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The Journal of Neuroscience, September 3, 2003, 23(22):8159-8166

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Mutations in deadly seven/notch1a Reveal Developmental Plasticity in the Escape Response Circuit

Katharine S. Liu,^1 * Michelle Gray,^2,3 * Stefanie J. Otto,¹ Joseph R. Fetcho,¹ and Christine E. Beattie^2,3,4

¹Department of Neurobiology, State University of New York at Stony Brook, Stony Brook, New York 11794, ²Center for Molecular Neurobiology, ³Molecular, Cellular, and Developmental Biology Program, and ⁴Department of Neuroscience, The Ohio State University, Columbus, Ohio 43210

The relatively simple neural circuit driving the escape response in zebrafish offers an excellent opportunity to study properties of neural circuit formation. The hindbrain Mauthner cell is an essential component of this circuit. Mutations in the zebrafish deadly seven/notch1a (des) gene result in supernumerary Mauthner cells. We addressed whether and how these extra cells are incorporated into the escape-response circuit. Calcium imaging revealed that all Mauthner cells in des^b420 mutants were active during an elicited escape response. However, the kinematic performance of the escape response in mutant larvae was very similar to wild-type fish. Analysis of the relationship between Mauthner axon collaterals and spinal neurons revealed that there was a decrease in the number of axon collaterals per Mauthner axon in mutant larvae compared with wild-type larvae, indicative of a decrease in the number of synapses formed with target spinal neurons. Moreover, we show that Mauthner axons projecting on the same side of the nervous system have primarily nonoverlapping collaterals. These data support the hypothesis that excess Mauthner cells are incorporated into the escape-response circuit, but they divide their target territory to maintain a normal response, thus demonstrating plasticity in the formation of the escape-response circuit. Such plasticity may be key to the evolution of the startle responses in mammals, which use larger populations of neurons in circuits similar to those in the fish escape response.

Key words: hindbrain; behavior; calcium imaging; mutant analysis; Mauthner cell; notch1a; axon collaterals

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Received May 1, 2003; revised July 3, 2003; accepted July 16, 2003.

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