Portal de Periódicos da CAPES

Local Spinal Cord Circuits and Bilateral Mauthner Cell Activity Function Together to Drive Alternative Startle Behaviors

2017; Elsevier BV; Volume: 27; Issue: 5 Linguagem: Inglês

10.1016/j.cub.2017.01.019

1879-0445

Yen-Chyi Liu, Melina E. Hale,

Sleep and Wakefulness Research

The reticulospinal Mauthner cells (M-cells) of the startle circuit have been considered to be dedicated to one basic motor output and the C-type startle response in fish. The neural circuit underlying the C-start, a startle behavior in which the fish forms a "C"-shaped body bend has been described in depth in goldfish and zebrafish [1Fetcho J.R. Faber D.S. Identification of motoneurons and interneurons in the spinal network for escapes initiated by the mauthner cell in goldfish.J. Neurosci. 1988; 8: 4192-4213Crossref PubMed Google Scholar, 2Faber D.S. Fetcho J.R. Korn H. Neuronal networks underlying the escape response in goldfish. General implications for motor control.Ann. N Y Acad. Sci. 1989; 563: 11-33Crossref PubMed Scopus (139) Google Scholar] and is thought to occur in other species [3Zottoli S.J. Comparative morphology of the Mauthner cell in fish and amphibians.in: Faber D.S. Korn H. Neurobiology of the Mauthner Cell. Raven Press, 1978: 13-45Google Scholar, 4Bierman H.S. Zottoli S.J. Hale M.E. Evolution of the Mauthner cell axon cap and the fast-start escape response.Brain Behav. Evol. 2009; 73: 174-187Crossref PubMed Scopus (18) Google Scholar]. However, previous research has shown that some species can perform a second type of startle called the S-start [5Hale M.E. S- and C-start escape responses of the muskellunge (Esox masquinongy) require alternative neuromotor mechanisms.J. Exp. Biol. 2002; 205: 2005-2016PubMed Google Scholar, 6Schriefer J.E. Hale M.E. Strikes and startles of northern pike (Esox lucius): A comparison of muscle activity and kinematics between S-start behaviors.J. Exp. Biol. 2004; 207: 535-544Crossref PubMed Scopus (45) Google Scholar, 7Liu Y.C. Bailey I. Hale M.E. Alternative startle motor patterns and behaviors in the larval zebrafish (Danio rerio).J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 2012; 198: 11-24Crossref PubMed Scopus (37) Google Scholar]. This startle response, in which the first movement creates an "S"-shaped body bend achieved with regional muscle activity on left and right sides, cannot be explained by M-cell circuit models. Here we use larval zebrafish to examine the S-start circuit. Since S-starts are elicited through tail stimulation [5Hale M.E. S- and C-start escape responses of the muskellunge (Esox masquinongy) require alternative neuromotor mechanisms.J. Exp. Biol. 2002; 205: 2005-2016PubMed Google Scholar, 6Schriefer J.E. Hale M.E. Strikes and startles of northern pike (Esox lucius): A comparison of muscle activity and kinematics between S-start behaviors.J. Exp. Biol. 2004; 207: 535-544Crossref PubMed Scopus (45) Google Scholar, 7Liu Y.C. Bailey I. Hale M.E. Alternative startle motor patterns and behaviors in the larval zebrafish (Danio rerio).J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 2012; 198: 11-24Crossref PubMed Scopus (37) Google Scholar] and ablating M-cells abolishes short-latency tail-elicited startles [8Liu K.S. Fetcho J.R. Laser ablations reveal functional relationships of segmental hindbrain neurons in zebrafish.Neuron. 1999; 23: 325-335Abstract Full Text Full Text PDF PubMed Scopus (320) Google Scholar, 9Hale M.E. Kheirbek M.A. Schriefer J.E. Prince V.E. Hox gene misexpression and cell-specific lesions reveal functionality of homeotically transformed neurons.J. Neurosci. 2004; 24: 3070-3076Crossref PubMed Scopus (33) Google Scholar], we hypothesized that M-cell activity was necessary for S-start generation. Our findings show that the M-cells fire simultaneously to generate the S-start. However, simultaneous M-cell spikes generated through direct current injection were not sufficient to generate S-starts. Through recordings of motoneurons, inhibitory interneurons, and sensory neurons, we uncover a mechanism for generating alternative startle behaviors; local sensory inputs drive inhibitory interneuron activity, which inhibits caudal motoneurons and pre-conditions their excitability prior to the arrival of M-cell spikes in the tail. We suggest that this motoneuron hyperpolarization can bias motor output to left or right sides, determining whether the fish performs a C-start or an S-start behavior.