Neuronal control of locomotor handedness in Drosophila

Abstract

Genetically identical individuals display variability in their physiology, morphology, and behaviors, even when reared in essentially identical environments, but there is little mechanistic understanding of the basis of such variation. Here, we investigated whether Drosophila melanogaster displays individual-toindividual variation in locomotor behaviors. We developed a new high-throughout platform capable of measuring the exploratory behavior of hundreds of individual flies simultaneously. With this approach, we find that, during exploratory walking, individual flies exhibit significant bias in their left vs. right locomotor choices, with some flies being strongly left biased or right biased. This idiosyncrasy was present in all genotypes examined, including wild-derived populations and inbred isogenic laboratory strains. The biases of individual flies persist for their lifetime and are nonheritable: i.e., mating two left-biased individuals does not yield left-biased progeny. This locomotor handedness is uncorrelated with other asymmetries, such as the handedness of gut twisting, leg-length asymmetry, and wing-folding preference. Using transgenics and mutants, we find that the magnitude of locomotor handedness is under the control of columnar neurons within the central complex, a brain region implicated in motor planning and execution. When these neurons are silenced, exploratory laterality increases, with more extreme leftiness and rightiness. This observation intriguingly implies that the brain may be able to dynamically regulate behavioral individuality.behavior | individuality | personality | circuit mapping | central complex H and dominance-better performance using either the left or right hand-is a familiar human trait, moderately heritable (1), and regulated by many genes (2), including those involved in general body symmetry (3). However, behavioral handedness in general, i.e., the preferential performance of a behavior on one side of the body or with a particular chiral twist, is a multifaceted phenomenon. For example, in the absence of visual feedback, people display clockwise or counterclockwise biases in their walking behavior (4). This "locomotor handedness" is uncorrelated to hand dominance or gross morphological asymmetry and instead may be due to asymmetries in the collection and processing of sensory information, resulting in individual locomotor biases with a neurological basis (4, 5).Handed behavioral tendencies specific to individuals are also prevalent throughout the animal kingdom and have been shown in species as disparate as mice (paw use) (6), octopi (eye use) (7), and tortoises (side rolled on during righting) (8). There is also evidence that, at the population mean level, some species of insects have handed behaviors and asymmetric neurophysiological patterns (9). However, there has been little investigation of the differences in handed behaviors among individuals of the same insect species, and the mechanisms by which asymmetries are instilled in behavior are unknown. Considering beha...

Systematic exploration of unsupervised methods for mapping behavior

“…The pairwise transition rates between clusters appeared to be idiosyncratic as well. These findings are consistent with behavioral individuality in Drosophila phototaxis (Kain et al 2012), locomotor handedness (Buchanan et al 2015) and thermal preference . However, the clear evidence of individuality in PCA 20 -GMM-SW cluster abundance distributions is notable when compared to the lack of signal of such individuality in the supervised classification results of Kain et al (2013).…”

A neural circuit basis for context-modulation of individual locomotor behavior

“…Importantly, we did not find that our thermogenetic manipulations substantially reduced activity level with the exception of one (activation of P-F-Rs through SS02293-Gal4). As seen previously (Akhund-Zade et al, 2019;Ayroles et al, 2015;Buchanan et al, 2015), the mean turn bias in all experimental groups was approximately 0.5 (0.49 +/-0.011). The variability in turn bias ranged from 0.09 to 0.15 (standard deviation) across all experimental groups ( Fig S2B).…”

“…To examine how sensory context (specifically, changes in luminance) affects individual locomotor biases, we modified instruments previously used to track flies as they made left-right locomotor choices in symmetrical Y-shaped mazes (Ayroles et al, 2015;Buchanan et al, 2015). We added a dual-channel illuminator, under computer control, so that behavioral arenas could be lit with white LEDs, infrared LEDs, or both ( Fig 1A).…”

“…C.f. Buchanan et al, 2015. I2) Scatter plot of LDM (difference of light and dark turn biases) on day 2 vs day 1.…”

Internal states drive nutrient homeostasis by modulating exploration-exploitation trade-off

“…Indeed, upon AA challenges, we observed that some flies increased their total time on yeast by having many short yeast visits, while some flies had fewer but longer visits. It will be interesting to investigate if these differences reflect behavioral idiosyncrasies, as observed before in many animals including Drosophila (Buchanan and de Bivort, 2015; Dingemanse et al, 2010; Kain and de Bivort, 2012). Differentiating between these two possibilities and identifying the physiological and circuit mechanisms leading to idiosyncrasies will be key to a better understanding of behavior.…”