Fatigue reversibly reduced cortical and hippocampal dendritic spines concurrent with compromise of motor endurance and spatial memory

Neuroscience

Volumn 161, Issue 4, 2009, Pages 1104-1113

  Chen, J R ^a   Wang, T J ^b   Huang, H Y ^a   Chen, L J ^c   Huang, Y S ^a   Wang, Y J ^d   Tseng, G F ^d  

^a NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^b National Taichung Nursing College   (Taiwan)

^c NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^d TZU CHI UNIVERSITY   (Taiwan)

Author keywords

corticospinal; dendrite; fatigue; hippocampus; plasticity; PSD 95

Indexed keywords

DYE; WATER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN CORTEX; BRAIN FUNCTION; CONTROLLED STUDY; DENDRITIC SPINE; ENDURANCE; FATIGUE; HIPPOCAMPUS; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; LEARNING TEST; MALE; MOTOR PERFORMANCE; NERVE CELL; NONHUMAN; PERFORMANCE; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SLEEP DEPRIVATION; SPATIAL DISCRIMINATION; SPATIAL MEMORY; STRESS; SWIMMING;

ANIMALS; CEREBRAL CORTEX; DENDRITIC SPINES; FATIGUE; HIPPOCAMPUS; IMAGING, THREE-DIMENSIONAL; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LEARNING DISORDERS; MALE; MAZE LEARNING; MEMBRANE PROTEINS; MEMORY DISORDERS; NEURAL PATHWAYS; NEURONAL PLASTICITY; NEURONS; PHYSICAL ENDURANCE; PYRAMIDAL CELLS; RATS; SLEEP DEPRIVATION; SPINAL CORD; SWIMMING;

EID: 66049148766     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2009.04.022     Document Type: Article

References (63)

1. Afari N., and Buchwald D. Chronic fatigue syndrome: a review. Am J Psychiatry 160 (2003) 221-236
2. Alvarez V.A., Ridenour D.A., and Sabatini B.L. Distinct structural and ionotropic roles of NMDA receptors in controlling spine and synapse stability. J Neurosci 27 (2007) 7365-7376
3. Blissitt P.A. Sleep, memory, and learning. J Neurosci Nurs 33 (2001) 208-215
4. Brown C.E., Li P., Boyd J.D., Delaney K.R., and Murphy T.H. Extensive turnover of dendritic spines and vascular remodeling in cortical tissues recovering from stroke. J Neurosci 27 (2007) 4101-4109
5. Buchwald D., Garrity D., Pascualy R., Kith P., Ashley R.L., Wener M.H., Kidd P.G., Katon W.J., and Russo J.E. Chronic fatigue syndrome. Toxicol Ind Health 8 (1992) 157-173
6. Campbell I.G., Guinan M.J., and Horowitz J.M. Sleep deprivation impairs long-term potentiation in rat hippocampal slices. J Neurophysiol 88 (2001) 1073-1076
7. Chao C.C., DeLaHunt M., Hu S., Close K., and Peterson P.K. Immunologically mediated fatigue: a murine model. Clin Immunol Immunopathol 64 (1992) 161-165
8. Chen J.R., Wang Y.J., and Tseng G.F. The effect of epidural compression on cerebral cortex: a rat model. J Neurotrauma 20 (2003) 767-780
9. Chen J.R., Wang Y.J., and Tseng G.F. The effects of decompression and exogenous NGF on compressed cerebral cortex. J Neurotrauma 21 (2004) 1640-1651
10. Chen J.R., Yan Y.J., Wang T.J., Chen L.J., Wang Y.J., and Tseng G.F. Gonadal hormones modulate the dendritic spine densities of primary cortical pyramidal neurons in adult female rat. Cereb Cortex (2009) doi:10.1093/cercor/bhp048
11. Cooke B.M., and Woolley C.S. Gonadal hormone modulation of dendrites in the mammalian CNS. J Neurobiol 64 (2005) 34-46
12. Davis C.J., Harding J.W., and Wright J.W. REM sleep deprivation-induced deficits in the latency-to-peak induction and maintenance of long-term potentiation within the CA1 region of the hippocampus. Brain Res 973 (2003) 293-297
13. de Lange F.P., Kalkman J.S., Bleijenberg G., Hagoort P., van der Meer J.W., and Toni I. Gray matter volume reduction in the chronic fatigue syndrome. Neuroimage 26 (2005) 777-781
14. de Lange F.P., Kalkman J.S., Bleijenberg G., Hagoort P., van der Werf S.P., van der Meer J.W., and Toni I. Neural correlates of the chronic fatigue syndrome-an fMRI study. Brain 127 (2004) 1948-1957
15. Deller T., Bas Orth C., Vlachos A., Merten T., Del Turco D., Dehn D., Mundel P., and Frotscher M. Plasticity of synaptopodin and the spine apparatus organelle in the rat fascia dentata following entorhinal cortex lesion. J Comp Neurol 499 (2006) 471-484
16. Fukuda K., Straus S.E., Hickie I., Sharpe M.C., Dobbins J.G., and Komaroff A. The chronic fatigue syndrome: a comprehensive approach to its definition and study. International Chronic Fatigue Syndrome Study Group. Ann Intern Med 121 (1994) 953-959
17. Furuyashiki T., Fujisawa K., Fujita A., Madaule P., Uchino S., Mishina M., Bito H., and Narumiya S. Citron, a Rho-target, interacts with PSD-95/SAP-90 at glutamatergic synapses in the thalamus. J Neurosci 19 (1999) 109-118
18. Gibertini M., Newton C., Friedman H., and Klein T.W. Spatial learning impairment in mice infected with Legionella pneumophila or administered exogenous interleukin-1-beta. Brain Behav Immun 9 (1995) 113-128
19. Glaser R., and Kiecolt-Glaser J.K. Stress-associated immune modulation: relevance to viral infections and chronic fatigue syndrome. Am J Med 105 (1998) S35-S42
20. Gould E., Woolley C.S., Frankfurt M., and McEwen B.S. Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J Neurosci 10 (1990) 1286-1291
21. Guan Z., Peng X., and Fang J. Sleep deprivation impairs spatial memory and decreases extracellular signal-regulated kinase phosphorylation in the hippocampus. Brain Res 1018 (2004) 38-47
22. Halpain S., Hipolito A., and Saffer L. Regulation of F-actin stability in dendritic spines by glutamate receptors and calcineurin. J Neurosci 18 (1998) 9835-9844
23. Horner C.H. Plasticity of the dendritic spine. Prog Neurobiol 41 (1993) 281-321
24. Katafuchi T., Kondo T., Yasaka T., Kubo K., Take S., and Yoshimura M. Prolonged effects of polyriboinosinic: polyribocytidylic acid on spontaneous running wheel activity and brain interferon-alpha mRNA in rats: a model for immunologically induced fatigue. Neuroscience 120 (2003) 837-845
25. Kolb B., Cote S., Ribeiro-da-Silva A., and Cuello A.C. Nerve growth factor treatment prevents dendritic atrophy and promotes recovery of function after cortical injury. Neuroscience 76 (1997) 1139-1151
26. Lange G., DeLuca J., Maldjian J.A., Lee H., Tiersky L.A., and Natelson B.H. Brain MRI abnormalities exist in a subset of patients with chronic fatigue syndrome. J Neurol Sci 171 (1999) 3-7
27. Ling E.A., Ng Y.K., Wu C.H., and Kaur C. Microglia: its development and role as a neuropathology sensor. Prog Brain Res 132 (2001) 61-79
28. Liu P.H., Yang L.H., Wang Y.J., and Tseng G.F. Proximity of lesioning determines response of facial motoneurons to peripheral axotomy. J Neurotrauma 23 (2006) 1857-1873
29. MacHale S.M., Lawrie S.M., Cavanagh J.T., Glabus M.F., Murray C.L., Goodwin G.M., and Ebmeier K.P. Cerebral perfusion in chronic fatigue syndrome and depression. Br J Psychiatry 176 (2000) 550-556
30. 2+ homeostasis and cell death. J Neurosci 15 (1995) 6239-6249
31. McDermott C.M., La Hoste G.J., Chen C., Musto A., Bazan N.G., and Magee J.C. Sleep deprivation causes behavioral, synaptic, and membrane excitability alterations in hippocampal neurons. J Neurosci 23 (2003) 9687-9695
32. McDermott C.M., Hardy M.N., Bazan N.G., and Magee J.C. Sleep deprivation-induced alterations in excitatory synaptic transmission in the CA1 region of the rat hippocampus. J Physiol 570 (2006) 553-565
33. McEwen B.S., and Woolley C.S. Estradiol and progesterone regulate neuronal structure and synaptic connectivity in adult as well as developing brain. Exp Gerontol 29 (1994) 431-436
34. 18F]fluoro-2-deoxy-D-glucose utilization measured by autoradiography and in brain monoamine levels of rat. Neurosci Lett 353 (2003) 169-172
35. Mizuno K., Tanaka M., Nozaki S., Yamaguti K., Mizuma H., Sasabe T., Sugino T., Shirai T., Kataoka Y., Kajimoto Y., Kuratsune H., Kajimoto O., and Watanabe Y. Mental fatigue-induced decrease in levels of several plasma amino acids. J Neural Transm 114 (2007) 555-561
36. Mizunoya W., Oyaizu S., Hirayama A., and Fushiki T. Effects of physical fatigue in mice on learning performance in a water maze. Biosci Biotechnol Biochem 68 (2004) 827-834
37. Morris R. Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 11 (1984) 47-60
38. Moser M.B., Moser E.I., Forrest E., Andersen P., and Morris R.G. Spatial learning with a minislab in the dorsal hippocampus. Proc Natl Acad Sci U S A 92 (1995) 9697-9701
39. Nagerl U.V., Eberhorn N., Cambridge S.B., and Bonhoeffer T. Bidirectional activity-dependent morphological plasticity in hippocampal neurons. Neuron 44 (2004) 759-767
40. Natelson B.H., Cohen J.M., Brassloff I., and Lee H.J. A controlled study of brain magnetic resonance imaging in patients with the chronic fatigue syndrome. J Neurol Sci 120 (1993) 213-217
41. Neuner-Jehle M., Denizot J.P., Borbely A.A., and Mallet J. Characterization and sleep deprivation-induced expression modulation of dendrin, a novel dendritic protein in rat brain neurons. J Neurosci Res 46 (1996) 138-151
42. Okada T., Tanaka M., Kuratsune H., Watanabe Y., and Sadato N. Mechanisms underlying fatigue: a voxel-based morphometric study of chronic fatigue syndrome. BMC Neurol 4 (2004) 14
43. Romcy-Pereiro R., and Pavlides C. Distinct modulatory effects of sleep on the maintenance of hippocampal and medial prefrontal cortex LTP. Eur J Neurosci 20 (2004) 3453-3462
44. Ruskin D.N., Liu C., Dunn K.E., Bazan N.G., and La Hoste G.J. Sleep deprivation impairs hippocampus-mediated contextual learning but not amygdala-mediated cued learning in rats. Eur J Neurosci 19 (2004) 3121-3124
45. Sacco P., Hope P.A., Thickbroom G.W., Byrnes M.L., and Mastaglia F.L. Corticomotor excitability and perception of effort during sustained exercise in the chronic fatigue syndrome. Clin Neurophysiol 110 (1999) 1883-1891
46. Samii A., Wassermann E.M., Ikoma K., Mercuri B., and Hallett M. Characterization of postexercise facilitation and depression of motor evoked potentials to transcranial magnetic stimulation. Neurology 46 (1996) 1376-1382
47. Samii A., Wassermann E.M., Ikoma K., Mercuri B., George M.S., O'Fallon A., Dale J.K., Straus S.E., and Hallett M. Decreased postexercise facilitation of motor evoked potentials in patients with chronic fatigue syndrome or depression. Neurology 47 (1996) 1410-1414
48. Schmaling K.B., Lewis D.H., Fiedelak J.I., Mahurin R., and Buchwald D.S. Single-photon emission computerized tomography and neurocognitive function in patients with chronic fatigue syndrome. Psychosom Med 65 (2003) 129-136
49. Starr A., Scalise A., Gordon R., Michalewski H.J., and Caramia M.D. Motor cortex excitability in chronic fatigue syndrome. Clin Neurophysiol 111 (2000) 2025-2031
50. Tailby C., Wright L.L., Metha A.B., and Calford M.B. Activity-dependent maintenance and growth of dendrites in adult cortex. Proc Natl Acad Sci U S A 102 (2005) 4631-4636
51. Tanaka M., Nakamura F., Mizokawa S., Matsumura A., Nozaki S., and Watanabe Y. Establishment and assessment of a rat model of fatigue. Neurosci Lett 352 (2003) 159-162
52. Tobler I., Murison R., Ursin R., Ursin H., and Borbely A.A. The effect of sleep deprivation and recovery sleep on plasma corticosterone in the rat. Neurosci Lett 35 (1983) 297-300
53. Tseng G.F., and Hu M.E. Axotomy induces retraction of the dendritic arbor of adult rat rubrospinal neurons. Acta Anat (Basel) 155 (1996) 184-193
54. Tseng G.F., and Prince D.A. Structural and functional alterations in rat corticospinal neurons after axotomy. J Neurophysiol 75 (1996) 248-267
55. Wang Y.J., Chen J.R., and Tseng G.F. Fate of the soma and dendrites of cord-projection central neurons after proximal and distal spinal axotomy: an intracellular dye injection study. J Neurotrauma 19 (2002) 1487-1502
56. Wang T.J., Chen J.R., Wang Y.J., and Tseng G.F. The cytoarchitecture and soma-dendritic arbors of the pyramidal neurons of aged rat sensorimotor cortex: an intracellular dye injection study. Neuroscience 158 (2009) 776-785
57. Watanabe Y., Gould E., and McEwen B.S. Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Res 588 (1992) 341-345
58. Woolley C.S., and McEwen B.S. Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. J Neurosci 12 (1992) 2549-2554
59. Woolley C.S., and McEwen B.S. Estradiol regulates hippocampal dendritic spine density via an N-methyl-D-aspartate receptor-dependent mechanism. J Neurosci 14 (1994) 7680-7687
60. Woolley C.S., and Schwartzkroin P.A. Hormonal effects on the brain. Epilepsia 39 Suppl 8 (1998) S2-S8
61. Woolley C.S., Gould E., and McEwen B.S. Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons. Brain Res 531 (1990) 225-231
62. Woolley C.S., Weiland N.G., McEwen B.S., and Schwartzkroin P.A. Estradiol increases the sensitivity of hippocampal CA1 pyramidal cells to NMDA receptor-mediated synaptic input: correlation with dendritic spine density. J Neurosci 17 (1997) 1848-1859
63. Yang R.H., Hu S.J., Wang Y., Zhang W.B., Luo W.J., and Chen J.Y. Paradoxical sleep deprivation impairs spatial learning and affects membrane excitability and mitochondrial protein in the hippocampus. Brain Res 1230 (2008) 224-232