Maze training in mice induces MRI-detectable brain shape changes specific to the type of learning

NeuroImage

Volumn 54, Issue 3, 2011, Pages 2086-2095

  Lerch, Jason P ^a,b   Yiu, Adelaide P ^a,b,c   Martinez Canabal, Alonso ^a,b,c   Pekar, Tetyana ^a,b,c   Bohbot, Veronique D ^d   Frankland, Paul W ^a,b,c   Henkelman, R Mark ^a,b   Josselyn, Sheena A ^a,b,c   Sled, John G ^a,b  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTHROPOMETRIC PARAMETERS; ARTICLE; ASTROCYTE; BRAIN NERVE CELL; BRAIN REGION; BRAIN SHAPE; CELL COUNT; CELL SIZE; CONTROLLED STUDY; CORPUS STRIATUM; HIPPOCAMPUS; IMAGE ANALYSIS; LEARNING; MALE; MAZE TEST; MORPHOLOGY; MOUSE; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL;

ANIMALS; BIOLOGICAL MARKERS; BRAIN; CELL COUNT; CORPUS STRIATUM; CUES; GAP-43 PROTEIN; HIPPOCAMPUS; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; MAGNETIC RESONANCE IMAGING; MALE; MAZE LEARNING; MICE; MICE, INBRED C57BL; NEURONAL PLASTICITY;

EID: 78650283593     PISSN: 10538119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2010.09.086     Document Type: Article

References (83)

1. Alvarez V.A., Sabatini B.L. Anatomical and physiological plasticity of dendritic spines. Annu. Rev. Neurosci. 2007, 30:79-97.
2. Avants B.B., Epstein C.L., Grossman M., Gee J.C. Symmetric diffeomorphic image registration with cross-correlation: evaluating automated labeling of elderly and neurodegenerative brain. Med. Image Anal. 2008, 12:26-41.
3. Barnes C.A., Nadel L., Honig W.K. Spatial memory deficit in senescent rats. Can. J. Psychol. 1980, 34:29-39.
4. Benowitz L.I., Routtenberg A. GAP-43: an intrinsic determinant of neuronal development and plasticity. Trends Neurosci. 1997, 20:84-91.
5. Bermudez P., Lerch J.P., Evans A.C., Zatorre R.J. Neuroanatomical correlates of musicianship as revealed by cortical thickness and voxel-based morphometry. Cereb. Cortex 2009, 19:1583-1596.
6. Bock N., Nieman B., Bishop J., Mark Henkelman R. In vivo multiple-mouse MRI at 7Tesla. Magn. Reson. Med. 2005, 54:1311-1316.
7. Bohbot V., Lerch J., Thorndycraft B., Iaria G., Zijdenbos A. Gray matter differences correlate with spontaneous strategies in a human virtual navigation task. J. Neurosci. 2007, 27:10078-10083.
8. Bourne J.N., Harris K.M. Balancing structure and function at hippocampal dendritic spines. Annu. Rev. Neurosci. 2008, 31:47-67.
9. Boyke J., Driemeyer J., Gaser C., Büchel C., May A. Training-induced brain structure changes in the elderly. J. Neurosci. 2008, 28:7031-7035.
10. Brown J., Cooper-Kuhn C., Kempermann G., Van Praag H., Winkler J., Gage F., Kuhn H. Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis. Eur. J. Neurosci. 2003, 17:2042-2046.
11. Chen X., Kovacevic N., Lobaugh N., Sled J., Henkelman R., Henderson J. Neuroanatomical differences between mouse strains as shown by high-resolution 3D MRI. Neuroimage 2005, 7.
12. Chklovskii D.B., Mel B.W., Svoboda K. Cortical rewiring and information storage. Nature 2004, 431:782-788.
13. Christie B., Cameron H. Neurogenesis in the adult hippocampus. Hippocampus 2006, 16:199-207.
14. Chung M.K., Worsley K.J., Paus T., Cherif C., Collins D.L., Giedd J.N., Rapoport J.L., Evans A.C. A unified statistical approach to deformation-based morphometry. Neuroimage 2001, 14:595-606.
15. Clapcote S., Lipina T., Millar J., Mackie S., Christie S., Ogawa F., Lerch J., Trimble K., Uchiyama M., Sakuraba Y. Behavioral phenotypes of Disc1 missense mutations in mice. Neuron 2007, 54:387-402.
16. Collins D.L., Neelin P., Peters T.M., Evans A.C. Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space. J. Comput. Assist. Tomogr. 1994, 18:192-205.
17. Collins D., Holmes C., Peters T.M., Evans A. Automatic 3-D model-based neuroanatomical segmentation. Hum. Brain Mapp. 1995, 3:190-208.
18. Colombo P.J., Brightwell J.J., Countryman R.A. Cognitive strategy-specific increases in phosphorylated cAMP response element-binding protein and c-Fos in the hippocampus and dorsal striatum. J. Neurosci. 2003, 23:3547-3554.
19. De Paola V., Holtmaat A., Knott G., Song S., Wilbrecht L., Caroni P., Svoboda K. Cell type-specific structural plasticity of axonal branches and boutons in the adult neocortex. Neuron 2006, 49:861-875.
20. Devan B.D., Goad E.H., Petri H.L. Dissociation of hippocampal and striatal contributions to spatial navigation in the water maze. Neurobiol. Learn. Mem. 1996, 66:305-323.
21. Dickerson B.C., Fenstermacher E., Salat D.H., Wolk D.A., Maguire R.P., Desikan R., Pacheco J., Quinn B.T., van der Kouwe A., Greve D.N., Blacker D., Albert M.S., Killiany R.J., Fischl B. Detection of cortical thickness correlates of cognitive performance: reliability across MRI scan sessions, scanners, and field strengths. Neuroimage 2008, 39:10-18.
22. Doeller C., King J., Burgess N. Parallel striatal and hippocampal systems for landmarks and boundaries in spatial memory. Proc. Natl Acad. Sci. 2008, 105:5915-5920.
23. Dorr A., Lerch J., Spring S., Kabani N., Henkelman R. High resolution three-dimensional brain atlas using an average magnetic resonance image of 40 adult C57Bl/6J mice. Neuroimage 2008, 42:60-69.
24. 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.
25. Driemeyer J., Boyke J., Gaser C., Büchel C., May A. Changes in gray matter induced by learning-revisited. PLoS ONE 2008, 3:e2669.
26. Eichenbaum H., Otto T., Cohen N.J. The hippocampus-what does it do?. Behav. Neural Biol. 1992, 57:2-36.
27. Ellegood J., Pacey L.K., Hampson D.R., Lerch J., Henkelman R.M. Anatomical phenotyping in a mouse model of fragile X syndrome with magnetic resonance imaging. Neuroimage 2010, 53:1023-1029.
28. Engert F., Bonhoeffer T. Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 1999, 399:66-70.
29. Gaser C., Schlaug G. Brain structures differ between musicians and non-musicians. J. Neurosci. 2003, 23:9240-9245.
30. 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.
31. Gold P. Acetylcholine modulation of neural systems involved in learning and memory. Neurobiol. Learn. Mem. 2003, 80:194-210.
32. Gusev P.A., Cui C., Alkon D.L., Gubin A.N. Topography of Arc/Arg3.1 mRNA expression in the dorsal and ventral hippocampus induced by recent and remote spatial memory recall: dissociation of CA3 and CA1 activation. J. Neurosci. 2005, 25:9384-9397.
33. Haber M., Zhou L., Murai K. Cooperative astrocyte and dendritic spine dynamics at hippocampal excitatory synapses. J. Neurosci. 2006, 26:8881-8891.
34. Hartley T., Maguire E., Spiers H., Burgess N. The well-worn route and the path less traveled: distinct neural bases of route following and wayfinding in humans. Neuron 2003, 37:877-888.
35. Holahan M., Honegger K., Tabatadze N., Routtenberg A. GAP-43 gene expression regulates information storage. Learn. Mem. 2007, 14:407-415.
36. Holtmaat A., Trachtenberg J., Wilbrecht L., Shepherd G., Zhang X., Knott G., Svoboda K. Transient and persistent dendritic spines in the neocortex in vivo. Neuron 2005, 45:279-291.
37. Hyde K.L., Lerch J., Norton A., Forgeard M., Winner E., Evans A., Schlaug G. Musical training shapes structural brain development. J. Neurosci. 2009, 29:3019-3025.
38. Iaria G., Petrides M., Dagher A., Pike B., Bohbot V.D. Cognitive strategies dependent on the hippocampus and caudate nucleus in human navigation: variability and change with practice. J. Neurosci. 2003, 23:5945-5952.
39. Kee N., Teixeira C.M., Wang A.H., Frankland P.W. Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus. Nat. Neurosci. 2007, 10:355-362.
40. Kempermann G., Kuhn H.G., Gage F.H. More hippocampal neurons in adult mice living in an enriched environment. Nature 1997, 386:493-495.
41. Klein A., Andersson J., Ardekani B.A., Ashburner J., Avants B., Chiang M.C., Christensen G.E., Collins D.L., Gee J., Hellier P., Song J.H., Jenkinson M., Lepage C., Rueckert D., Thompson P., Vercauteren T., Woods R.P., Mann J.J., Parsey R.V. Evaluation of 14 nonlinear deformation algorithms applied to human brain MRI registration. Neuroimage 2009, 46:786-802.
42. Knott G., Holtmaat A., Wilbrecht L., Welker E., Svoboda K. Spine growth precedes synapse formation in the adult neocortex in vivo. Nat. Neurosci. 2006, 9:1117-1124.
43. Korol D.L., Kolo L.L. Estrogen-induced changes in place and response learning in young adult female rats. Behav. Neurosci. 2002, 116:411-420.
44. Kovacevi 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.
45. Lendvai B., Stern E.A., Chen B., Svoboda K. Experience-dependent plasticity of dendritic spines in the developing rat barrel cortex in vivo. Nature 2000, 404:876-881.
46. Lenroot R., Schmitt J., Ordaz S., Wallace G., Neale M., Lerch J., Kendler K., Evans A., Giedd J. Differences in genetic and environmental influences on the human cerebral cortex associated with development during childhood and adolescence. Hum. Brain Mapp. 2009, 30:163-174.
47. Lerch J., Carroll J., Dorr A., Spring S., Evans A., Hayden M., Sled J., Henkelman R. Cortical thickness measured from MRI in the YAC128 mouse model of Huntington's disease. Neuroimage 2008, 41:243-251.
48. Lerch J., Carroll J., Spring S., Bertram L., Schwab C., Hayden M., Markhenkelman R. Automated deformation analysis in the YAC128 Huntington disease mouse model. Neuroimage 2008, 39:32-39.
49. Lippman J., Dunaevsky A. Dendritic spine morphogenesis and plasticity. J. Neurobiol. 2005, 64:47-57.
50. Maguire E.A., Gadian D.G., Johnsrude I.S., Good C.D., Ashburner J., Frackowiak R.S., Frith C.D. Navigation-related structural change in the hippocampi of taxi drivers. Proc. Natl Acad. Sci. USA 2000, 97:4398-4403.
51. Maguire E., Woollett K., Spiers H. London taxi drivers and bus drivers: a structural MRI and neuropsychological analysis. Hippocampus 2006, 16:1091-1101.
52. Markham J.A., Greenough W.T. Experience-driven brain plasticity: beyond the synapse. Neuron Glia Biol. 2004, 1:351-363.
53. May A., Gaser C. Magnetic resonance-based morphometry: a window into structural plasticity of the brain. Curr. Opin. Neurol. 2006, 19:407-411.
54. May A., Hajak G., Ganssbauer S., Steffens T., Langguth B., Kleinjung T., Eichhammer P. Structural brain alterations following 5 days of intervention: dynamic aspects of neuroplasticity. Cereb. Cortex 2006, 17:205-210.
55. McDonald R.J., White N.M. A triple dissociation of memory systems: hippocampus, amygdala, and dorsal striatum. Behav. Neurosci. 1993, 107:3-22.
56. McDonald R.J., White N.M. Parallel information processing in the water maze: evidence for independent memory systems involving dorsal striatum and hippocampus. Behav. Neural Biol. 1994, 61:260-270.
57. Mercer R.E., Kwolek E.M., Bischof J.M., van Eede M., Henkelman R.M., Wevrick R. Regionally reduced brain volume, altered serotonin neurochemistry, and abnormal behavior in mice null for the circadian rhythm output gene Magel2. Am. J. Med. Genet. B Neuropsychiatr. Genet. 2009, 150B:1085-1099.
58. Morris R.G., Garrud P., Rawlins J.N., O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature 1982, 297:681-683.
59. Nieman B., Bock N., Bishop J., Chen X.J., Sled J., Rossant J., Henkelman R.M. Magnetic resonance imaging for detection and analysis of mouse phenotypes. NMR Biomed. 2005, 18:447-468.
60. Nieman B., Bishop J., Dazai J., Bock N., Lerch J., Feintuch A., Chen X.J., Sled J., Henkelman R.M. MR technology for biological studies in mice. NMR Biomed. 2007, 20:291-303.
61. O'Keefe J., Nadel L. The Hippocampus as a Cognitive Map 1978, Clarendon Press Oxford University Press, Oxford New York.
62. Olson A., Eadie B., Ernst C., Christie B. Environmental enrichment and voluntary exercise massively increase neurogenesis in the adult hippocampus via dissociable pathways. Hippocampus 2006, 16:250-260.
63. Packard M.G., McGaugh J.L. Double dissociation of fornix and caudate nucleus lesions on acquisition of two water maze tasks: further evidence for multiple memory systems. Behav. Neurosci. 1992, 106:439-446.
64. Packard M.G., Hirsh R., White N.M. Differential effects of fornix and caudate nucleus lesions on two radial maze tasks: evidence for multiple memory systems. J. Neurosci. 1989, 9:1465-1472.
65. Poldrack R.A., Packard M.G. Competition among multiple memory systems: converging evidence from animal and human brain studies. Neuropsychologia 2003, 41:245-251.
66. Rekart J.L., Meiri K., Routtenberg A. Hippocampal-dependent memory is impaired in heterozygous GAP-43 knockout mice. Hippocampus 2005, 15:1-7.
67. Routtenberg A., Cantallops I., Zaffuto S., Serrano P., Namgung U. Enhanced learning after genetic overexpression of a brain growth protein. Proc. Natl Acad. Sci. USA 2000, 97:7657-7662.
68. Schlaug G. The brain of musicians. A model for functional and structural adaptation. Ann. NY Acad. Sci. 2001, 930:281-299.
69. 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.
70. Shaw P., Greenstein D., Lerch J., Clasen L., Lenroot R., Gogtay N., Evans A., Rapoport J., Giedd J. Intellectual ability and cortical development in children and adolescents. Nature 2006, 440:676-679.
71. Snyder J., Hong N., Mcdonald R., Wojtowicz J. A role for adult neurogenesis in spatial long-term memory. Neuroscience 2005, 130:843-852.
72. Spring S., Lerch J., Henkelman R. Sexual dimorphism revealed in the structure of the mouse brain using three-dimensional magnetic resonance imaging. Neuroimage 2007, 35:1424-1433.
73. Spring S., Lerch J., Wetzel M.K., Evans A., Henkelman R.M. Cerebral asymmetries in 12-week-old C57Bl/6J mice measured by magnetic resonance imaging. Neuroimage 2010, 50:409-415.
74. Squire L.R., Butters N. Neuropsychology of Memory 1984, Guilford Press, New York.
75. Squire L.R., Zola-Morgan S. The medial temporal lobe memory system. Science 1991, 253:1380-1386.
76. Teixeira C., Pomedli S.R., Maei H.R., Kee N., Frankland P. Involvement of the anterior cingulate cortex in the expression of remote spatial memory. J. Neurosci. 2006, 26:7555-7564.
77. Thomas A.G., Marrett S., Saad Z.S., Ruff D.A., Martin A., Bandettini P.A. Functional but not structural changes associated with learning: an exploration of longitudinal voxel-based morphometry (VBM). Neuroimage 2009, 15:117-125.
78. Todd K., Serrano A., Lacaille J., Robitaille R. Glial cells in synaptic plasticity. J. Physiol. Paris 2006, 99:75-83.
79. Tyszka J.M., Readhead C., Bearer E.L., Pautler R.G., Jacobs R.E. Statistical diffusion tensor histology reveals regional dysmyelination effects in the shiverer mouse mutant. Neuroimage 2006, 29:1058-1065.
80. 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. USA 1999, 96:13427-13431.
81. Woolf N.J. A structural basis for memory storage in mammals. Prog. Neurobiol. 1998, 55:59-77.
82. Yu T., Li Z., Jia Z., Clapcote S.J., Liu C., Li S., Asrar S., Pao A., Chen R., Fan N., Carattini-Rivera S., Bechard A.R., Spring S., Henkelman R.M., Stoica G., Matsui S., Nowak N.J., Roder J.C., Chen C., Bradley A., Yu Y.E. A mouse model of Down syndrome trisomic for all human chromosome 21 syntenic regions. Hum. Mol. Genet. 2010, 19:2780-2791.
83. Zijdenbos A.P., Forghani R., Evans A. Automatic "pipeline" analysis of 3-D MRI data for clinical trials: application to multiple sclerosis. IEEE Trans. Med. Imaging 2002, 21:1280-1291.