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The Journal of Neuroscience, March 24, 2004, 24(12):3070-3076; doi:10.1523/JNEUROSCI.5624-03.2004

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Development/Plasticity/Repair
Hox Gene Misexpression and Cell-Specific Lesions Reveal Functionality of Homeotically Transformed Neurons

Melina E. Hale,^1,2,3 Mazen A. Kheirbek,² Julie E. Schriefer,¹ and Victoria E. Prince^1,2,4,5

¹Department of Organismal Biology and Anatomy, Committees on ²Neurobiology, ³Computational Neurobiology, ⁴Evolutionary Biology, and ⁵Developmental Biology, University of Chicago, Chicago, Illinois 60637

Hox genes are critical for establishing the segmental pattern of the vertebrate hindbrain. Changes in their expression can alter neural organization of hindbrain segments and may be a mechanism for brain evolution. To test the hypothesis that neurons induced through changes in Hox gene expression can integrate into functional neural circuits, we examined the roles of ectopic Mauthner cells (M-cells) in the escape response of larval zebrafish. The activity of the paired Mauthner cells in rhombomere 4 (r4) has been shown to be critical for generating a high-performance startle behavior in response to stimulation of the tail (Liu and Fetcho, 1999). Previous studies have found that misexpression of particular Hox genes causes ectopic M-cells to be generated in r2 in addition to the r4 cells (Alexandre et al., 1996; McClintock et al., 2001). With calcium imaging, we found that the homeotically transformed neurons respond to startle stimuli. To determine the roles of ectopic and endogenous M-cells in the behavior, we lesioned the r2, r4, or both M-cells with cell-specific laser lesion and examined the effect on startle performance. Lesion of the normal M-cells did not decrease escape performance when the ectopic cells were present. These results indicate that the homeotically transformed Mauthner cells are fully functional in the escape circuit and are functionally redundant with normal M-cells. We suggest that such functional redundancy between neurons may provide a substrate for evolution of neural circuits.

Key words: hindbrain; Hox genes; homeosis; Mauthner cell; startle; escape response

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Received Dec 20, 2003; revised February 2, 2004; accepted February 4, 2004.

This article has been cited by other articles:

				K. Nishikawa, A. A. Biewener, P. Aerts, A. N. Ahn, H. J. Chiel, M. A. Daley, T. L. Daniel, R. J. Full, M. E. Hale, T. L. Hedrick, et al. Neuromechanics: an integrative approach for understanding motor control Integr. Comp. Biol., July 1, 2007; 47(1): 16 - 54. [Abstract] [Full Text] [PDF]

				S. Wohl and S. Schuster The predictive start of hunting archer fish: a flexible and precise motor pattern performed with the kinematics of an escape C-start J. Exp. Biol., January 15, 2007; 210(2): 311 - 324. [Abstract] [Full Text] [PDF]

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