Neuromodulatory selection of motor neuron recruitment patterns in a visuomotor behavior increases speed

Abstract

Animals generate locomotion at different speeds to suit their behavioral needs. Spinal circuits generate locomotion at these varying speeds by sequential activation of different spinal interneurons and motor neurons. Larval zebrafish can generate slow swims for prey capture and exploration by activation of secondary motor neurons and much faster and vigorous swims during escapes and struggles via the additional activation of primary motor neurons. Neuromodulators are known to alter motor output of spinal circuits yet their precise role in speed regulation is not understood well. Here, in the context of optomotor response (OMR), an innate, evoked locomotor behavior, we show that dopamine (DA) provides an additional layer to regulation of swim speed in larval zebrafish. Activation of D1-like receptors increases swim speed during OMR in free-swimming larvae. By analysing tail bend kinematics in head-restrained larvae, we show that the increase in speed is actuated by larger tail bends. Whole cell patch clamp recordings from motor neurons reveal that during OMR, typically only secondary motor neurons are active while primary motor neurons are quiescent. Activation of D1-like receptors increases motor drive from secondary motor neurons by decreasing spike threshold and latency. In addition, D1-like receptor activation enhances excitability and recruits quiescent primary motor neurons. Our findings provide an example of neuromodulatory reconfiguration of spinal motor neuron speed modules such that members are selectively recruited and motor drive is increased to effect changes in locomotor speed.\n\nHighlightsO_LIZebrafish larvae generate swims of increased speed during optomotor response when D1-like receptors are activated.\nC_LIO_LID1-like receptor activation increases the extent of tail bending during forward swims and turns resulting in increased swim speed.\nC_LIO_LINeuromodulation via D1-like receptors increases motor drive by enhancing excitability of slow motor neurons. In addition, D1-like receptor activation recruits quiescent fast motor neurons to increase swim speed.\nC_LIO_LIThis demonstrates neuromodulatory selection of motor neurons belonging to different speed modules to alter swimming behavior.\nC_LI\n\nGraphical abstract\n\nO_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=180 SRC=\"FIGDIR/small/683649v2_ufig1.gif\" ALT=\"Figure 1\">\nView larger version (34K):\norg.highwire.dtl.DTLVardef@17e90c4org.highwire.dtl.DTLVardef@524e45org.highwire.dtl.DTLVardef@190b1ecorg.highwire.dtl.DTLVardef@913733_HPS_FORMAT_FIGEXP M_FIG C_FIG