Auditory brainstem neural activation patterns are altered in EphA4- and ephrin-B2-deficient mice

Journal of Comparative Neurology

Volumn 505, Issue 6, 2007, Pages 669-681

  Miko, Ilona J ^a   Nakamura, Paul A ^a   Henkemeyer, Mark ^b   Cramer, Karina S ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Auditory; Brainstem; c fos; Development; Eph receptor; Ephrin; Tonotopy; Topography

Indexed keywords

EPHRIN RECEPTOR A4; EPHRIN RECEPTOR B2;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUDITORY CORTEX; AUDITORY STIMULATION; BRAIN STEM; COCHLEAR NUCLEUS; CONTROLLED STUDY; GENE EXPRESSION; GENE MUTATION; MOUSE; NONHUMAN; ONCOGENE C FOS; PRIORITY JOURNAL;

ACOUSTIC STIMULATION; ANIMALS; AUDITORY PATHWAYS; AUDITORY PERCEPTION; BODY PATTERNING; BRAIN STEM; CELL COUNT; COCHLEAR NUCLEUS; EPHRIN-B2; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE; MICE, KNOCKOUT; NEURONS; OLIVARY NUCLEUS; PROTO-ONCOGENE PROTEINS C-FOS; RECEPTOR, EPHA4;

EID: 37049003498     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21530     Document Type: Article

References (49)

1. Abercrombie M. 1946. Estimation of nuclear population from microtome sections. Anat Rec 94:239-247.
2. Bianchi LM, Gray NA. 2002. EphB receptors influence growth of ephrin-B1-positive statoacoustic nerve fibers. Eur J Neurosci 16:1499-1506.
3. Brors D, Bodmer D, Pak K, Aletsee C, Schafers M, Dazert S, Ryan AF. 2003. EphA4 provides repulsive signals to developing cochlear ganglion neurites mediated through ephrin-B2 and -B3. J Comp Neurol 462:90-100.
4. Brown MC, Liu TS. 1995. Fos-like immunoreactivity in central auditory neurons of the mouse. J Comp Neurol 357:85-97.
5. Cang J, Kaneko M, Yamada J, Woods G, Stryker MP, Feldheim DA. 2005. Ephrin-as guide the formation of functional maps in the visual cortex. Neuron 48:577-589.
6. Cant NB, Benson CG. 2003. Parallel auditory pathways: projection patterns of the different neuronal populations in the dorsal and ventral cochlear nuclei. Brain Res Bull 60:457-474.
7. Cowan CA, Henkemeyer M. 2002. Ephrins in reverse, park and drive. Trends Cell Biol 12:339-346.
8. Cowan CA, Yokoyama N, Bianchi LM, Henkemeyer M, Fritzsch B. 2000. EphB2 guides axons at the midline and is necessary for normal vestibular function. Neuron 26:417-430.
9. Cramer KS. 2005. Eph proteins and the assembly of auditory circuits. Hear Res 206:42-51.
10. Cramer KS, Rosenberger MH, Frost DM, Cochran SL, Pasquale EB, Rubel EW. 2000. Developmental regulation of EphA4 expression in the chick auditory brainstem. J Comp Neurol 426:270-278.
11. Cramer KS, Karam SD, Bothwell M, Cerretti DP, Pasquale EB, Rubel EW. 2002. Expression of EphB receptors and EphrinB ligands in the developing chick auditory brainstem. J Comp Neurol 452:51-64.
12. Cramer KS, Bermingham-McDonogh O, Krull CE, Rubel EW. 2004. EphA4 signaling promotes axon segregation in the developing auditory system. Dev Biol 269:26-35.
13. Cramer KS, Cerretti DP, Siddiqui SA. 2006. EphB2 regulates axonal growth at the midline in the developing auditory brainstem. Dev Biol 295:76-89.
14. Dalva MB, McClelland AC, Kayser MS. 2007. Cell adhesion molecules: signalling functions at the synapse. Nat Rev Neurosci 8:206-220.
15. Dravis C, Yokoyama N, Chumley MJ, Cowan CA, Silvany RE, Shay J, Baker LA, Henkemeyer M. 2004. Bidirectional signaling mediated by ephrin-B2 and EphB2 controls urorectal development. Dev Biol 271: 272-290.
16. Dufour A, Seibt J, Passante L, Depaepe V, Ciossek T, Frisen J, Kullander K, Flanagan JG, Polleux F, Vanderhaeghen P. 2003. Area specificity and topography of thalamocortical projections are controlled by ephrin/ Eph genes. Neuron 39:453-465.
17. Ehret G, Fischer R. 1991. Neuronal activity and tonotopy in the auditory system visualized by c-fos gene expression. Brain Res 567:350-354.
18. Ellis J, Liu Q, Breitman M, Jenkins NA, Gilbert DJ, Copeland NG, Tempest HV, Warren S, Muir E, Schilling H, et al. 1995. Embryo brain kinase: a novel gene of the eph/elk receptor tyrosine kinase family. Mech Dev 52:319-341.
19. Feldheim DA, Kim YI, Bergemann AD, Frisen J, Barbacid M, Flanagan JG. 2000. Genetic analysis of ephrin-A2 and ephrin-A5 shows their requirement in multiple aspects of retinocollicular mapping. Neuron 25:563-574.
20. Feldheim DA, Nakamoto M, Osterfield M, Gale NW, DeChiara TM, Rohatgi R, Yancopoulos GD, Flanagan JG. 2004. Loss-of-function analysis of EphA receptors in retinotectal mapping. J Neurosci 24:2542-2550.
21. Flanagan JG, Vanderhaeghen P. 1998. The ephrins and Eph receptors in neural development. Annu Rev Neurosci 21:309-345.
22. Friauf E. 1992. Tonotopic order in the adult and developing auditory system of the rat as shown by c-fos immunocytochemistry. Eur J Neurosci 4:798-812.
23. Friauf E. 1995. C-fos immunocytochemical evidence for acoustic pathway mapping in rats. Behav Brain Res 66:217-224.
24. Friauf E, Lehmann C. 1999. Development of auditory brainstem circuitry. Activity-dependent and activity-independent processes. Cell Tissue Res 297:187-195.
25. Frisen J, Yates PA, McLaughlin T, Friedman GC, O'Leary DD, Barbacid M. 1998. Ephrin-A5 (AL-1/RAGS) is essential for proper retinal axon guidance and topographic mapping in the mammalian visual system. Neuron 20:235-243.
26. Gale NW, Holland SJ, Valenzuela DM, Flenniken A, Pan L, Ryan TE, Henkemeyer M, Strebhardt K, Hirai H, Wilkinson DG, Pawson T, Davis S, Yancopoulos GD. 1996. Eph receptors and ligands comprise two major specificity subclasses and are reciprocally compartmentalized during embryogenesis. Neuron 17:9-19.
27. Garel S, Rubenstein JL. 2004. Intermediate targets in formation of topographic projections: inputs from the thalamocortical system. Trends Neurosci 27:533-539.
28. Grunwald IC, Korte M, Adelmann G, Plueck A, Kullander K, Adams RH, Frotscher M, Bonhoeffer T, Klein R. 2004. Hippocampal plasticity requires postsynaptic ephrinBs. Nat Neurosci 7:33-40.
29. Hansen MJ, Dallal GE, Flanagan JG. 2004. Retinal axon response to ephrin-as shows a graded, concentration-dependent transition from growth promotion to inhibition. Neuron 42:717-730.
30. Henkemeyer M, Marengere LE, McGlade J, Olivier JP, Conlon RA, Holmyard DP, Letwin K, Pawson T. 1994. Immunolocalization of the Nuk receptor tyrosine kinase suggests roles in segmental patterning of the brain and axonogenesis. Oncogene 9:1001-1014.
31. Himanen JP, Chumley MJ, Lackmann M, Li C, Barton WA, Jeffrey PD, Vearing C, Geleick D, Feldheim DA, Boyd AW, Henkemeyer M, Nikolov DB. 2004. Repelling class discrimination: ephrin-A5 binds to and activates EphB2 receptor signaling. Nat Neurosci 7:501-509.
32. Hoffpauir BK, Grimes JL, Mathers PH, Spirou GA. 2006. Synaptogenesis of the calyx of Held: rapid onset of function and one-to-one morphological innervation. J Neurosci 26:5511-5523.
33. Holmberg J, Frisen J. 2002. Ephrins are not only unattractive. Trends Neurosci 25:239-243.
34. Hsieh CY, Hong CT, Cramer KS. 2007. Deletion of the Eph receptor EphA4 enhances deafferentation-induced ipsilateral sprouting in auditory brainstem projections. J Comp Neurol 504:508-518.
35. Huffman KJ, Cramer KS. 2007. EphA4 misexpression alters tonotopic projections in the auditory brainstem. Dev Neurobiol 67:1655-1668.
36. Kaur S, Lazar R, Metherate R. 2004. Intracortical pathways determine breadth of subthreshold frequency receptive fields in primary auditory cortex. J Neurophysiol 91:2551-2567.
37. Kil J, Kageyama GH, Semple MN, Kitzes LM. 1995. Development of ventral cochlear nucleus projections to the superior olivary complex in gerbil. J Comp Neurol 353:317-340.
38. Kim G, Kandler K. 2003. Elimination and strengthening of glycinergic/GABAergic connections during tonotopic map formation. Nat Neurosci 6:282-290.
39. Kovacs KJ. 1998. c-Fos as a transcription factor: a stressful (re)view from a functional map. Neurochem Int 33:287-297.
40. Leake PA, Snyder RL, Hradek GT. 2002. Postnatal refinement of auditory nerve projections to the cochlear nucleus in cats. J Comp Neurol 448: 6-27.
41. Leighton PA, Mitchell KJ, Goodrich LV, Lu X, Pinson K, Scherz P, Skarnes WC, Tessier-Lavigne M. 2001. Defining brain wiring patterns and mechanisms through gene trapping in mice. Nature 410:174-179.
42. Mann F, Harris WA, Holt CE. 2004. New views on retinal axon development: a navigation guide. Int J Dev Biol 48:957-964.
43. Marquardt T, Shirasaki R, Ghosh S, Andrews SE, Carter N, Hunter T, Pfaff SL. 2005. Coexpressed EphA receptors and ephrin-A ligands mediate opposing actions on growth cone navigation from distinct membrane domains. Cell 121:127-139.
44. McLaughlin T, O'Leary DD. 2005. Molecular gradients and development of retinotopic maps. Annu Rev Neurosci 28:327-355.
45. McLaughlin T, Hindges R, Yates PA, O'Leary DD. 2003. Bifunctional action of ephrin-B1 as a repellent and attractant to control bidirectional branch extension in dorsal-ventral retinotopic mapping. Development 130:2407-2418.
46. Mikaelian DO, Warfield D, Norris O. 1974. Genetic progressive hearing loss in the C57-b16 mouse. Relation of behavioral responses to chochlear anatomy. Acta Otolaryngol 77:327-334.
47. Morgan JI, Curran T. 1989. Calcium and proto-oncogene involvement in the immediate-early response in the nervous system. Ann N Y Acad Sci 568:283-290.
48. Murai KK, Nguyen LN, Irie F, Yamaguchi Y, Pasquale EB. 2003. Control of hippocampal dendritic spine morphology through ephrin-A3/EphA4 signaling. Nat Neurosci 6:153-160.
49. Ouagazzal AM, Reiss D, Romand R. 2006. Effects of age-related hearing loss on startle reflex and prepulse inhibition in mice on pure and mixed C57BL and 129 genetic background. Behav Brain Res 172:307-315.