Rotarod training in mice is associated with changes in brain structure observable with multimodal MRI

NeuroImage

Volumn 107, Issue , 2015, Pages 182-189

  Scholz, Jan ^a   Niibori, Yosuke ^a   W Frankland, Paul ^a,b,c   P Lerch, Jason ^a,b  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ARTICLE; CEREBELLUM; CONTROLLED STUDY; CORPUS CALLOSUM; DEFORMATION BASED MORPHOMETRY; DIFFUSION WEIGHTED IMAGING; FEMALE; FRACTIONAL ANISOTROPY; HIPPOCAMPUS; MALE; MORPHOMETRICS; MOTOR COORDINATION; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIMARY MOTOR CORTEX; ROTAROD TEST; STRIATE CORTEX; WHITE MATTER; ANATOMY AND HISTOLOGY; ANIMAL; ANISOTROPY; BODY EQUILIBRIUM; BRAIN; C57BL MOUSE; HEMISPHERIC DOMINANCE; IMAGE PROCESSING; LEARNING; NERVE TRACT; PHYSIOLOGY; PSYCHOMOTOR PERFORMANCE;

ANIMALS; ANISOTROPY; BRAIN; DIFFUSION MAGNETIC RESONANCE IMAGING; FEMALE; FUNCTIONAL LATERALITY; IMAGE PROCESSING, COMPUTER-ASSISTED; LEARNING; MALE; MICE; MICE, INBRED C57BL; NEURAL PATHWAYS; POSTURAL BALANCE; PSYCHOMOTOR PERFORMANCE;

EID: 84949114764     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2014.12.003     Document Type: Article

References (60)

1. Avants B.B., Tustison N.J., Wu J., Cook P.A., Gee J.C. An open source multivariate framework for n-tissue segmentation with evaluation on public data. Neuroinformatics 2011, 9:381-400.
2. Beaulieu C. The basis of anisotropic water diffusion in the nervous system - a technical review. NMR Biomed. 2002, 15:435-455.
3. Beraneck M., Cullen K.E. Activity of vestibular nuclei neurons during vestibular and optokinetic stimulation in the alert mouse. J. Neurophysiol. 2007, 98:1549-1565.
4. Bezzola L., Mérillat S., Gaser C., Jäncke L. Training-induced neural plasticity in golf novices. J. Neurosci. 2011, 31:12444-12448.
5. Blumenfeld-Katzir T., Pasternak O., Dagan M., Assaf Y. Diffusion MRI of structural brain plasticity induced by a learning and memory task. PLoS ONE 2011, 6:e20678.
6. Boyden E.S., Katoh A., Raymond J.L. Cerebellum-dependent learning: the role of multiple plasticity mechanisms. Annu. Rev. Neurosci. 2004, 27:581-609.
7. Brooks S.P., Dunnett S.B. Tests to assess motor phenotype in mice: a user's guide. Nat. Rev. Neurosci. 2009, 10:519-529.
8. Buitrago M.M., Schulz J.B., Dichgans J., Luft A.R. Short and long-term motor skill learning in an accelerated rotarod training paradigm. Neurobiol. Learn. Mem. 2004, 81:211-216.
9. Bureau G., Carrier M., Lebel M., Cyr M. Intrastriatal inhibition of extracellular signal-regulated kinases impaired the consolidation phase of motor skill learning. Neurobiol. Learn. Mem. 2010, 94:107-115.
10. Cahill L.S., Laliberté C.L., Ellegood J., Spring S., Gleave J.A., Eede M.C.V., Lerch J.P., Henkelman R.M. Preparation of fixed mouse brains for MRI. NeuroImage 2012, 60:933-939.
11. Cendelín J., Korelusová I., Vozeh F. The effect of repeated rotarod training on motor skills and spatial learning ability in Lurcher mutant mice. Behav. Brain Res. 2008, 189:65-74.
12. Christianson J.P., Benison A.M., Jennings J., Sandsmark E.K., Amat J., Kaufman R.D., Baratta M.V., Paul E.D., Campeau S., Watkins L.R., Barth D.S., Maier S.F. The sensory insular cortex mediates the stress-buffering effects of safety signals but not behavioral control. J. Neurosci. 2008, 28:13703-13711.
13. Craig A.D. How do you feel? Interoception: the sense of the physiological condition of the body. Nat. Rev. Neurosci. 2002, 3:655-666.
14. Demerens C., Stankoff B., Logak M., Anglade P., Allinquant B., Couraud F., Zalc B., Lubetzki C. Induction of myelination in the central nervous system by electrical activity. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:9887-9892.
15. Ding A.Y., Li Q., Zhou I.Y., Ma S.J., Tong G., McAlonan G.M., Wu E.X. MR diffusion tensor imaging detects rapid microstructural changes in amygdala and hippocampus following fear conditioning in mice. PLoS ONE 2013, 8:e51704.
16. Dorr A.E., Lerch J.P., Spring S., Kabani N., Henkelman R.M. High resolution three-dimensional brain atlas using an average magnetic resonance image of 40 adult C57Bl/6J mice. NeuroImage 2008, 42:60-69.
17. 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.
18. Drapeau E., Mayo W., Aurousseau C., Moal M.L., Piazza P.-V., Abrous D.N. Spatial memory performances of aged rats in the water maze predict levels of hippocampal neurogenesis. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:14385-14390.
19. Fanselow M.S., Dong H.-W. Are the dorsal and ventral hippocampus functionally distinct structures?. Neuron 2010, 65:7-19.
20. Gelman A. Data analysis Using Regression and Multilevel/Hierarchical Models 2007, Cambridge University Press, Cambridge New York.
21. 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.
22. Ghashghaei H.T., Lai C., Anton E.S. Neuronal migration in the adult brain: are we there yet?. Nat. Rev. Neurosci. 2007, 8:141-151.
23. Gittis A.H., du Lac S. Intrinsic and synaptic plasticity in the vestibular system. Curr. Opin. Neurobiol. 2006, 16:385-390.
24. Gould T.J., Rowe W.B., Heman K.L., Mesches M.H., Young D.A., Rose G.M., Bickford P.C. Effects of hippocampal lesions on patterned motor learning in the rat. Brain Res. Bull. 2002, 58:581-586.
25. Gross C.G. Neurogenesis in the adult brain: death of a dogma. Nat. Rev. Neurosci. 2000, 1:67-73.
26. Hammar I., Krutki P., Drzymala-Celichowska H., Nilsson E., Jankowska E. A trans-spinal loop between neurones in the reticular formation and in the cerebellum. J. Physiol. 2011, 589:653-665.
27. Heinrichs S.C., Leite-Morris K.A., Guy M.D., Goldberg L.R., Young A.J., Kaplan G.B. Dendritic structural plasticity in the basolateral amygdala after fear conditioning and its extinction in mice. Behav. Brain Res. 2013, 248:80-84.
28. Hickmott P.W., Steen P.A. Large-scale changes in dendritic structure during reorganization of adult somatosensory cortex. Nat. Neurosci. 2005, 8:140-142.
29. Jäncke L., Koeneke S., Hoppe A., Rominger C., Hänggi J. The architecture of the golfer's brain. PLoS ONE 2009, 4:e4785.
30. Jenkinson M., Beckmann C.F., Behrens T.E.J., Woolrich M.W., Smith S.M. FSL. NeuroImage 2012, 62:782-790.
31. Kempermann G., Kuhn H.G., Gage F.H. More hippocampal neurons in adult mice living in an enriched environment. Nature 1997, 386:493-495.
32. Kempermann G., Kuhn H.G., Gage F.H. Experience-induced neurogenesis in the senescent dentate gyrus. J. Neurosci. 1998, 18:3206-3212.
33. Kovacević N., Henderson J.T., Chan E., Lifshitz N., Bishop J., Evans A.C., Henkelman R.M., Chen X.J. A three-dimensional MRI atlas of the mouse brain with estimates of the average and variability. Cereb. Cortex 2005, 15:639-645.
34. Lerch J.P., Carroll J.B., Spring S., Bertram L.N., Schwab C., Hayden M.R., Henkelman R.M. Automated deformation analysis in the YAC128 Huntington disease mouse model. NeuroImage 2008, 39:32-39.
35. Lerch J.P., Sled J.G., Henkelman R.M. MRI phenotyping of genetically altered mice. Magnetic Resonance Neuroimaging SE - 17 2011, 349-361. Humana Press. M. Modo, J.W.M. Bulte (Eds.).
36. 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.
37. Loseva E., Yuan T.-F., Karnup S. Neurogliogenesis in the mature olfactory system: a possible protective role against infection and toxic dust. Brain Res. Rev. 2009, 59:374-387.
38. Ma D.K., Kim W.R., Ming G.-l., Song H. Activity-dependent extrinsic regulation of adult olfactory bulb and hippocampal neurogenesis. Ann. N. Y. Acad. Sci. 2009, 1170:664-673.
39. Madroñal N., López-Aracil C., Rangel A., del Río J.A., Delgado-García J.M., Gruart A. Effects of enriched physical and social environments on motor performance, associative learning, and hippocampal neurogenesis in mice. PLoS ONE 2010, 5:e11130.
40. Moraga-Amaro R., Stehberg J. The insular cortex and the amygdala: shared functions and interactions. The Amygdala - A Discrete Multitasking Manager 2012, InTech. B. Ferry (Ed.).
41. Nagao S., Kitazawa H. Effects of reversible shutdown of the monkey flocculus on the retention of adaptation of the horizontal vestibulo-ocular reflex. Neuroscience 2003, 118:563-570.
42. Nakagawa H., Ueno M., Itokazu T., Yamashita T. Bilateral movement training promotes axonal remodeling of the corticospinal tract and recovery of motor function following traumatic brain injury in mice. Cell Death Dis. 2013, 4:e534.
43. Sampaio-Baptista C., Khrapitchev A.A., Foxley S., Schlagheck T., Scholz J., Jbabdi S., DeLuca G.C., Miller K.L., Taylor A., Thomas N., Kleim J., Sibson N.R., Bannerman D., Johansen-Berg H. Motor skill learning induces changes in white matter microstructure and myelination. J. Neurosci. 2013, 33:19499-19503.
44. Schacher S., Castellucci V.F., Kandel E.R. cAMP evokes long-term facilitation in Aplysia sensory neurons that requires new protein synthesis. Science 1988, 240:1667-1669.
45. Scholz J., Klein M.C., Behrens T.E.J., Johansen-Berg H. Training induces changes in white-matter architecture. (Supplement). Nat. Neurosci. 2009, 12:1370-1371.
46. Sekirnjak C., du Lac S. Physiological and anatomical properties of mouse medial vestibular nucleus neurons projecting to the oculomotor nucleus. J. Neurophysiol. 2006, 95:3012-3023.
47. Shepherd T.M., Thelwall P.E., Stanisz G.J., Blackband S.J. Aldehyde fixative solutions alter the water relaxation and diffusion properties of nervous tissue. Magn. Reson. Med. 2009, 62:26-34.
48. Shibata H. Direct projections from the anterior thalamic nuclei to the retrohippocampal region in the rat. J. Comp. Neurol. 1993, 337:431-445.
49. Shiotsuki H., Yoshimi K., Shimo Y., Funayama M., Takamatsu Y., Ikeda K., Takahashi R., Kitazawa S., Hattori N. A rotarod test for evaluation of motor skill learning. J. Neurosci. Methods 2010, 189:180-185.
50. Shrestha S.S., Bannatyne B.A., Jankowska E., Hammar I., Nilsson E., Maxwell D.J. Excitatory inputs to four types of spinocerebellar tract neurons in the cat and the rat thoraco-lumbar spinal cord. J. Physiol. 2012, 590:1737-1755.
51. Shutoh F., Ohki M., Kitazawa H., Itohara S., Nagao S. Memory trace of motor learning shifts transsynaptically from cerebellar cortex to nuclei for consolidation. Neuroscience 2006, 139:767-777.
52. Steadman P.E., Ellegood J., Szulc K.U., Turnbull D.H., Joyner A.L., Henkelman R.M., Lerch J.P. Genetic effects on cerebellar structure across mouse models of autism using a magnetic resonance imaging atlas. Autism Res. 2013, 1-14.
53. Taubert M., Draganski B., Anwander A., Müller K., Horstmann A., Villringer A., Ragert P. Dynamic properties of human brain structure: learning-related changes in cortical areas and associated fiber connections. J. Neurosci. 2010, 30:11670-11677.
54. Ullmann J.F.P., Watson C., Janke A.L., Kurniawan N.D., Reutens D.C. A segmentation protocol and MRI atlas of the C57BL/6J mouse neocortex. NeuroImage 2013, 78C:196-203.
55. 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.
56. van Eede M.C., Scholz J., Chakravarty M.M., Henkelman R.M., Lerch J.P. Mapping registration sensitivity in MR mouse brain images. NeuroImage 2013, 82:226-236.
57. Van Groen T., Wyss J.M. Projections from the anterodorsal and anteroventral nucleus of the thalamus to the limbic cortex in the rat. J. Comp. Neurol. 1995, 358:584-604.
58. van Praag H., Christie B.R., Sejnowski T.J., Gage F.H. Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:13427-13431.
59. van Praag H., Shubert T., Zhao C., Gage F.H. Exercise enhances learning and hippocampal neurogenesis in aged mice. J. Neurosci. 2005, 25:8680-8685.
60. Yang G., Pan F., Gan W.-B. Stably maintained dendritic spines are associated with lifelong memories. Nature 2009, 462:920-924.