A higher control center of locomotor behavior in the Drosophila brain

TLDR

The study investigates how mutations affecting the central complex influence walking behavior in 15 Drosophila mutant strains. Walking activity, speed, and straightness were quantified in object fixation, phototaxis, and negative geotaxis assays, and detailed deficits were analyzed with mosaic analysis and high‑speed cinematography. All mutants showed walking impairments that correlate with the severity of central complex structural defects, indicating a specific role for the CC in walking speed, step size, turning, and start/stop maneuvers rather than in basic stepping rhythm.

Abstract

In order to elucidate the behavioral significance of the central complex (CC), we have examined walking in 15 Drosophila mutant strains belonging to eight independent X-linked genes that affect the structure of the CC. Compared to four different wild-type strains, all are impaired either in a general or in a paradigm-dependent manner. Behavioral deficits concern walking activity, walking speed, or "straightness of walking" as measured in an object fixation task, in fast phototaxis, and in negative geotaxis. Behavioral deficits of three strains with mutations in different genes were studied in detail using mosaic analysis and high-speed cinematography. In all cases the focus for declining walking activity is located in the brain and is fully correlated with the respective defect of the CC. A high correlation between the degree of the behavioral impairment and the severity of the structural defect in two strains further adds to the evidence. Declining walking activity is not an unspecific side effect of structural brain defects, as steady walking is observed in structural mutants of the visual system and mushroom bodies. In mutant flies no-bridgeKS49 (nob), step size as a function of the stepping period is reduced. The focus of the resulting reduced average and maximum walking speeds resides in the brain and, again, the behavioral impairment fully correlates with the structural defects of the CC. While no indication is found for a role of the CC in setting up the basic stepping rhythm in straight walking (a respective phenotype in mutant central-complexKS181 flies resides in the ventral ganglion), a role in turning and start/stop maneuvers is suggested by aberrations in the stepping pattern of nob flies during such episodes.