Mutational ataxia resulting from abnormal vestibular acquisition and processing is partially compensated for

Behavioral Neuroscience

Volumn 126, Issue 2, 2012, Pages 301-313

  Kopecky, Benjamin ^a   DeCook, Rhonda ^b   Fritzsch, Bernd ^b  

^a The University of Iowa   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

Catwalk; N Myc; Regularity index; Stride length; Stride speed

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATAXIA; CEREBELLUM; COCHLEA; CONTROLLED STUDY; EAR MALFORMATION; EMBRYO DEVELOPMENT; EVOKED BRAIN STEM AUDITORY RESPONSE; GAIT DISORDER; HAIR CELL; MOUSE; NONHUMAN; ONCOGENE MYC; VESTIBULAR DISORDER; VESTIBULAR SYSTEM; ANIMAL; CONGENITAL MALFORMATION; GAIT; GENETICS; MOUSE MUTANT; PATHOPHYSIOLOGY; PRENATAL DEVELOPMENT; VESTIBULE;

ANIMALS; CEREBELLUM; COCHLEA; GAIT; GAIT ATAXIA; GENES, MYC; MICE; MICE, KNOCKOUT; VESTIBULAR DISEASES; VESTIBULE, LABYRINTH;

EID: 84864296723     PISSN: 07357044     EISSN: 19390084     Source Type: Journal    
DOI: 10.1037/a0026896     Document Type: Article

References (62)

1. Belyantseva, I. A., Perrin, B. J., Sonnemann, K. J., Zhu, M., Stepanyan, R., McGee, J.,... Ervasti, J. M. (2009). Gamma-actin is required for cytoskeletal maintenance but not development. Proceedings of the National Academy of Sciences of the United States of America, 106, 9703-9708. doi:10.1073/pnas.0900221106
2. Beraneck, M., McKee, J. L., Aleisa, M., & Cullen, K. E. (2008). Asymmetric recovery in cerebellar-deficient mice following unilateral labyrinthectomy. Journal of Neurophysiology, 100, 945-958. doi:10.1152/jn.90319.2008
3. Bermingham, N. A., Hassan, B. A., Wang, V. Y., Fernandez, M., Banfi, S., Bellen, H. J.,... Zoghbi, H. Y. (2001). Proprioceptor pathway development is dependent on Math1. Neuron, 30, 411-422. doi:10.1016/S0896-6273(01)00305-1
4. Caddy, K. W., Sidman, R. L., & Eicher, E. M. (1981). Stumbler, a new mutant mouse with cerebellar disease. Brain Research, 208, 251-255. doi:10.1016/0006-8993(81)90643-0
5. Cendelin, J., Voller, J., & Vozeh, F. (2010). Ataxic gait analysis in a mouse model of the olivocerebellar degeneration. Behavioural Brain Research, 210, 8-15. doi:10.1016/j.bbr.2010.01.035
6. Chizhikov, V. V., & Millen, K. J. (2004). Control of roof plate formation by Lmx1a in the developing spinal cord. Development, 131, 2693-2705. doi:10.1242/dev.01139
7. Cullen, K. E., Minor, L. B., Beraneck, M., & Sadeghi, S. G. (2009). Neural substrates underlying vestibular compensation: Contribution of peripheral versus central processing. Journal of Vestibular Research, 19, 171-182.
8. Cutuli, D., Rossi, S., Burello, L., Laricchiuta, D., De Chiara, V., Foti, F.,... Petrosini, L. (2011). Before or after does it matter? Different protocols of environmental enrichment differently influence motor, synaptic and structural deficits of cerebellar origin. Neurobiology of Disease, 42, 9-20. doi:S0969-9961(10)00400-6[pii]
9. Davis, A. C., Wims, M., Spotts, G. D., Hann, S. R., & Bradley, A. (1993). A null C-Myc mutation causes lethality before 10.5 days of gestation in homozygotes and reduced fertility in heterozygous female mice. Genes and Development, 7, 671-682. doi:10.1101/gad.7.4.671
10. de Caprona, M. D., Beisel, K. W., Nichols, D. H., & Fritzsch, B. (2004). Partial behavioral compensation is revealed in balance tasked mutant mice lacking otoconia. Brain Research Bulletin, 64, 289-301. doi: 10.1016/j.brainresbull.2004.08.004
11. Dominguez-Frutos, E., Lopez-Hernandez, I., Vendrell, V., Neves, J., Gallozzi, M., Gutsche, K.,... Schimmang, T. (2011). N-Myc controls proliferation, morphogenesis and patterning of the inner ear. Journal of Neuroscience, 31, 7178-7189. doi:31/19/7178[pii]
12. Dutia, M. B. (2010). Mechanisms of vestibular compensation: Recent advances. Current Opinion in Otolaryngology and Head and Neck Surgery, 18, 420-424. doi:10.1097/MOO.0b013e32833de71f
13. Eilers, M., & Eisenman, R. N. (2008). Myc's broad reach. Genes and Development, 22, 2755-2766. doi:10.1101/gad.1712408
14. Foti, F., Laricchiuta, D., Cutuli, D., De Bartolo, P., Gelfo, F., Angelucci, F., & Petrosini, L. (2011). Exposure to an enriched environment accelerates recovery from cerebellar lesion. Cerebellum, 10, 104-119. doi: 10.1007/s12311-010-0236-z
15. Fritzsch, B., Signore, M., & Simeone, A. (2001). Otx1 null mutant mice show partial segregation of sensory epithelia comparable to lamprey ears. Development Genes and Evolution, 211, 388-396. doi:10.1007/s004270100166
16. Goddard, M., Zheng, Y., Darlington, C. L., & Smith, P. F. (2008). Locomotor and exploratory behavior in the rat following bilateral vestibular deafferentation. Behavioral Neuroscience, 122, 448-459. doi:10.1037/0735-7044.122.2.448
17. Green, M. C., & Sidman, R. L. (1962). Tottering-a neuromusclar mutation in the mouse. And its linkage with oligosyndacylism. Journal of Heredity, 53, 233-237.
18. Grüsser, C., & Grüsser-Cornehls, U. (1998). Improvement in motor performance of Weaver mutant mice following lesions of the cerebellum. Behavioural Brain Research, 97, 189-194. doi:10.1016/S01664328(98)00042-4
19. Grüsser-Cornehls, U., & Baurle, J. (2001). Mutant mice as a model for cerebellar ataxia. Progress in Neurobiology, 63, 489-540. doi:10.1016/S0301-0082(00)00024-1
20. Grüsser-Cornehls, U., Grüsser, C., & Baurle, J. (1999). Vermectomy enhances parvalbumin expression and improves motor performance in weaver mutant mice: An animal model for cerebellar ataxia. Neuroscience, 91, 315-326. doi:10.1016/S0306-4522(98)00618-6
21. Hamers, F. P. T, Koopmans, G. C., & Joosten, E. A. (2006). CatWalk-assisted gait analysis in the assessment of spinal cord injury. Journal of Neurotrauma, 23, 537-548. doi:10.1089/neu.2006.23.537
22. Hamers, F. P. T, Lankhorst, A. J., van Laar, T. J., Veldhuis, W. B., & Gispen, W. H. (2001). Automated quantitative gait analysis during overground locomotion in the rat: Its application to spinal cord contusion and transection injuries. Journal of Neurotrauma, 18, 187-201. doi: 10.1089/08977150150502613
23. Helmchen, C., Klinkenstein, J. C., Kruger, A., Gliemroth, J., Mohr, C., & Sander, T. (2011). Structural brain changes following peripheral vestibulo-cochlear lesion may indicate multisensory compensation. Journal of Neurology, Neurosurgery & Psychiatry, 82, 309-316. doi: 10.1136/jnnp.2010.204925
24. Herbin, M., Hackert, R., Gasc, J. P., & Renous, S. (2007). Gait parameters of treadmill versus overground locomotion in mouse. Behavioural Brain Research, 181, 173-179. doi:10.1016/j.bbr.2007.04.001
25. Hollander, W. F., & Waggie, K. S. (1977). Meander tail: A recessive mutant located in chromosome 4 of the mouse. Journal of Heredity, 68, 403-406.
26. Jahan, I., Kersigo, J., Pan, N., & Fritzsch, B. (2010). Neurod1 regulates survival and formation of connections in mouse ear and brain. Cell and Tissue Research, 341, 95-110. doi:10.1007/s00441-010-0984-6
27. Jahan, I., Pan, N., Kersigo, J., & Fritzsch, B. (2010). Neurod1 suppresses hair cell differentiation in ear ganglia and regulates hair cell subtype development in the cochlea. PLoS One, 5, e11661. doi:10.1371/journal.pone.0011661
28. Jones, S. M., Jones, T. A., Mills, K. N., & Gaines, G. C. (2009). Anatomical and physiological considerations in vestibular dysfunction and compensation. Seminars in Hearing, 30, 231-241. doi:10.1055/s-00291241124
29. Jones, T. A., Jones, S. M., & Hoffman, L. F. (2008). Resting discharge patterns of macular primary afferents in otoconia-deficient mice. Journal of the Association for Research in Otolaryngology, 9, 490-505. doi: 10.1007/s10162-008-0132-0
30. Jones, T. A., Jones, S. M., Vijayakumar, S., Brugeaud, A., Bothwell, M., & Chabbert, C. (2011). The adequate stimulus for mammalian linear vestibular evoked potentials (VsEPs). Hearing Research, 280, 133-140.
31. Kaemmerer, W. F., & Low, W. C. (1999). Cerebellar allografts survive and transiently alleviate ataxia in a transgenic model of spinocerebellar ataxia type-1. Experimental Neurology, 158, 301-311. doi:10.1006/exnr.1999.7099
32. Kale, A., Amende, I., Meyer, G. P., Crabbe, J. C., & Hampton, T. G. (2004). Ethanol's effects on gait dynamics in mice investigated by ventral plane videography. Alcoholism, Clinical and Experimental Research, 28, 1839-1848. doi:10.1097/01.ALC.0000148103.09378.81
33. Khan, Z., Carey, J., Park, H. J., Lehar, M., Lasker, D., & Jinnah, H. A. (2004). Abnormal motor behavior and vestibular dysfunction in the stargazer mouse mutant. Neuroscience, 127, 785-796. doi:10.1016/j.neuroscience.2004.05.052
34. Klisch, T. J., Xi, Y., Flora, A., Wang, L., Li, W., & Zoghbi, H. Y. (2011). In Vivo Atoh1 targetome reveals how a proneural transcription factor regulates cerebellar development. Proceedings of the National Academy of Sciences of the United States of America, 108, 3288-3293. doi: 10.1073/pnas.1100230108
35. Knoepfler, P. S., & Kenney, A. M. (2006). Neural precursor cycling at sonic speed: N-Myc pedals, GSK-3 brakes. Cell Cycle, 5, 47-52. doi: 10.4161/cc.5.1.2292
36. Koopmans, G. C., Deumens, R., Brook, G., Gerver, J., Honig, W. M., Hamers, F. P., & Joosten, E. A. (2007). Strain and locomotor speed affect over-ground locomotion in intact rats. Physiology and Behavior, 92, 993-1001. doi:S0031-9384(07)00285-5[pii]
37. Kopecky, B., Santi, P., Johnson, S., Schmitz, H., & Fritzsch, B. (2011). Conditional deletion of N-Myc disrupts neurosensory and non-sensory development of the ear. Developmental Dynamics, 240, 1373-1390. doi:10.1002/dvdy.22620
38. Lasorella, A., Boldrini, R., Dominici, C., Donfrancesco, A., Yokota, Y., Inserra, A., & Iavarone, A. (2002). Id2 is critical for cellular proliferation and is the oncogenic effector of N-Myc in human neuroblastoma. Cancer Research, 62, 301-306.
39. Lasorella, A., Noseda, M., Beyna, M., Yokota, Y., & Iavarone, A. (2000). Id2 is a retinoblastoma protein target and mediates signalling by Myc oncoproteins. Nature, 407, 592-598. doi:10.1038/35036504
40. Maklad, A., Kamel, S., Wong, E., & Fritzsch, B. (2010). Development and organization of polarity-specific segregation of primary vestibular afferent fibers in mice. Cell and Tissue Research, 340, 303-321. doi:10.1007/s00441-010-0944-1
41. Millonig, J. H., Millen, K. J., & Hatten, M. E. (2000). The mouse Dreher gene Lmx1a controls formation of the roof plate in the vertebrate CNS. Nature, 403, 764-769. doi:10.1038/35001573
42. Modak, S., & Cheung, N. K. (2010). Neuroblastoma: Therapeutic strategies for a clinical enigma. Cancer Treatment Reviews, 36, 307-317.
43. Morsli, H., Tuorto, F., Choo, D., Postiglione, M. P., Simeone, A., & Wu, D. K. (1999). Otx1 and Otx2 activities are required for the normal development of the mouse inner ear. Development, 126, 2335-2343.
44. Mott, J. L., Kurita, S., Cazanave, S. C., Bronk, S. F., Werneburg, N. W., & Fernandez-Zapico, M. E. (2010). Transcriptional suppression of mir29b-1/mir-29a promoter by C-Myc, hedgehog, and NF-kappaB. Journal of Cellular Biochemistry, 110, 1155-1164. doi:10.1002/jcb.22630
45. Mullen, R. J., Eicher, E. M., & Sidman, R. L. (1976). Purkinje cell degeneration, a new neurological mutation in the mouse. Proceedings of the National Academy of Sciences of the United States of America, 73, 208-212. doi:10.1073/pnas.73.1.208
46. Nichols, D. H., Pauley, S., Jahan, I., Beisel, K. W., Millen, K. J., & Fritzsch, B. (2008). Lmx1a is required for segregation of sensory epithelia and normal ear histogenesis and morphogenesis. Cell and Tissue Research, 334, 339-358. doi:10.1007/s00441-008-0709-2
47. Ohyama, T., & Groves, A. K. (2004). Generation of Pax2-Cre mice by modification of a Pax2 bacterial artificial chromosome. Genesis, 38, 195-199. doi:10.1002/gene.20017
48. Pan, N., Jahan, I., Kersigo, J., Kopecky, B., Santi, P., Johnson, S.,... Fritzsch, B. (2011). Conditional deletion of Atoh1 using Pax2-Cre results in viable mice without differentiated cochlear hair cells that have lost most of the organ of Corti. Hearing Research, 275, 66-80. doi: S0378-5955(10)00435-1[pii]
49. Parietti-Winkler, C., Gauchard, G. C., Simon, C., & Perrin, P. P. (2011). Pre-operative vestibular pattern and balance compensation after vestibular schwannoma surgery. Neuroscience, 172, 285-292. doi:10.1016/j.neuroscience.2010.10.059
50. Pauley, S., Kopecky, B., Beisel, K., Soukup, G., & Fritzsch, B. (2008). Stem Cells and molecular strategies to restore hearing. Panminerva Medica, 50, 41-53.
51. Pauley, S., Lai, E., & Fritzsch, B. (2006). Foxg1 is required for morphogenesis and histogenesis of the mammalian inner ear. Developmental Dynamics, 235, 2470-2482. doi:10.1002/dvdy.20839
52. Romand, R., Hirning-Folz, U., & Ehret, G. (1994). N-myc expression in the embryonic cochlea of the mouse. Hearing Research, 72, 53-58. doi:10.1016/0378-5955(94)90205-4
53. Ruggero, D. (2009). The role of Myc-induced protein synthesis in cancer. Cancer Research, 69, 8839-8843. doi:10.1158/0008-5472.CAN-091970
54. Sidman, R. L., Appel, S. H., & Fullier, J. F. (1965). Neurological Mutants of the Mouse. Science, 150, 513-516. doi:10.1126/science.150.3695.513
55. Sidman, R. L., Lane, P. W., & Dickie, M. M. (1962). Staggerer, a new mutation in the mouse affecting the cerebellum. Science, 137, 610-612. doi:10.1126/science.137.3530.610
56. Simon, D., Seznec, H., Gansmuller, A., Carelle, N., Weber, P., Metzger, D.,... Puccio, H. (2004). Friedreich ataxia mouse models with progressive cerebellar and sensory ataxia reveal autophagic neurodegeneration in dorsal root ganglia. Journal of Neuroscience, 24, 1987-1995. doi: 10.1523/JNEUROSCI.4549-03.2004
57. Stanton, B. R., Perkins, A. S., Tessarollo, L., Sassoon, D. A., & Parada, L. F. (1992). Loss of N-Myc function results in embryonic lethality and failure of the epithelial component of the embryo to develop. Genes and Development, 6, 2235-2247. doi:10.1101/gad.6.12a.2235
58. Vandeputte, C., Taymans, J. M., Casteels, C., Coun, F., Ni, Y., Van Laere, K., & Baekelandt, V. (2010). Automated quantitative gait analysis in animal models of movement disorders. BMC Neuroscience, 11, 92. doi:10.1186/1471-2202-11-92
59. Vrinten, D. H., & Hamers, F. F. T. (2003). `CatWalk' automated quantitative gait analysis as a novel method to assess mechanical allodynia in the rat; a comparison with von Frey testing. Pain, 102, 203-209. doi:10.1016/s0304-3959(02)00382-2
60. Weimar, W. R., Lane, P. W., & Sidman, R. L. (1982). Vibrator (vb): a spinocerebellar system degeneration with autosomal recessive inheritance in mice. Brain Research, 251, 357-364. doi:10.1016/0006-8993(82)90754-5
61. Wey, A., Martinez Cerdeno, V., Pleasure, D., & Knoepfler, P. S. (2010). cand N-Myc regulate neural precursor cell fate, cell cycle, and metabolism to direct cerebellar development. Cerebellum, 9, 537-547. doi: 10.1007/s12311-010-0190-9
62. Wooley, C. M., Xing, S., Burgess, R. W., Cox, G. A., & Seburn, K. L. (2009). Age, experience and genetic background influence treadmill walking in mice. Physiology and Behavior, 96, 350-361. doi:10.1016/j.physbeh.2008.10.020