Diversity and wiring variability of olfactory local interneurons in the Drosophila antennal lobe

Drosophila typically move toward light (phototax positively) when startled. The various species of Drosophila exhibit some variation in their respective mean phototactic behaviors; however, it is not clear to what extent genetically identical individuals within each species behave idiosyncratically. Such behavioral individuality has indeed been observed in laboratory arthropods; however, the neurobiological factors underlying individual-to-individual behavioral differences are unknown. We developed "FlyVac," a high-throughput device for automatically assessing phototaxis in single animals in parallel. We observed surprising variability within every species and strain tested, including identically reared, isogenic strains. In an extreme example, a domesticated strain of Drosophila simulans harbored both strongly photopositive and strongly photonegative individuals. The particular behavior of an individual fly is not heritable and, because it persists for its lifetime, constitutes a model system for elucidating the molecular mechanisms of personality. Although all strains assayed had greater than expected variation (assuming binomial sampling), some had more than others, implying a genetic basis. Using genetics and pharmacology, we identified the metabolite transporter White and white-dependent serotonin as suppressors of phototactic personality. Because we observed behavioral idiosyncrasy in all experimental groups, we suspect it is present in most behaviors of most animals.ethology | stochasticity | bet-hedging | Ischnopterapion virens F ew debates in biology have generated broader interest than nature versus nurture. Not surprisingly, both heritable and environmental factors play significant roles in shaping an organism's traits. However, the precise contributions of genetic and environmental factors to complex traits, such as most behaviors, are poorly understood. Behavioral individuality, in the absence of genetic variation, has indeed been observed in the laboratory. Specifically, clonal pea aphids were shown to vary in their predator escape behavior, and these differences were maintained for at least 5 d (1). In another example, the naïve odor preference of fruit flies was highly variable across individuals (2). These experiments suggest that even when deterministic influences from genetics and environment are held constant, there is nevertheless considerable behavioral variability. Drosophila is an ideal model system to test whether individuals, matched both genetically and environmentally, possess unique behavioral personalities, and what genetic and neurobiological factors control the magnitude of this idiosyncrasy.To determine whether individuals are behaving idiosyncratically we need to measure the trial-to-trial variation in an individual's behavior and compare that to the variation between individuals. If we observe greater variability between individuals than within individuals (that cannot be explained by sampling error), this would constitute evidence for behavioral idiosyncrasy. This analysis req...

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“…6). Such diversifying processes have been shown to act at both the level of neuronal wiring and physiology within arthropod brains (27,28).…”

Section: Discussionmentioning

confidence: 99%

Phototactic personality in fruit flies and its suppression by serotonin and white

Kain

Stokes

Bivort

2012

Proc. Natl. Acad. Sci. U.S.A.

157

205

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“…6A) (Masse et al, 2009). Recent large-scale anatomical analyses of LNs and PNs (Wong et al, 2002;Jefferis et al, 2007;Lin et al, 2007;Chou et al, 2010b;Yu et al, 2010a;Chiang et al, 2011) allowed us to examine the organization of these elements of the olfactory circuits receiving input from IR-expressing OSNs and compare this with ORdependent olfactory circuitry. A minimum of 100 ipsilaterally and 100 bilaterally projecting LNs are estimated to innervate each antennal lobe (Chou et al, 2010b).…”

Section: Anatomy Of Processing and Higherorder Representations Of Ir mentioning

confidence: 99%

“…The axons of OSNs expressing the same receptor converge onto segregated regions of neuropil called glomeruli in the olfactory bulb (or antennal lobe in insects) (Hansson et al, 1992;Mombaerts et al, 1996;Zou et al, 2009). Here, OSNs synapse with projection neurons (PNs) that transmit odor-evoked signals to higher brain regions (Mori et al, 1999;Masse et al, 2009), as well as with local interneurons (LNs) that modulate OSN input and PN output activity within and between glomeruli (Christensen et al, 1993;Wachowiak and Shipley, 2006;Chou et al, 2010b).…”

Section: Introductionmentioning

confidence: 99%

Complementary Function and Integrated Wiring of the Evolutionarily DistinctDrosophilaOlfactory Subsystems

Silbering¹,

Rytz²,

Grosjean³

et al. 2011

J. Neurosci.

464

749

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To sense myriad environmental odors, animals have evolved multiple, large families of divergent olfactory receptors. How and why distinct receptor repertoires and their associated circuits are functionally and anatomically integrated is essentially unknown. We have addressed these questions through comprehensive comparative analysis of the Drosophila olfactory subsystems that express the ionotropic receptors (IRs) and odorant receptors (ORs). We identify ligands for most IR neuron classes, revealing their specificity for select amines and acids, which complements the broader tuning of ORs for esters and alcohols. IR and OR sensory neurons exhibit glomerular convergence in segregated, although interconnected, zones of the primary olfactory center, but these circuits are extensively interdigitated in higher brain regions. Consistently, behavioral responses to odors arise from an interplay between IR-and OR-dependent pathways. We integrate knowledge on the different phylogenetic and developmental properties of these receptors and circuits to propose models for the functional contributions and evolution of these distinct olfactory subsystems.

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“…Airborne chemicals result in activation of olfactory receptor neurons, which project their axons to the antennal lobes. At this level, information is computed within the layers of local neurons (LNs) and projection neurons (PNs) and conveyed to higher olfactory centers, i.e., the lateral horn and the MBs (Fiala et al, 2002;Wang et al, 2003;Shang et al, 2007;Chou et al, 2010).…”

Section: Rugose Supports Odor Learning At the Level Of The Mbsmentioning

confidence: 99%

Drosophila rugoseIs a Functional Homolog of MammalianNeurobeachinand Affects Synaptic Architecture, Brain Morphology, and Associative Learning

Volders

Scholz²,

Slabbaert

et al. 2012

J. Neurosci.

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Neurobeachin (Nbea) is implicated in vesicle trafficking in the regulatory secretory pathway, but details on its molecular function are currently unknown. We have used Drosophila melanogaster mutants for rugose (rg), the Drosophila homolog of Nbea, to further elucidate the function of this multidomain protein. Rg is expressed in a granular pattern reminiscent of the Golgi network in neuronal cell bodies and colocalizes with transgenic Nbea, suggesting a function in secretory regulation. In contrast to Nbea Ϫ/Ϫ mice, rg null mutants are viable and fertile and exhibit aberrant associative odor learning, changes in gross brain morphology, and synaptic architecture as determined at the larval neuromuscular junction. At the same time, basal synaptic transmission is essentially unaffected, suggesting that structural and functional aspects are separable. Rg phenotypes can be rescued by a Drosophila rg؉ transgene, whereas a mouse Nbea transgene rescues aversive odor learning and synaptic architecture; it fails to rescue brain morphology and appetitive odor learning. This dissociation between the functional redundancy of either the mouse or the fly transgene suggests that their complex composition of numerous functional and highly conserved domains support independent functions. We propose that the detailed compendium of phenotypes exhibited by the Drosophila rg null mutant provided here will serve as a test bed for dissecting the different functional domains of BEACH (for beige and human Chediak-Higashi syndrome) proteins, such as Rugose, mouse Nbea, or Nbea orthologs in other species, such as human.

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Diversity and wiring variability of olfactory local interneurons in the Drosophila antennal lobe

Cited by 343 publications

References 54 publications

Phototactic personality in fruit flies and its suppression by serotonin and white

Phototactic personality in fruit flies and its suppression by serotonin and white

Complementary Function and Integrated Wiring of the Evolutionarily DistinctDrosophilaOlfactory Subsystems

Drosophila rugoseIs a Functional Homolog of MammalianNeurobeachinand Affects Synaptic Architecture, Brain Morphology, and Associative Learning

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