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The Journal of Neuroscience, May 27, 2009, 29(21):6780-6793; doi:10.1523/JNEUROSCI.0801-09.2009

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Behavioral/Systems/Cognitive
Functional Role of a Specialized Class of Spinal Commissural Inhibitory Neurons during Fast Escapes in Zebrafish

Chie Satou,^1,2 Yukiko Kimura,¹ Tsunehiko Kohashi,³ Kazuki Horikawa,⁴ Hiroyuki Takeda,⁴ Yoichi Oda,³ and Shin-ichi Higashijima^1,2

¹National Institutes of Natural Sciences, Okazaki Institute for Integrative Bioscience, National Institute for Physiological Sciences, Okazaki, Aichi 444-8787, Japan, ²Department of Physiological Sciences, Graduate University for Advanced Studies (SOKENDAI), Okazaki, Aichi 444-8585, Japan, ³Division of Biological Science, Graduate School of Science, Nagoya University, Nagoya 464-8602, Japan, and ⁴Department of Biological Sciences, Graduate School of Science, University of Tokyo, Bunkyo-ku, Tokyo 113-8654, Japan

Correspondence should be addressed to Shin-ichi Higashijima, Okazaki Institute for Integrative Bioscience, Higashiyama 5-1, Myodaiji, Okazaki, Aichi 444-8787, Japan. Email: shigashi{at}nips.ac.jp

In teleost fish, the Mauthner (M) cell, a large reticulospinal neuron in the brainstem, triggers escape behavior. Spinal commissural inhibitory interneurons that are electrotonically excited by the M-axon have been identified, but the behavioral roles of these neurons have not yet been addressed. Here, we studied these neurons, named CoLo (commissural local), in larval zebrafish using an enhancer-trap line in which the entire population of CoLos was visualized by green fluorescent protein. CoLos were present at one cell per hemi-segment. Electrophysiological recordings showed that an M-spike evoked a spike in CoLos via electrotonic transmission and that CoLos made monosynaptic inhibitory connections onto contralateral primary motoneurons, consistent with the results in adult goldfish. We further showed that CoLos were active only during escapes. We examined the behavioral roles of CoLos by investigating escape behaviors in CoLo-ablated larvae. The results showed that the escape behaviors evoked by sound/vibration stimuli were often impaired with a reduced initial bend of the body, indicating that CoLos play important roles in initiating escapes. We obtained several lines of evidence that strongly suggested that the impaired escapes occurred during bilateral activation of the M-cells: in normal larvae, CoLo-mediated inhibitory circuits enable animals to perform escapes even in these occasions by silencing the output of the slightly delayed firing of the second M-cell. This study illustrates (1) a clear example of the behavioral role of a specialized class of interneurons and (2) the capacity of the spinal circuits to filter descending commands and thereby produce the appropriate behavior.

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Received Feb. 17, 2009; revised April 7, 2009; accepted April 15, 2009.

Correspondence should be addressed to Shin-ichi Higashijima, Okazaki Institute for Integrative Bioscience, Higashiyama 5-1, Myodaiji, Okazaki, Aichi 444-8787, Japan. Email: shigashi{at}nips.ac.jp

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