A neurodevelopmental origin of behavioral individuality (original) (raw)
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A neurodevelopmental origin of behavioral individuality in the Drosophila visual system
Science, 2020
The genome versus experience, or "Nature versus Nurture", debate has dominated our understanding of individual behavioral variation. A third factor, namely variation in complex behavior potentially due to non-heritable "developmental noise" in brain development, has been largely ignored. Using the Drosophila vinegar fly we demonstrate a causal link between variation in brain wiring due to developmental noise, and behavioral individuality. A population of visual system neurons called DCNs shows non-heritable, inter-individual variation in right/left wiring asymmetry, and control object orientation in freely walking flies. We show that DCN wiring asymmetry predicts an individual's object responses: the greater the asymmetry, the better the individual orients. Silencing DCNs abolishes correlations between anatomy and behavior, while inducing visual asymmetry via monocular deprivation "rescues" object orientation in DCN-symmetric individuals.
Innate visual preferences and behavioral flexibility in Drosophila
The Journal of Experimental Biology, 2018
Visual decision-making in animals is influenced by innate preferences as well as experience. Interaction between hard-wired responses and changing motivational states determines whether a visual stimulus is attractive, aversive, or neutral. It is however difficult to separate the relative contribution of nature versus nurture in experimental paradigms, especially for more complex visual parameters such as the shape of objects. We used a closed-loop virtual reality paradigm for walking Drosophila flies to uncover innate visual preferences for the shape and size of objects, in a recursive choice scenario allowing the flies to reveal their visual preferences over time. We found that Drosophila flies display a robust attraction / repulsion profile for a range of objects sizes in this paradigm, and that this visual preference profile remains evident under a variety of conditions and persists into old age. We also demonstrate a level of flexibility in this behavior: innate repulsion to ce...
Making scents of behavioural genetics: lessons from Drosophila
Genetics Research, 2010
SummaryThe expression of behaviours is influenced by many segregating genes. Behaviours are, therefore, complex traits. They have, however, unique characteristics that set them apart from physiological and morphological quantitative traits. First, behaviours are the ultimate expression of the nervous system. This means that understanding the genetic underpinnings of behaviours requires a neurobiological context, i.e. an understanding of the genes–brain–behaviour axis. In other words, how do ensembles of genes empower specific neural circuits to drive behaviours? Second, behaviours represent the interface between an organism and its environment. Thus, environmental effects are likely to make substantial contributions to determining behavioural outputs and genotype-by-environment interactions are expected to be prominent. It is important to differentiate between genes that contribute to the manifestation of the behavioural phenotype and genes that contribute to phenotypic variation in...
The neurogenetics of group behavior in Drosophila melanogaster
The Journal of experimental biology, 2017
Organisms rarely act in isolation. Their decisions and movements are often heavily influenced by direct and indirect interactions with conspecifics. For example, we each represent a single node within a social network of family and friends, and an even larger network of strangers. This group membership can affect our opinions and actions. Similarly, when in a crowd, we often coordinate our movements with others like fish in a school, or birds in a flock. Contributions of the group to individual behaviors are observed across a wide variety of taxa but their biological mechanisms remain largely unknown. With the advent of powerful computational tools as well as the unparalleled genetic accessibility and surprisingly rich social life of Drosophila melanogaster, researchers now have a unique opportunity to investigate molecular and neuronal determinants of group behavior. Conserved mechanisms and/or selective pressures in D. melanogaster can likely inform a much wider phylogenetic scale...
Brain and behavioral lateralization in invertebrates
Frontiers in Psychology, 2013
Traditionally, only humans were thought to exhibit brain and behavioral asymmetries, but several studies have revealed that most vertebrates are also lateralized. Recently, evidence of left-right asymmetries in invertebrates has begun to emerge, suggesting that lateralization of the nervous system may be a feature of simpler brains as well as more complex ones. Here I present some examples in invertebrates of sensory and motor asymmetries, as well as asymmetries in the nervous system. I illustrate two cases where an asymmetric brain is crucial for the development of some cognitive abilities. The first case is the nematode Caenorhabditis elegans, which has asymmetric odor sensory neurons and taste perception neurons. In this worm left/right asymmetries are responsible for the sensing of a substantial number of salt ions, and lateralized responses to salt allow the worm to discriminate between distinct salt ions. The second case is the fruit fly Drosophila melanogaster, where the presence of asymmetry in a particular structure of the brain is important in the formation or retrieval of long-term memory. Moreover, I distinguish two distinct patterns of lateralization that occur in both vertebrates and invertebrates: individuallevel and population-level lateralization. Theoretical models on the evolution of lateralization suggest that the alignment of lateralization at the population level may have evolved as an evolutionary stable strategy in which individually asymmetrical organisms must coordinate their behavior with that of other asymmetrical organisms. This implies that lateralization at the population-level is more likely to have evolved in social rather than in solitary species. I evaluate this new hypothesis with a specific focus on insects showing different level of sociality. In particular, I present a series of studies on antennal asymmetries in honeybees and other related species of bees, showing how insects may be extremely useful to test the evolutionary hypothesis.
PLoS computational biology, 2017
All organisms wishing to survive and reproduce must be able to respond adaptively to a complex, changing world. Yet the computational power available is constrained by biology and evolution, favouring mechanisms that are parsimonious yet robust. Here we investigate the information carried in small populations of visually responsive neurons in Drosophila melanogaster. These so-called 'ring neurons', projecting to the ellipsoid body of the central complex, are reported to be necessary for complex visual tasks such as pattern recognition and visual navigation. Recently the receptive fields of these neurons have been mapped, allowing us to investigate how well they can support such behaviours. For instance, in a simulation of classic pattern discrimination experiments, we show that the pattern of output from the ring neurons matches observed fly behaviour. However, performance of the neurons (as with flies) is not perfect and can be easily improved with the addition of extra neu...
Visually guided orientation in flies : case studies in computational neuroethology
2006
To understand the functioning of nervous systems and, in particular, how they control behaviour we must bridge many levels of complexity from molecules, cells and synapses to perception behaviour. Although experimental analysis is a precondition for understanding by nervous systems, it is in no way sufficient. The understanding is aided at all levels of complexity by modelling. Modelling proved to be an inevitable tool to test the experimentally established hypotheses. In this review it will by exemplified by three case studies that the appropriate level of modelling needs to be adjusted to the particular computational problems that are to be solved. (1) Specific features of the highly virtuosic pursuit behaviour of male flies can be understood on the basis of a phenomenological model that relates the visual input to the motor output. The processing of retinal image motion as is experienced by freely moving animals can be understood on the basis of a model consisting of algorithmic components and components which represent a simple equivalent circuit of nerve cells. Behaviourally relevant features of the reliability of encoding of visual motion information can be understood by modelling the transformation of postsynaptic potentials into sequences of spike trains.
on Complex Behaviors and Brain Structure
2000
Understanding how genotypic variation influences variation in brain structures and behavioral phenotypes represents a central challenge in behavioral genetics. In Drosophila melanogaster, the neuralized (neur) gene plays a key role in development of the nervous system. Different Pelement insertional mutations of neur allow the development of viable and fertile adults with profoundly altered behavioral phenotypes that depend on the exact location of the inserted Pelement. The neur mutants exhibit reduced responsiveness to noxious olfactory and mechanosensory stimulation and increased aggression when limited food is presented after a period of food deprivation. These behavioral phenotypes are correlated with distinct structural changes in integrative centers in the brain, the mushroom bodies and ellipsoid body of the central complex. Transcriptional profiling of neur mutants revealed considerable overlap among ensembles of co-regulated genes in the different mutants, but also distinct allele-specific differences. The diverse phenotypic effects arising from nearby P-element insertions in neur provide a new appreciation of the concept of allelic effects on phenotype, in which the wild type and null mutant are at the extreme ends of a continuum of pleiotropic allelic effects. neurotrypsin ortholog, regulates long-term memory formation in Drosophila.
Heritability of Directional Asymmetry in Drosophila melanogaster
International Journal of Evolutionary Biology, 2009
Directional asymmetry (DA), the consistent difference between a pair of morphological structures in which the same side is always larger than the other, presents an evolutionary mystery. Although many paired traits show DA, genetic variation for DA has not been unambiguously demonstrated. Artificial selection is a powerful technique for uncovering selectable genetic variation; we review and critique the limited number of previous studies that have been performed to select on DA and present the results of a novel artificial selection experiment on the DA of posterior crossvein location in Drosophila wings. Fifteen generations of selection in two genetically distinct lines were performed and none of the lines showed a significant response to selection. Our results therefore support and reconfirm previous findings; despite apparent natural variation and evolution of DA in nature, DA remains a paradoxical trait that does not respond to artificial selection.