Abstract
Command-like descending neurons can induce many behaviors, such as backward locomotion, escape, feeding, courtship, egg-laying, or grooming (we define 'command-like neuron' as a neuron whose activation elicits or 'commands' a specific behavior). In most animals, it remains unknown how neural circuits switch between antagonistic behaviors: via top-down activation/inhibition of antagonistic circuits or via reciprocal inhibition between antagonistic circuits. Here, we use genetic screens, intersectional genetics, circuit reconstruction by electron microscopy, and functional optogenetics to identify a bilateral pair of Drosophila larval 'mooncrawler descending neurons' (MDNs) with command-like ability to coordinately induce backward locomotion and block forward locomotion; the former by stimulating a backward-active premotor neuron, and the latter by disynaptic inhibition of a forward-specific premotor neuron. In contrast, direct monosynaptic reciprocal inhibition between forward and backward circuits was not observed. Thus, MDNs coordinate a transition between antagonistic larval locomotor behaviors. Interestingly, larval MDNs persist into adulthood, where they can trigger backward walking. Thus, MDNs induce backward locomotion in both limbless and limbed animals.
Highlights
Animals typically execute one behavior to the exclusion of all other possible behaviors (Briggman and Kristan, 2008)
Identification of brain neurons sufficient and necessary for larval backward locomotion We previously showed that activating neurons labeled by the Janelia R53F07-Gal4 line could induce backward larval locomotion, but this line has broad expression in the brain, subesophageal zone (SEZ), and both motor neurons and interneurons of the ventral nerve cord (VNC) (Clark et al, 2016)
We identified three lines called Split1, Split2, and Split3 labeling different subsets of the original pattern; the only neurons present in all three Split lines are a bilateral pair of neurons with cell bodies located in the ventral, anterior, medial brain with descending processes to A3-A5 in the VNC (Figure 1A–C, arrowheads)
Summary
Animals typically execute one behavior to the exclusion of all other possible behaviors (Briggman and Kristan, 2008). Leeches can either crawl or swim, but cannot do both simultaneously (Briggman and Kristan, 2006; Kristan, 2008); or using the same set of muscles, a locust is capable of either walking or flying but cannot execute both behaviors at the same time (Ramirez and Pearson, 1988) Such mutually exclusive choice of behavior has been observed in several other systems, including Caenorhabditis elegans (forward vs backward crawling), Tritonia (crawling vs swimming), leech (feeding vs swimming), tadpole (struggling vs swimming), turtle (swimming vs scratching), and zebrafish (left vs right escape) (Berkowitz, 2002; Gaudry and Kristan, 2010; Koyama et al, 2016; Popescu and Frost, 2002; Roberts et al, 2016; Soffe, 1993).
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