A neurodevelopmental origin of behavioral individuality

Linneweber, Gerit Arne; Andriatsilavo, Maheva; Dutta, Suchetana; Hellbruegge, Liz; Liu, Guangda; Ejsmont, Radoslaw K; Fenk, Lisa M.; Straw, Andrew; Wernet, Mathias F.; Hiesinger, P. Robin; Hassan, Bassem

doi:10.1101/540880

Cited by 8 publications

(12 citation statements)

References 52 publications

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“…Handed locomotor biases at the individual level have been found to be stable over time in numerous species including humans (Lebovich et al, 2019) and flies (Ayroles et al, 2015;Buchanan et al, 2015;Linneweber et al, 2019). The stability of these biases over time suggests a rigidity to individual behavioral biases.…”

Section: Discussionmentioning

confidence: 99%

“…Individual Drosophila melanogaster larvae exhibit stochastic variation in the branching pattern of 12A hemilineage interneuron projections, and this variation predicts individual differences in the timing of flight initiation (Mellert et al, 2016). In adult flies, left-right wiring asymmetry in bilaterallyprojecting visual Dorsal Cluster Neurons predicts idiosyncratic deviation from direct walking between attractive visual cues (Linneweber et al, 2019). A general approach to mapping such correlates of individual bias could be to prioritize neural bottlenecks: regions of the brain in which many inputs converge onto a relatively small number of output cells.…”

Section: Introductionmentioning

confidence: 99%

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

Skutt-Kakaria

Reimers

Currier

et al. 2019

Preprint

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Defying the cliche that biological variation arises from differences in nature or nurture, genetically identical animals reared in the same environment exhibit striking differences in their behaviors. Innate behaviors can be surprisingly flexible, for example by exhibiting context-dependence. The intersection of behavioral individuality and contextdependence is largely unexplored, particularly at the neural circuit level. Here, we show that individual flies' tendencies to turn left or right (locomotor handedness) changes when ambient illumination changes. This change is itself a stable individual behavioral characteristic. Silencing output neurons of the central complex (a premotor area that mediates goal-directed navigation) blocks this change. These neurons respond to light with idiosyncratic changes to their baseline calcium levels, and idiosyncratic morphological variation in their presynaptic arbors correlates with idiosyncratic sensory-context-specific turn biases. These findings provide a circuit mechanism by which individual locomotor biases arise and are modulated by sensory context.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

Skutt-Kakaria

Reimers

Currier

et al. 2019

Preprint

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“…Many studies have focused on characterizing the intragenotypic variability in morphological, physiological, and behavioral traits (Abley et Sørensen et al, 2015). Morphological variations present in the ventral nerve cord and optic lobes are of particular note as they respectively correlate with the timing of flight initiation and visually-guided locomotor biases, providing a link between morphological and behavioral intragenotypic variability (Linneweber et al, 2019;Mellert et al, 2016). Our research has identified intragenotypic variability in isogenic lines of D. melanogaster for turning bias, phototaxis, and thermotaxis (Ayroles et al, 2015;Kain et al, 2012;Kain et al, 2015).…”

Section: Introductionmentioning

confidence: 71%

The effect of environmental enrichment on behavioral variability depends on genotype, behavior, and type of enrichment

Akhund-Zade

O’Leary

et al. 2019

Preprint

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Non-genetic individuality in behavior, also termed intragenotypic variability, has been observed across many different organisms. A potential cause of intragenotypic variability is sensitivity to minute environmental differences during development, even as major environmental parameters are kept constant. Animal enrichment paradigms often include the addition of environmental diversity, whether in the form of social interaction, novel objects, or exploratory opportunities. Enrichment could plausibly affect intragenotypic variability in opposing ways: it could cause an increase in variability due to the increase in microenvironmental variation, or a decrease in variability due to elimination of aberrant behavior as animals are taken out of impoverished laboratory conditions. In order to test our hypothesis, we assayed five isogenic Drosophila melanogaster lines raised in control and mild enrichment conditions, and one isogenic line under both mild and intense enrichment conditions. We compared the mean and variability of six behavioral metrics between our enriched fly populations and the laboratory housing control. We found that enrichment often caused a small increase in variability across most of our behaviors, but that the ultimate effect of enrichment on both behavioral means and variabilities was highly dependent on genotype and its interaction with the particular enrichment treatment. Our results support previous work on enrichment that presents a highly variable picture of its effects on both behavior and physiology.

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“…From a perspective of biological mechanism, the correlation between these two behaviors (or other pairs we discovered) could be established during development. Individual wiring (Mellert et al, 2016;Linneweber et al, 2019) or physiological variations in neurons that mediate more than one behavior could impart coupled changes to all such behaviors.…”

Section: Discussionmentioning

confidence: 99%

The structure of behavioral variation within a genotype

Werkhoven¹,

Bravin²,

Skutt-Kakaria

et al. 2019

Preprint

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Individual animals vary in their behaviors. This is true even when they share the same genotype and were reared in the same environment. Clusters of covarying behaviors constitute behavioral syndromes, and an individual's position along such axes of covariation is a representation of their personality. Despite these conceptual frameworks, the structure of behavioral covariation within a genotype is essentially uncharacterized and its mechanistic origins unknown. Passing hundreds of isogenic Drosophila individuals through an experimental pipeline that captured hundreds of behavioral measures, we found correlations only between sparse pairs of behaviors. Thus, the space of behavioral variation has many independent dimensions. Manipulating the physiology of the brain, and specific neural populations, altered specific correlations. We also observed that variation in gene expression can predict an individual's position on some behavior axes. This work represents the first steps in understanding the biological mechanisms determining the structure of behavioral variation within a genotype.

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A neurodevelopmental origin of behavioral individuality

Abstract: 45

Cited by 8 publications

References 52 publications

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

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

The effect of environmental enrichment on behavioral variability depends on genotype, behavior, and type of enrichment

The structure of behavioral variation within a genotype

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