Exogenous testosterone reverses age-related atrophy in a spinal neuromuscular system

Hormones and Behavior

Volumn 51, Issue 1, 2007, Pages 20-30

  Fargo, Keith N ^a   Iwema, Carrie L ^a   Clark Phelps, Marie C ^a   Sengelaub, Dale R ^a  

^a INDIANA UNIVERSITY   (United States)

Author keywords

Aging; Bulbocavernosus; Dendrites; Ischiocavernosus; Levator ani; Motoneurons; SNB

Indexed keywords

ANDROGEN; TESTOSTERONE;

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL LOSS; CELL NUCLEUS; CONTROLLED STUDY; DENDRITE; DRUG EFFECT; INNERVATION; LUMBAR SPINE; MALE; MORPHOLOGY; MOTONEURON; MUSCLE MASS; NEUROMUSCULAR SYSTEM; NONHUMAN; PENIS; PRIORITY JOURNAL; RAT; SEXUAL BEHAVIOR; SOMATIC CELL; SPINAL MUSCULAR ATROPHY;

AGING; ANIMALS; ATROPHY; BODY WEIGHT; CELL COUNT; CELL SIZE; MALE; MOTOR NEURONS; MUSCLE, SKELETAL; PENIS; RATS; RATS, INBRED F344; SPINAL CORD; TESTOSTERONE;

EID: 33751525334     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2006.07.006     Document Type: Article

References (94)

1. Andrews T.J., Li D., Halliwell J., and Cowen T. The effect of age on dendrites in the rat superior cervical ganglion. J. Anat. 184 (1994) 111-117
2. Aperghis M., Johnson I.P., Patel N., Khadir A., Cannon J., and Goldspink G. Age, diet and injury affect the survival of facial motoneurons. Neuroscience 117 (2003) 97-104
3. Breedlove S.M., and Arnold A.P. Hormone accumulation in a sexually dimorphic motor nucleus of the rat spinal cord. Science 210 (1980) 564-566
4. Breedlove S.M., and Arnold A.P. Sexually dimorphic motor nucleus in the rat lumbar spinal cord: response to adult hormone manipulation, absence in androgen-insensitive rats. Brain Res. 225 (1981) 297-307
5. Burke K.A., Widows M.R., and Sengelaub D.R. Synergistic effects of testosterone metabolites on the development of motoneuron morphology in a sexually dimorphic rat spinal nucleus. J. Neurobiol. 33 (1997) 1-10
6. Burke K.A., Kuwajima M., and Sengelaub D.R. Aromatase inhibition reduces dendritic growth in a sexually dimorphic rat spinal nucleus. J. Neurobiol. 38 (1999) 301-312
7. Chambers K.C., and Phoenix C.H. Testosterone and the decline of sexual behavior in aging male rats. Behav. Neural Biol. 40 (1984) 87-97
8. Chambers K.C., and Phoenix C.H. Testosterone is more effective than dihydrotestosterone plus estradiol in activating sexual behavior in old male rats. Neurobiol. Aging 7 (1986) 127-132
9. Chambers K.C., Thornton J.E., and Roselli C.E. Age-related deficits in brain androgen binding and metabolism, testosterone, and sexual behavior of male rats. Neurobiol. Aging 12 (1991) 123-130
10. Chan K.M., Doherty T.J., and Brown W.F. Contractile properties of human motor units in health, aging, and disease. Muscle Nerve 24 (2001) 1113-1133
11. Clemens L.G., Wee B.E.F., Weaver D.R., Roy E.J., Goldman B.D., and Rakerds B. Retention of masculine sexual behavior following castration in male B6D2F1 mice. Physiol. Behav. 42 (1988) 69-76
12. Coggeshall R.E. A consideration of neural counting methods. Trends Neurosci. 15 (1992) 9-13
13. Cruz-Sánchez F.F., Moral A., Tolosa E., de Belleroche J., and Rossi M.L. Evaluation of neuronal loss, astrocytosis and abnormalities of cytoskeletal components of large motor neurons in the human anterior horn in aging. J. Neural Transm. 105 (1998) 689-701
14. Cupp C.J., and Uemura E. Age-related changes in prefrontal cortex of Macaca mulatta: quantitative analysis of dendritic branching patterns. Exp. Neurol. 69 (1980) 143-163
15. Davidson J.M., Stefanick M.L., Sachs B.D., and Smith E.R. Role of androgen in sexual reflexes of the male rat. Physiol. Behav. 21 (1978) 141-146
16. Davidson J.M., Kwan M., and Greenleaf W.J. Hormonal replacement and sexuality in men. Clin. Endocrinol. Metab. 11 (1982) 599-623
17. Davidson J.M., Chen J.J., Crapo L., Gray G.D., Greenleaf W.J., and Catania J.A. Hormonal changes and sexual function in aging men. J. Clin. Endocrinol. Metab. 57 (1983) 71-77
18. Fargo K.N., and Sengelaub D.R. Exogenous testosterone prevents motoneuron atrophy induced by contralateral motoneuron depletion. J. Neurobiol. 60 (2004) 348-359
19. Fargo K.N., and Sengelaub D.R. Testosterone manipulation protects motoneurons from dendritic atrophy after contralateral motoneuron depletion. J. Comp. Neurol. 469 (2004) 96-106
20. Feldman M.L. Dendritic changes in aging rat brain: pyramidal cell dendrite length and ultrastructure. In: Nandy K., and Sherwin I. (Eds). The Aging Brain and Senile Dementia (1977), Plenum Press, New York 23-37
21. Foresta C., Caretta N., Garolla A., and Rossato M. Erectile function in elderly: role of androgens. J. Endocrinol. Invest. 26 3 Suppl. (2003) 77-81
22. Foresta C., Caretta N., Rossato M., Garolla A., and Ferlin A. Role of androgens in erectile function. J. Urol. 171 6 Pt. 1 (2004) 2358-2362
23. Forger N.G., and Breedlove S.M. Seasonal variation in mammalian striated muscle mass and motoneuron morphology. J. Neurobiol. 18 (1987) 155-165
24. Frankel A.I., and Mock E.J. Time course of hormonal response to sexual behavior in aging male rats. Exp. Gerontol. 16 (1981) 363-369
25. Garban H., Marquez D., Cai L., Rajfer J., and Gonzalez-Cadavid N.F. Restoration of normal adult penile erectile response in aged rats by long-term treatment with androgens. Biol. Reprod. 53 (1995) 1365-1372
26. Ghanadian R., Lewis J.G., and Chisholm J.D. Serum testosterone and dihydrotestosterone changes with age in rat. Steroids 25 (1975) 753-762
27. Goldstein L.A., and Sengelaub D.R. Motoneuron morphology in the dorsolateral nucleus of the rat spinal cord: normal development and androgenic regulation. J. Comp. Neurol. 338 (1993) 588-600
28. Goldstein L.A., and Sengelaub D.R. Differential effects of dihydrotestosterone and estrogen on the development of motoneuron morphology in a sexually dimorphic rat spinal nucleus. J. Neurobiol. 25 (1994) 878-892
29. Goldstein L.A., Kurz E.M., and Sengelaub D.R. Androgen regulation of dendritic growth and retraction in the development of a sexually dimorphic spinal nucleus. J. Neurosci. 10 (1990) 935-946
30. Goldstein L.A., Kurz E.M., Kalkbrenner A.E., and Sengelaub D.R. Changes in dendritic morphology of rat spinal motoneurons during development and after unilateral target deletion. Dev. Brain Res. 73 (1993) 151-163
31. Gray G.D. Age-related changes in penile erections and circulating testosterone in middle-aged male rats. In: Finch C.E. (Ed). Advances in Experimental Medicine and Biology (1978), Plenum Press, New York 149-158
32. Gray G.D. Changes in the levels of luteinizing hormone and testosterone in the circulation of ageing male rats. J. Endocrinol. 76 (1978) 551-552
33. Gray G.D., Smith E.R., and Davidson J.M. Hormonal regulation of penile erection in castrated male rats. Physiol. Behav. 24 (1980) 463-468
34. Gray G.D., Smith E.R., Dorsa D.M., and Davidson J.M. Sexual behavior and testosterone in middle-aged male rats. Endocrinology 109 (1981) 1597-1604
35. Gruenewald D.A., and Matsumoto A.M. Testosterone supplementation therapy for older men: potential benefits and risks. J. Am. Geri. Soc. 51 (2003) 101-115 (Discussion 115)
36. Grunt J.A., and Young W.C. Changes in strength of sex drive in the male guinea pig from age 22 to 439 days. Anat. Rec. 113 (1952) 596
37. Hart B.L. Testosterone regulation of sexual reflexes in spinal male rats. Science 155 (1967) 1283-1284
38. Hart B.L., and Haugen C.M. Activation of sexual reflexes in male rats by spinal implantation of testosterone. Physiol. Behav. 3 (1968) 735-738
39. Hart B.L., and Melese-D'Hospital P.Y. Penile mechanisms and the role of the striated penile muscles in penile reflexes. Physiol. Behav. 31 (1983) 807-813
40. Hart B.L., Wallach S.J., and Melese-d'Hospital P.Y. Differences in responsiveness to testosterone of penile reflexes and copulatory behavior of male rats. Horm. Behav. 17 (1983) 274-283
41. Hashizume K., and Kanda K. Neuronal dropout is greater in hindlimb motor nuclei than in forelimb motor nuclei in aged rats. Neurosci. Lett. 113 (1990) 267-269
42. Hashizume K., and Kanda K. Differential effects of aging on motoneurons and peripheral nerves innervating the hindlimb and forelimb muscles of rats. Neurosci. Res. 22 (1995) 189-196
43. Hashizume K., Kanda K., and Burke R.E. Medial gastrocnemius motor nucleus in the rat: age-related changes in the number and size of motoneurons. J. Comp. Neurol. 269 (1988) 425-430
44. Hebbeler S.L., and Sengelaub D.R. Development of a sexually dimorphic neuromuscular system in male rats after spinal transection: morphologic changes and implications for estrogen sites of action. J. Comp. Neurol. 467 (2003) 80-96
45. Hebbeler S.L., Verhovshek T., and Sengelaub D.R. Ovariectomy attenuates dendritic growth in hormone-sensitive spinal motoneurons. J. Neurobiol. 48 (2001) 301-314
46. Hebbeler S.L., Verhovshek T., and Sengelaub D.R. N-methyl-d-aspartate receptor blockade inhibits estrogenic support of dendritic growth in a sexually dimorphic rat spinal nucleus. J. Comp. Neurol. 451 (2002) 142-152
47. Hinds J.W., and McNelly N.A. Aging of the rat olfactory bulb: growth and atrophy of constituent layers and changes in size and number of mitral cells. J. Comp. Neurol. 171 (1977) 345-368
48. Hsu H.K., Hsu C., Yu J.Y., and Peng M.T. Effects of long-term testosterone replacement on copulatory activity in old male rats. Gerontology 32 (1986) 10-17
49. Johnson H., Hökfelt T., and Ulfhake B. Decreased expression of TrkB and TrkC mRNAs in spinal motoneurons of aged rats. Eur. J. Neurosci. 8 (1996) 494-499
50. Kalb R.G. Regulation of motor neuron dendrite growth by NMDA receptor activation. Development 120 (1994) 3063-3071
51. Kaler L.W., and Neaves W.B. The androgen status of aging male rats. Endocrinology 108 (1981) 712-719
52. Katagiri T., Gibson S.J., Su H.C., and Polak J.M. Composition and central projections of the pudendal nerve in the rat investigated by combined peptide immunocytochemistry and retrograde fluorescent labelling. Brain Res. 372 (1986) 313-322
53. Kawamura Y., O'Brien P., Okazaki H., and Dyck P.J. Lumbar motoneurons of man II: the number and diameter distribution of large- and intermediate-diameter cytons in "motoneuron columns" of spinal cord of man. J. Neuropathol. Exp. Neurol. 36 (1977) 861-870
54. Kurz E.M., Sengelaub D.R., and Arnold A.P. Androgens regulate the dendritic length of mammalian motoneurons in adulthood. Science 232 (1986) 395-398
55. Kurz E.M., Brewer R.G., and Sengelaub D.R. Hormonally mediated plasticity of motoneuron morphology in the adult rat spinal cord: a cholera toxin-HRP study. J. Neurobiol. 22 (1991) 976-988
56. Lamberts S.W., van den Beld A.W., and van der Lely A.J. The endocrinology of aging. Science 278 (1997) 419-424
57. Larsson K. Sexual activity in senile male rats. J. Gerontol. 13 (1958) 136-139
58. Larsson K. Individual differences in reactivity to androgen in male rats. Physiol. Behav. 1 (1966) 255-258
59. Larsson K. Features of the neuroendocrine regulation of masculine sexual behavior. In: Beyer C. (Ed). Endocrine Control of Sexual Behavior (1979), Raven Press, New York 77-163
60. Leedy M.G., Beattie M.S., and Bresnahan J.C. Testosterone-induced plasticity of synaptic inputs to adult mammalian motoneurons. Brain Res. 424 (1987) 386-390
61. Leslie M., Forger N.G., and Breedlove S.M. Does androgen affect axonal transport of cholera toxin HRP in spinal motoneurons?. Neurosci. Lett. 126 (1991) 199-202
62. Leslie M., Forger N.G., and Breedlove S.M. Sexual dimorphism and androgen effects on spinal motoneurons innervating the rat flexor digitorum brevis. Brain Res. 561 (1991) 269-273
63. Machado-Salas J., Scheibel M.E., and Scheibel A.B. Morphologic changes in the hypothalamus of the old mouse. Exp. Neurol. 57 (1977) 102-111
64. Machado-Salas J., Scheibel M.E., and Scheibel A.B. Neuronal changes in the aging mouse: spinal cord and lower brain stem. Exp. Neurol. 54 (1977) 504-512
65. Matsumoto A. Hormonally induced neuronal plasticity in the adult motoneurons. Brain Res. Bull. 44 (1997) 539-547
66. Matsumoto A. Synaptic changes in the perineal motoneurons of aged male rats. J. Comp. Neurol. 400 (1998) 103-109
67. Matsumoto A. Age-dependent changes in phosphorylated cAMP response element-binding protein immunoreactivity in motoneurons of the spinal nucleus of the bulbocavernosus of male rats. Neurosci. Lett. 279 (2000) 117-120
68. Matsumoto A. Androgen stimulates neuronal plasticity in the perineal motoneurons of aged male rats. J. Comp. Neurol. 430 (2001) 389-395
69. Matsumoto A. Age-related changes in nuclear receptor coactivator immunoreactivity in motoneurons of the spinal nucleus of the bulbocavernosus of male rats. Brain Res. 943 (2002) 202-205
70. Matsumoto A., and Prins G.S. Age-dependent changes in androgen receptor immunoreactivity in motoneurons of the spinal nucleus of the bulbocavernosus of male rats. Neurosci. Lett. 243 (1998) 29-32
71. Matsumoto A., and Prins G.S. Androgenic regulation of expression of androgen receptor protein in the perineal motoneurons of aged male rats. J. Comp. Neurol. 443 (2002) 383-387
72. Matsumoto A., Arnold A.P., Zampighi G.A., and Micevych P.E. Androgenic regulation of gap junctions between motoneurons in the rat spinal cord. J. Neurosci. 8 (1988) 4177-4183
73. Matsumoto A., Micevych P.E., and Arnold A.P. Androgen regulates synaptic input to motoneurons of the adult rat spinal cord. J. Neurosci. 8 (1988) 4168-4176
74. McKenna K.E., and Nadelhaft I. The organization of the pudendal nerve in the male and female rat. J. Comp. Neurol. 248 (1986) 532-549
75. Meisel R.L., O'Hanlon J.K., and Sachs B.D. Differential maintenance of penile responses and copulatory behavior by gonadal hormones in castrated male rats. Horm. Behav. 18 (1984) 56-64
76. Mesulam M.M. Tracing Neural Connections with Horseradish Peroxidase (1982), Wiley, Chichester
77. Minnick R.S., Warden C.J., and Arieti S. The effects of sex hormones on the copulatory behavior of senile white rats. Science 103 (1946) 749-750
78. Sachs B.D. Role of striated penile muscles in penile reflexes, copulation, and induction of pregnancy in the rat. J. Reprod. Fertil. 66 (1982) 433-443
79. Sasaki M., and Arnold A.P. Androgenic regulation of dendritic trees of motoneurons in the spinal nucleus of the bulbocavernosus: reconstruction after intracellular iontophoresis of horseradish peroxidase. J. Comp. Neurol. 308 (1991) 11-27
80. Sato Y., Shibuya A., Adachi H., Kato R., Horita H., and Tsukamoto T. Restoration of sexual behavior and dopaminergic neurotransmission by long term exogenous testosterone replacement in aged male rats. J. Urol. 160 (1998) 1572-1575
81. Scheibel M.E., Lindsay R.D., Tomiyasu U., and Scheibel A.B. Progressive dendritic changes in aging human cortex. Exp. Neurol. 47 (1975) 392-403
82. Schrøder H.D. Organization of the motoneurons innervating the pelvic muscles of the male rat. J. Comp. Neurol. 192 (1980) 567-587
83. Smith E.R., Damassa D.A., and Davidson J.M. Hormone administration: peripheral and intracranial implants. In: Meyer R.D. (Ed). Methods in Psychobiology vol. III (1977), Academic Press, New York 259-279
84. Smith E.R., Stefanick M.L., Clark J.T., and Davidson J.M. Hormones and sexual behavior in relationship to aging in male rats. Horm. Behav. 26 (1992) 110-135
85. Stone C.P. Copulatory activity in adult male rats following castration and injections of testosterone propionate. Endocrinology 24 (1939) 165-174
86. Ueyama T., Arakawa H., and Mizuno N. Central distribution of efferent and afferent components of the pudendal nerve in rat. Anat. Embryol. (Berl.) 177 (1987) 37-49
87. Ulfhake B., Bergman E., Edström E., Fundin B.T., Johnson H., Kullberg S., and Ming Y. Regulation of neurotrophin signaling in aging sensory and motoneurons: dissipation of target support?. Mol. Neurobiol. 21 (2001) 109-135
88. Vaughan D.W. Age-related deterioration of pyramidal cell basal dendrites in rat auditory cortex. J. Comp. Neurol. 171 (1977) 501-516
89. Venable J.H. Morphology of the cells of normal, testosterone-deprived and testosterone-stimulated levator ani muscles. Am. J. Anat. 119 (1966) 271-301
90. Wainman P., and Shipounoff G.C. The effects of castration and testosterone propionate on the striated perineal musculature in the rat. Endocrinology 29 (1941) 975-978
91. Welle S. Cellular and molecular basis of age-related sarcopenia. Can. J. Appl. Physiol. 27 (2002) 19-41
92. West M.J., and Gundersen H.J.G. Unbiased stereological estimation of the number of neurons in the human hippocampus. J. Comp. Neurol. 296 (1990) 1-22
93. Xie Y.Y., Yao Z.B., and Wu W.T. Survival of motor neurons and expression of β-amyloid protein in the aged rat spinal cord. NeuroReport 11 (2000) 697-700
94. Xie Y., Yao Z., Chai H., Wong W.M., and Wu W. Expression and role of low-affinity nerve growth factor receptor (p75) in spinal motor neurons of aged rats following axonal injury. Dev. Neurosci. 2 (2003) 65-71