Regional gray matter volume increases following 7days of voluntary wheel running exercise: A longitudinal VBM study in rats

NeuroImage

Volumn 98, Issue , 2014, Pages 82-90

  Sumiyoshi, Akira ^a   Taki, Yasuyuki ^a   Nonaka, Hiroi ^a   Takeuchi, Hikaru ^a   Kawashima, Ryuta ^a  

^a TOHOKU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ANATOMICAL VARIATION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASSOCIATION CORTEX; BRAIN SIZE; BRAIN TISSUE; CEREBELLUM; CONTROLLED STUDY; HIPPOCAMPUS; IMAGE ANALYSIS; MALE; MOTOR CORTEX; NERVE CELL PLASTICITY; NEUROANATOMY; NEUROIMAGING; NON INVASIVE PROCEDURE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; RAT; REGIONAL GRAY MATTER VOLUME; SOMATOSENSORY CORTEX; TREADMILL EXERCISE; VISUAL CORTEX; VOXEL BASED MORPHOMETRY; ANATOMY AND HISTOLOGY; ANIMAL; BRAIN CORTEX; GRAY MATTER; LONGITUDINAL STUDY; MOTOR ACTIVITY; PHYSIOLOGY; WISTAR RAT;

ANIMALS; CEREBRAL CORTEX; GRAY MATTER; LONGITUDINAL STUDIES; MAGNETIC RESONANCE IMAGING; MALE; MOTOR ACTIVITY; RATS; RATS, WISTAR;

EID: 84904634320     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2014.04.075     Document Type: Article

References (92)

1. Abraham W.C. Metaplasticity: tuning synapses and networks for plasticity. Nat. Rev. Neurosci. 2008, 9:387-399.
2. Anderson B.J., Eckburg P.B., Relucio K.I. Alterations in the thickness of motor cortical subregions after motor-skill learning and exercise. Learn. Mem. 2002, 9:1-9.
3. Asami T., Bouix S., Whitford T.J., Shenton M.E., Salisbury D.F., McCarley R.W. Longitudinal loss of gray matter volume in patients with first-episode schizophrenia: DARTEL automated analysis and ROI validation. NeuroImage 2012, 59:986-996.
4. Ashburner J. A fast diffeomorphic image registration algorithm. NeuroImage 2007, 38:95-113.
5. Ashburner J., Friston K.J. Voxel-based morphometry-the methods. NeuroImage 2000, 11:805-821.
6. Ashburner J., Friston K.J. Unified segmentation. NeuroImage 2005, 26:839-851.
7. Attwell D., Buchan A.M., Charpak S., Lauritzen M., Macvicar B.A., Newman E.A. Glial and neuronal control of brain blood flow. Nature 2010, 468:232-243.
8. Bennett E.L., Diamond M.C., Krech D., Rosenzweig M.R. Chemical and anatomical plasticity of brain. Science 1964, 146:610-619.
9. Biedermann S., Fuss J., Zheng L., Sartorius A., Falfán-Melgoza C., Demirakca T., Gass P., Ende G., Weber-Fahr W. In vivo voxel based morphometry: detection of increased hippocampal volume and decreased glutamate levels in exercising mice. NeuroImage 2012, 61:1206-1212.
10. Brett-Green B., Fifková E., Larue D.T., Winer J.A., Barth D.S. A multisensory zone in rat parietotemporal cortex: intra- and extracellular physiology and thalamocortical connections. J. Comp. Neurol. 2003, 460:223-237.
11. Briones T.L., Klintsova A.Y., Greenough W.T. Stability of synaptic plasticity in the adult rat visual cortex induced by complex environment exposure. Brain Res. 2004, 1018:130-135.
12. Brown J., Cooper-Kuhn C.M., Kempermann G., Van Praag H., Winkler J., Gage F.H., Kuhn H.G. Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis. Eur. J. Neurosci. 2003, 17:2042-2046.
13. Calabrese E., Badea A., Watson C., Johnson G.A. A quantitative magnetic resonance histology atlas of postnatal rat brain development with regional estimates of growth and variability. NeuroImage 2013, 71:196-206.
14. Camel J.E., Withers G.S., Greenough W.T. Persistence of visual cortex dendritic alterations induced by postweaning exposure to a "superenriched" environment in rats. Behav. Neurosci. 1986, 100:810-813.
15. Chen Y.C., Lei J.L., Chen Q.S., Wang S.L. Effect of physical training on the age-related changes of acetylcholinesterase-positive fibers in the hippocampal formation and parietal cortex in the C57BL/6J mouse. Mech. Ageing Dev. 1998, 102:81-93.
16. DeFelipe J., Alonso-Nanclares L., Arellano J.I. Microstructure of the neocortex: comparative aspects. J. Neurocytol. 2002, 31:299-316.
17. Diamond M.C., Krech D., Rosenzweig M.R. The effects of an enriched environment on the histology of the rat cerebral cortex. J. Comp. Neurol. 1964, 123:111-120.
18. Diamond M.C., Johnson R.E., Ingham C.A. Morphological changes in the young, adult and aging rate cerebral cortex, hippocampus, and diencephalon. Behav. Biol. 1975, 14:163-174.
19. Ding Y.-H., Luan X.-D., Li J., Rafols J.A., Guthinkonda M., Diaz F.G., Ding Y. Exercise-induced overexpression of angiogenic factors and reduction of ischemia/reperfusion injury in stroke. Curr. Neurovasc. Res. 2004, 1:411-420.
20. Draganski B., Gaser C., Busch V., Schuierer G., Bogdahn U., May A. Neuroplasticity: changes in grey matter induced by training. Nature 2004, 427:311-312.
21. Draganski B., Gaser C., Kempermann G., Kuhn H.G., Winkler J., Büchel C., May A. Temporal and spatial dynamics of brain structure changes during extensive learning. J. Neurosci. 2006, 26:6314-6317.
22. Eadie B.D., Redila V.A., Christie B.R. Voluntary exercise alters the cytoarchitecture of the adult dentate gyrus by increasing cellular proliferation, dendritic complexity, and spine density. J. Comp. Neurol. 2005, 486:39-47.
23. Ehninger D., Kempermann G. Regional effects of wheel running and environmental enrichment on cell genesis and microglia proliferation in the adult murine neocortex. Cereb. Cortex 2003, 13:845-851.
24. Eikelboom R., Mills R. A microanalysis of wheel running in male and female rats. Physiol. Behav. 1988, 43:625-630.
25. Erickson K.I., Voss M.W., Prakash R.S., Basak C., Szabo A., Chaddock L., Kim J.S., Heo S., Alves H., White S.M. Exercise training increases size of hippocampus and improves memory. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:3017-3022.
26. Eriksson S.H., Free S.L., Thom M., Symms M.R., Martinian L., Duncan J.S., Sisodiya S.M. Quantitative grey matter histological measures do not correlate with grey matter probability values from in vivo MRI in the temporal lobe. J. Neurosci. Methods 2009, 181:111-118.
27. Eschenko O., Canals S., Simanova I., Beyerlein M., Murayama Y., Logothetis N.K. Mapping of functional brain activity in freely behaving rats during voluntary running using manganese-enhanced MRI: implication for longitudinal studies. NeuroImage 2010, 49:2544-2555.
28. Ferreira A.F.B., Real C.C., Rodrigues A.C., Alves A.S., Britto L.R.G. Moderate exercise changes synaptic and cytoskeletal proteins in motor regions of the rat brain. Brain Res. 2010, 1361:31-42.
29. Flöel A., Ruscheweyh R., Krüger K., Willemer C., Winter B., Völker K., Lohmann H., Zitzmann M., Mooren F., Breitenstein C., Knecht S. Physical activity and memory functions: are neurotrophins and cerebral gray matter volume the missing link?. NeuroImage 2010, 49:2756-2763.
30. Garcia P.C., Real C.C., Ferreira A.F.B., Alouche S.R., Britto L.R.G., Pires R.S. Different protocols of physical exercise produce different effects on synaptic and structural proteins in motor areas of the rat brain. Brain Res. 2012, 1456:36-48.
31. Gaser C., Schmidt S., Metzler M., Herrmann K.-H., Krumbein I., Reichenbach J.R., Witte O.W. Deformation-based brain morphometry in rats. NeuroImage 2012, 63:47-53.
32. Genovese C.R., Lazar N.A., Nichols T. Thresholding of statistical maps in functional neuroimaging using the false discovery rate. NeuroImage 2002, 15:870-878.
33. Goff M.L., Finger F.W. Activity rhythms and adiurnal light-dark control. Science 1966, 154:1346-1349.
34. Greenwood B.N., Foley T.E., Day H.E.W., Campisi J., Hammack S.H., Campeau S., Maier S.F., Fleshner M. Freewheel running prevents learned helplessness/behavioral depression: role of dorsal raphe serotonergic neurons. J. Neurosci. 2003, 23:2889-2898.
35. Holschneider D.P., Maarek J.-M.I., Yang J., Harimoto J., Scremin O.U. Functional brain mapping in freely moving rats during treadmill walking. J. Cereb. Blood Flow Metab. 2003, 23:925-932.
36. Hughes C.C., Lantos P.L. A morphometric study of blood vessel, neuron and glial cell distribution in young and old rat brain. J. Neurol. Sci. 1987, 79:101-110.
37. Iadecola C. Neurovascular regulation in the normal brain and in Alzheimer's disease. Nat. Rev. Neurosci. 2004, 5:347-360.
38. Johansen-Berg H. The future of functionally-related structural change assessment. NeuroImage 2012, 62:1293-1298.
39. Kale S.C., Lerch J.P., Henkelman R.M., Chen X.J. Optimization of the SNR-resolution tradeoff for registration of magnetic resonance images. Hum. Brain Mapp. 2008, 29:1147-1158.
40. Kempermann G., Fabel K., Ehninger D., Babu H., Leal-Galicia P., Garthe A., Wolf S.A. Why and how physical activity promotes experience-induced brain plasticity. Front. Neurosci. 2010, 4:189.
41. Klante G., Secci K., Masson-Pévet M., Pévet P., Vivien-Roels B., Steinlechner S., Wollnik F. Interstrain differences in activity pattern, pineal function, and SCN melatonin receptor density of rats. Am. J. Physiol. 1999, 276:R1078-R1086.
42. Kleim J.A., Cooper N.R., VandenBerg P.M. Exercise induces angiogenesis but does not alter movement representations within rat motor cortex. Brain Res. 2002, 934:1-6.
43. Kobilo T., Liu Q.-R., Gandhi K., Mughal M., Shaham Y., Van Praag H. Running is the neurogenic and neurotrophic stimulus in environmental enrichment. Learn. Mem. 2011, 18:605-609.
44. Kocharyan A., Fernandes P., Tong X.-K., Vaucher E., Hamel E. Specific subtypes of cortical GABA interneurons contribute to the neurovascular coupling response to basal forebrain stimulation. J. Cereb. Blood Flow Metab. 2008, 28:221-231.
45. Lerch J.P., Yiu A.P., Martinez-Canabal A., Pekar T., Bohbot V.D., Frankland P.W., Henkelman R.M., Josselyn S.A., Sled J.G. Maze training in mice induces MRI-detectable brain shape changes specific to the type of learning. NeuroImage 2011, 54:2086-2095.
46. Li J., Ding Y.-H., Rafols J.A., Lai Q., McAllister J.P., Ding Y. Increased astrocyte proliferation in rats after running exercise. Neurosci. Lett. 2005, 386:160-164.
47. Lockwood-Estrin G., Thom M., Focke N.K., Symms M.R., Martinian L., Sisodiya S.M., Duncan J.S., Eriksson S.H. Correlating 3T MRI and histopathology in patients undergoing epilepsy surgery. J. Neurosci. Methods 2012, 205:182-189.
48. Lu H., Scholl C.A., Zuo Y., Demny S., Rea W., Stein E.A., Yang Y. Registering and analyzing rat fMRI data in the stereotaxic framework by exploiting intrinsic anatomical features. Magn. Reson. Imaging 2010, 28:146-152.
49. Markham J.A., Greenough W.T. Experience-driven brain plasticity: beyond the synapse. Neuron Glia Biol. 2004, 1:351-363.
50. May A. Experience-dependent structural plasticity in the adult human brain. Trends Cogn. Sci. 2011, 15:475-482.
51. McAllister A.K., Katz L.C., Lo D.C. Neurotrophins and synaptic plasticity. Annu. Rev. Neurosci. 1999, 22:295-318.
52. Neeper S.A., Gómez-Pinilla F., Choi J., Cotman C.W. Exercise and brain neurotrophins. Nature 1995, 373:109.
53. Neeper S.A., Gómez-Pinilla F., Choi J., Cotman C.W. Physical activity increases mRNA for brain-derived neurotrophic factor and nerve growth factor in rat brain. Brain Res. 1996, 726:49-56.
54. Nie B., Chen K., Zhao S., Liu J., Gu X., Yao Q., Hui J., Zhang Z., Teng G., Zhao C., Shan B. A rat brain MRI template with digital stereotaxic atlas of fine anatomical delineations in paxinos space and its automated application in voxel-wise analysis. Hum. Brain Mapp. 2013, 34:1306-1318.
55. Nithianantharajah J., Hannan A.J. Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nat. Rev. Neurosci. 2006, 7:697-709.
56. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 2007, Academic Press, San Diego. Sixth edition.
57. Pereira A.C., Huddleston D.E., Brickman A.M., Sosunov A.A., Hen R., McKhann G.M., Sloan R., Gage F.H., Brown T.R., Small S.A. An in vivo correlate of exercise-induced neurogenesis in the adult dentate gyrus. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:5638-5643.
58. Pietropaolo S., Sun Y., Li R., Brana C., Feldon J., Yee B.K. The impact of voluntary exercise on mental health in rodents: a neuroplasticity perspective. Behav. Brain Res. 2008, 192:42-60.
59. Pinto-Hamuy T., Olavarria J., Guic-Robles E., Morgues M., Nassal O., Petit D. Rats with lesions in anteromedial extrastriate cortex fail to learn a visuosomatic conditional response. Behav. Brain Res. 1987, 25:221-231.
60. Quallo M.M., Price C.J., Ueno K., Asamizuya T., Cheng K., Lemon R.N., Iriki A. Gray and white matter changes associated with tool-use learning in macaque monkeys. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:18379-18384.
61. Real C.C., Ferreira A.F.B., Hernandes M.S., Britto L.R.G., Pires R.S. Exercise-induced plasticity of AMPA-type glutamate receptor subunits in the rat brain. Brain Res. 2010, 1363:63-71.
62. Redila V.A., Christie B.R. Exercise-induced changes in dendritic structure and complexity in the adult hippocampal dentate gyrus. Neuroscience 2006, 137:1299-1307.
63. Renner M.J., Rosenzweig M.R. Enriched and Impoverished Environments: Effects on Brain and Behaviour 1987, Springer, New York.
64. Rhodes J.S., van Praag H., Jeffrey S., Girard I., Mitchell G.S., Garland T., Gage F.H. Exercise increases hippocampal neurogenesis to high levels but does not improve spatial learning in mice bred for increased voluntary wheel running. Behav. Neurosci. 2003, 117:1006-1016.
65. Rhyu I.J., Bytheway J.A., Kohler S.J., Lange H., Lee K.J., Boklewski J., McCormick K., Williams N.I., Stanton G.B., Greenough W.T., Cameron J.L. Effects of aerobic exercise training on cognitive function and cortical vascularity in monkeys. Neuroscience 2010, 167:1239-1248.
66. Rosenzweig M.R., Krech D., Bennett E.L., Diamond M.C. Effects of environmental complexity and training on brain chemistry and anatomy: a replication and extension. J. Comp. Physiol. Psychol. 1962, 55:429-437.
67. Scholz J., Klein M.C., Behrens T.E.J., Johansen-Berg H. Training induces changes in white-matter architecture. Nat. Neurosci. 2009, 12:1370-1371.
68. Schwarz A.J., Danckaert A., Reese T., Gozzi A., Paxinos G., Watson C., Merlo-Pich E.V., Bifone A. A stereotaxic MRI template set for the rat brain with tissue class distribution maps and co-registered anatomical atlas: application to pharmacological MRI. NeuroImage 2006, 32:538-550.
69. Schweinhardt P., Fransson P., Olson L., Spenger C., Andersson J.L.R. A template for spatial normalisation of MR images of the rat brain. J. Neurosci. Methods 2003, 129:105-113.
70. Steiner B., Kronenberg G., Jessberger S., Brandt M.D., Reuter K., Kempermann G. Differential regulation of gliogenesis in the context of adult hippocampal neurogenesis in mice. Glia 2004, 46:41-52.
71. Stranahan A.M., Khalil D., Gould E. Social isolation delays the positive effects of running on adult neurogenesis. Nat. Neurosci. 2006, 9:526-533.
72. Suzuki H., Sumiyoshi A., Taki Y., Matsumoto Y., Fukumoto Y., Kawashima R., Shimokawa H. Voxel-based morphometry and histological analysis for evaluating hippocampal damage in a rat model of cardiopulmonary resuscitation. NeuroImage 2013, 77:215-221.
73. Swain R.A., Harris A.B., Wiener E.C., Dutka M.V., Morris H.D., Theien B.E., Konda S., Engberg K., Lauterbur P.C., Greenough W.T. Prolonged exercise induces angiogenesis and increases cerebral blood volume in primary motor cortex of the rat. Neuroscience 2003, 117:1037-1046.
74. Takeuchi H., Sekiguchi A., Taki Y., Yokoyama S., Yomogida Y., Komuro N., Yamanouchi T., Suzuki S., Kawashima R. Training of working memory impacts structural connectivity. J. Neurosci. 2010, 30:3297-3303.
75. Takeuchi H., Taki Y., Hashizume H., Sassa Y., Nagase T., Nouchi R., Kawashima R. Effects of training of processing speed on neural systems. J. Neurosci. 2011, 31:12139-12148.
76. Tees R.C. The effects of posterior parietal and posterior temporal cortical lesions on multimodal spatial and nonspatial competencies in rats. Behav. Brain Res. 1999, 106:55-73.
77. Thomas C., Baker C.I. Teaching an adult brain new tricks: a critical review of evidence for training-dependent structural plasticity in humans. NeuroImage 2013, 73:225-236.
78. Thomas A.G., Dennis A., Bandettini P.A., Johansen-Berg H. The effects of aerobic activity on brain structure. Front. Psychol. 2012, 3:86.
79. Toldi J., Fehér O., Wolff J.R. Sensory interactive zones in the rat cerebral cortex. Neuroscience 1986, 18:461-465.
80. Tung A., Herrera S., Fornal C.A., Jacobs B.L. The effect of prolonged anesthesia with isoflurane, propofol, dexmedetomidine, or ketamine on neural cell proliferation in the adult rat. Anesth. Analg. 2008, 106:1772-1777.
81. Uda M., Ishido M., Kami K., Masuhara M. Effects of chronic treadmill running on neurogenesis in the dentate gyrus of the hippocampus of adult rat. Brain Res. 2006, 1104:64-72.
82. Valdés-Hernández P.A., Sumiyoshi A., Nonaka H., Haga R., Aubert-Vásquez E., Ogawa T., Iturria-Medina Y., Riera J.J., Kawashima R. An in vivo MRI template set for morphometry, tissue segmentation, and fMRI localization in rats. Front. Neuroinform. 2011, 5:26.
83. 1 relaxation in in vivo mouse brain at ultra-high field. Magn. Reson. Med. 2007, 58:390-395.
84. Van der Borght K., Kóbor-Nyakas D.E., Klauke K., Eggen B.J.L., Nyakas C., Van der Zee E.A., Meerlo P. Physical exercise leads to rapid adaptations in hippocampal vasculature: temporal dynamics and relationship to cell proliferation and neurogenesis. Hippocampus 2009, 19:928-936.
85. van Praag H. Neurogenesis and exercise: past and future directions. Neuromol. Med. 2008, 10:128-140.
86. van Praag H., Kempermann G., Gage F.H. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat. Neurosci. 1999, 2:266-270.
87. Vissing J., Andersen M., Diemer N.H. Exercise-induced changes in local cerebral glucose utilization in the rat. J. Cereb. Blood Flow Metab. 1996, 16:729-736.
88. Voss M.W., Vivar C., Kramer A.F., van Praag H. Bridging animal and human models of exercise-induced brain plasticity. Trends Cogn. Sci. 2013, 17:525-544.
89. Wallace M.T., Ramachandran R., Stein B.E. A revised view of sensory cortical parcellation. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:2167-2172.
90. Wegener S., Wong E.C. Longitudinal MRI studies in the isoflurane-anesthetized rat: long-term effects of a short hypoxic episode on regulation of cerebral blood flow as assessed by pulsed arterial spin labelling. NMR Biomed. 2008, 21:696-703.
91. Winters B.D., Reid J.M. A distributed cortical representation underlies crossmodal object recognition in rats. J. Neurosci. 2010, 30:6253-6261.
92. Zhu C., Gao J., Karlsson N., Li Q., Zhang Y., Huang Z., Li H., Kuhn H.G., Blomgren K. Isoflurane anesthesia induced persistent, progressive memory impairment, caused a loss of neural stem cells, and reduced neurogenesis in young, but not adult, rodents. J. Cereb. Blood Flow Metab. 2010, 30:1017-1030.