh, J.B. (1964) The significance of the "dying back" process in experimental and human neurological disease. Int. Rev. Exp. Pathol. 3:219-267.
13. Cerimele, D., L. Celleno, and F. Serri (1990) Physiological changes in ageing skin. Br. J. Dermatol. 122:13-20.
14. Coggeshall, R.E. (1992) A consideration of neural counting methods. Trends Neurosci. 15:9-13.
15. Coggeshall, R.E., R. La Forte, and C.M. Klein (1990) Calibration of methods for determining numbers of dorsal root ganglion cells [published erratum appears in J. Neurosci. Methods 40(2-3):87-90, 1991]. J. Neurosci. Methods 35:187-194.
16. Coleman, P.D. and D.G. Flood (1987) Neuron numbers and dendritic extent in normal aging and Alzheimer's disease. Neurobiol. Aging 8:521-545.
17. Coons, A.H. (1958) Fluorescent antibody methods. In J.F. Danielli (ed): General Cytochemical Methods. New York: Academic Press, pp. 399-422.
18. Cotard-Bartley, M.P., J. Secchi, R. Glomot, and J.B. Cavanagh (1981) Spontaneous degenerative lesions of peripheral nerves in aging rats. Vet. Pathol. 18:110-113.
19. Cowen, T. and C. Thrasivoulou (1990) Cerebrovascular nerves in old rats show reduced accumulation of 5-hydroxytryptamine and loss of nerve fibres. Brain Res. 513:237-243.
20. Cowen, T., A.J. Haven, C. Wen Qin, D.D. Gallen, F. Franc, and G. Burnstock (1982) Development and ageing of perivascular adrenergic nerves in the rabbit. A quantitative fluorescence histochemical study using image analysis. J. Autonom. Nerv. Syst. 5:317-336.
21. Critchley, M. (1956) Neurological changes in the aged. In J.E. Moore, H.H. Merritt, and R.J. Masserlink (eds): The Neurologic and Psychiatric Aspects of the Disorders of Aging. Baltimore: Williams and Wilkins, pp. 198-223.
22. de Neeling, J.N., P.J. Beks, F.W. Bertelsmann, R.J. Heine, and L.M. Bouter (1994) Sensory thresholds in older adults: Reproducibility and reference values. Muscle Nerve 17:454-61.
23. Dhall, U., T. Cowen, A.J. Haven, and G. Burnstock (1986) Perivascular noradrenergic and peptide-containing nerves show different patterns of change during development and ageing in the guinea-pig. J. Autonom. Nerv. Syst. 16:109-126.
24. Dyck, P.J., J. Karnes, P.C. O'Brien, and I. Zimmerman (1984) Detection thresholds of cutaneous sensations in humans. In P.J. Dyck, P.K. Thomas, E.H. Lambert, and R. Bunge (eds): Peripheral Neuropathy. Philadelphia: Saunders, pp. 1103-1138.
25. Emery, L. and R. Singhal (1973) Changes associated with growth in the cells of the dorsal root ganglion in children. Dev. Med. Child. Neurol. 15:460-466.
26. Espejo, E.F. and D. Mir (1993) Structure of the rat's behaviour in the hot plate test. Behav. Brain Res. 56:171-176.
27. Feringa, E.R., G.W. Lee, H.L. Valshing, and W.J. Gilbertic (1985) Cell death in the adult rat dorsal root ganglion after hind limb amputation, spinal cord transaction, or both operations. Exp. Neurol. 87:349-357.
28. Ferrell, W.R., A. Crighton, and R.D. Sturrock (1992) Age-dependent changes in position sense in human proximal interphalangeal joints. Neuroreport 3:259-261.
29. Ferrer, T., M.J. Ramos, P. Perez-Sales, A. Perez-Jimenez, and E. Alvarez (1995) Sympathetic sudomotor function and aging. Muscle Nerve 18:395-401.
30. Foster, K.G., F.P. Ellis, C. Doré, A.N. Exton-Smith, and J.S. Weiner (1976) Sweat responses in the aged. Age Ageing 5:91-101.
31. Fundin, B.T., E. Bergman, and B. Ulfhake (1997) Alterations in mystacial pad innervation in the aged rat. Exp. Brain Res 117:324-340.
32. Gardner, E. (1940) Decrease in human neurones with age. Anat. Rec. 77:529-536.
33. Gescheider, G.A., S.J. Bolanowski, K.L. Hall, K.E. Hoffman, and R.T. Verrillo (1994) The effects of aging on information-processing channels in the sense of touch: I. Absolute sensitivity. Somatosens. Motor Res. 11:345-357.
34. Gilmore, S.A. (1972) Spinal nerve root degeneration in aging laboratory rats: A light microscopic study. Anat. Rec. 174:251-257.
35. Gold, B.G., W.C. Mobley, and S.F. Matheson (1991) Regulation of axonal caliber, neurofilament content, and nuclear localization in mature sensory neurons by nerve growth factor. J. Neurosci. 11:943-955.
36. Gundersen, H.J.G. (1986) Stereology of arbitrary particles. A review of unbiased number and size estimators and the presentation of some new ones, in memory of William R. Thompson. J. Microsc. 143:3-45.
37. Gundersen, H.J.G. and E.B. Jensen (1987) The efficiency of systematic sampling in stereology and its prediction. J. Microsc. 147:229-263.
38. Gundersen, H.J.G., P. Bagger, T.F. Bendtsen, S.M. Evans, L. Korbo, N. Marcussen, A. Moller, K. Nielsen, J.R. Nyengaard, B. Pakkenberg, F.B. Sorensen, A. Vesterby and M.J. West (1988a) The new stereological tools: Disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis. APMIS 96:857-881.
39. Gundersen, H.J.G., T.F. Bendtsen, L. Korbo, N. Marcussen, A. Moller, K. Nielsen, J.R. Nyengaard, B. Pakkenberg, F.B. Sorensen, A. Vesterby, and M.J. West (1988b) Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. APMIS 96:379-394.
40. Gutman, B. and V. Hanzlikova (1972) Age Changes in the Neuromuscular System. Bristol: Scientechnica Ltd.
41. Hashizume, K. and K. Kanda (1995) Differential effects of aging on motoneurons and peripheral nerves innervating the hindlimb and forelimb muscles of rats. Neurosci. Res. 22:189-196.
42. Hoffmann, P.N., D.W. Cleveland, J.W. Griffin, P.W. Landes, N.J. Cowan, and D.L. Price (1987) Neurofilament gene expression: A major determinant of axonal caliber. Proc. Natl. Acad. Sci. USA 84:3472-3476.
43. Jellinger, K. (1973) Neuroaxonal dystrophy: Its natural history and related disorders. In H.M. Jimmernan (ed): Progress in Neuropathology. London: Grune and Stratton, pp. 129-180.
44. Johnson, G.D. and G.M. de C Nogueira Araujo (1981) A simple method of reducing the fading of immunofluorescence during microscopy. J. Immunol. Methods 43:349-350.
45. Johnson, H., B. Ulfhake, A. Dagerlind, G.W. Bennett, K.C. Fone, and T. Hökfelt (1993) The serotoninergic bulbospinal system and brainstem-spinal cord content of serotonin-, TRH-, and substance P-like immunoreactivity in the aged rat with special reference to the spinal cord motor nucleus. Synapse 15:63-89.
46. Johnson, H., K. Mossberg, U. Arvidsson, F. Piehl, T. Hōkfelt, and B. Ulfhake (1995) Increase in alpha-CGRP and GAP-43 in aged motoneurons: A study of peptides, growth factors, and ChaT mRNA in the lumbar spinal cord of senescent rats with symptoms of hindlimb incapacities. J. Comp. Neurol. 359:69-89.
47. Kenney, W.L. and S.R. Fowler (1988) Methylcholine-activated eccrine sweat gland density and outputs as a function of age. J. Appl. Physiol. 13:1082-1086.
48. Knox, C.A., E. Kokmen, and P.J. Dyck (1989) Morphometric alteration of rat myelinated fibers with aging. J. Neuropathol. Exp. Neurol. 48:119-139.
49. Kokmen, E., R.W. Bossemeyer, Jr., J. Barney, and W.J. Williams (1977) Neurological manifestations of aging. J. Gerontol. 32:411-419.
50. Krinke, G. (1983) Spinal radiculoneuropathy in aging rats: Demyelination secondary to neuron dwindling? Acta Neuropathol. (Berlin). 59:63-69.
51. Kuchel, G.A., T. Poon, K. Irshad, C. Richard, J.P. Julien, and T. Cowen (1996) Decreased neurofilament gene expression is an index of selective axonal hypotrophy in ageing. Neuroreport 7:1353-1359.
52. La Forte, R.A., S. Melville, K. Chung, and R.E. Coggeshall (1991) Absence of neurogenesis of adult rat dorsal root ganglion cells. Somatosens. Motor Res. 8:3-7.
53. Langerman, L., M.I. Zakowski, B. Piskoun, and G.J. Grant (1995) Hot plate versus tail flick: Evaluation of acute tolerance to continuous morphine infusion in the rat model. J. Pharmacol. Toxicol. Methods 34:23-27.
54. Lawson, S.N., A.A. Harper, E.I. Harper, J.A. Garson, and B.H. Anderton (1984) A monoclonal antibody against neurofilament protein specifically labels a subpopulation of rat sensory neurons. J. Comp. Neurol. 228:263-272.
55. Macintosh, S.R. and D.C. Sinclair (1978) Age-related changes in the innervation of the rat snout. J. Anat. 125:149-154.
56. Madeira, M.D., N. Sousa, R.M. Santer, M.M. Paula-Barbosa, and H.J. Gundersen (1995) Age and sex do not affect the volume, cell numbers, or cell size of the suprachiasmatic nucleus of the rat: An unbiased stereological study. J. Comp. Neurol. 361:585-601.
57. Masoro, E.J. (1980) Mortality and characteristics of rat strains commonly used in aging research. Exp. Aging Res. 6:219-233.
58. Mione, M.C., K.K. Dhital, F. Amenta, and G. Burnstock (1988) An increase in the expression of neuropeptidergic vasodilator, but not vasoconstrictor, cerebrovascular nerves in aging rats. Brain Res. 460:103-113.
59. Mitsumori, K., K. Maita, and Y. Shirasu (1981) An ultrastructural study on spinal nerve roots and dorsal root ganglia in aging rats with spontaneous radiculoneuropathy. Vet. Pathol. 18:714-726.
60. Mittal, K.R. and F.H. Logmani (1987) Age-related reduction in 8th cervical ventral nerve root myelinated fiber diameters and number in man. J. Gerontol. 42:8-10.
61. Nagashima, K. and K. Oota (1974) A histopathological study of the human spinal ganglia. 1. Normal variations in aging. Acta Pathol. Japonica 24:333-44.
62. Navarro, X. and W.R. Kennedy (1990) Changes in sudomotor nerve territories with aging in the mouse. J. Autonom. Nerv. Syst. 31:101-107.
63. Ohta, M., K. Offord, and P.J. Dyck (1974) Morphometric evaluation of first sacral ganglia of man. J. Neurol. Sci. 22:73-82.
64. Parhad, I.M., J.N. Scott, L.A. Cellars, J.S. Bains, C.A. Krekoski, and A.W. Clark (1995) Axonal atrophy in aging is associated with a decline in neurofilament gene expression. J. Neurosci. Res. 41:355-66.
65. Pease, P.C. (1962) Buffered formaldehyde as a killing agent and primary fixative for electron microscopy. Anat. Rec. 142:342.
66. Platt, J.L. and A.F. Michael (1983) Retardation of fading and enhancement of intensity of immunofluorescence by p-phenylenediamine. J. Histochem. Cytochem. 31:840-842.
67. Pover, C.M. and R.E. Coggeshall (1991) Verification of the disector method for counting neurons, with comments on the empirical method. Anat. Rec. 231:573-578.
68. Price, J. (1985) An immunohistochemical and quantitative examination of dorsal root ganglion neuronal subpopulation. J. Neurosci. 5:2051-2059.
69. Quoniam, C., L. Hay. J.P. Roll, and F. Harlay (1995) Age effects on reflex and postural responses to propriomuscular inputs generated by tendon vibration. J. Gerontol. S A Biol. Sci. Med. Sci. 50:B155-B165.
70. Rambourg, A., Y. Clermont, and A. Beaudet (1983) Ultrastructural features of six types of neurons in dorsal root ganglia, J. Neurocytol. 12:47-66.
71. Rao, R.S. and G. Krinke (1983) Changes with age in the number and size of myelinated axons in the rat L4 dorsal spinal root. Acta Anat (Basel) 117:187-192.
72. Robbins, S., E. Waked, and J. McClaran (1995) Proprioception and stability: Foot position awareness as a function of age and footwear. Age Ageing 24:67-72.
73. Satorre, J., J. Cano, and F. Reinoso-Suarez (1985) Stability of the neuronal population of the dorsal lateral geniculate nucleus (LGNd) of aged rats. Brain Res. 339:375-377.
74. Schimirgk, K. and H. Ruttiger (1980) The touch corpuscles of the plantar surface of the big toe. Histological and histometrical investigations with respect to age. Eur. J. Neurol. 19:49-60.
75. Schmalbruch, H. (1987) The number of neurons in dorsal root ganglia L4-L6 of the rat. Anat. Rec. 219:315-322.
76. Schmidt, R.F., L.K. Wahren, and K.E. Hagbarth (1990) Multiunit neural responses to strong finger pulp vibration. I. Relationship to age. Acta Physiol. Scand. 140:1-10.
77. Sharma, A.K., S. Bajada, and P.K. Thomas (1980) Age changes in the tibial and plantar nerves of the rat. J. Anat. 130:417-428.
78. Spencer, P.S. and J. Ochoa (1981) Aging and cell structure. In J.E. Johnson, Jr. (ed): The Mammalian Peripheral Nervous System. New York: Plenum Press, pp. 35-103.
79. Sterio, D.C. (1984) The unbiased estimation of number and sizes of arbitrary particles using the disector. J. Microsc. 134:127-136.
80. Tal, M. and G.J. Bennett (1994) Extra-territorial pain in rats with a peripheral mononeuropathy: Mechano-hyperalgesia and mechano-allodynia in the territory of an uninjured nerve. Pain 57:375-382.
81. Tandrup, T. (1993) A method for unbiased and efficient estimation of number and mean volume of specified neuron subtypes in rat dorsal root ganglion. J. Comp. Neurol. 329:269-276.
82. Thomas, P.K., R.H. King, and A.K. Sharma (1980) Changes with age in the peripheral nerves of the rat. An ultrastructural study. Acta Neuropathol. (Berlin) 52:1-6.
83. Ulfhake, B., K. Carlsson, K. Mossberg, and P. Wallen (1994) Preparation, staining and examination of nervous tissue in the confocal scanning laser microscope. Neurosci. Prot. 94-050-01:1-28.
84. van Steenis, G. and R. Kroes (1971) Changes in the nervous system and musculature of old rats. Vet. Pathol. 8:320-332.
85. Wang, H., C. Rivero-Melian, B. Robertson, and G. Grant (1994) Transganglionic transport and binding of the isolectin B4 from Griffonia simplicifolia I in rat primary sensory neurons. Neuroscience 62:539-551.
86. West, M.J. (1993) New stereological methods for counting neurons. Neurobiol. Aging 14:275-285.
87. West, M.J. and H.J. Gundersen (1990) Unbiased stereological estimation of the number of neurons in the human hippocampus. J. Comp. Neurol. 296:1-22.
88. Wickelgren, I. (1996) Is hippocampal cell death a myth? [news] [see comments]. Science 271:1229-1230.
89. Winkelmann, R.K. (1965) Nerve changes in aging skin. In W. Montagna (ed): Advances in Biology of the Skin. New York: Pergamon Press, pp. 51-62.
90. Wood, J.W. and B.H. Anderton (1981) Monoclonal antibodies to mammalian neurofilaments. Biosci. Rep. 1:263-298.
91. Zamboni, I. and C. De Martino (1967) Buffered picric acid-formaldehyde: A new, rapid fixative for electron microscopy. J. Cell Biol. 35:148A.
92. Zhang, X., Z. Wiesenfeld-Hallin, and T. Hökfelt (1994) Effect of peripheral axotomy on expression of neuropeptide Y receptor mRNA in rat lumbar dorsal root ganglia. Eur. J. Neurosci. 6:43-57.