Article

Motor Control in a Drosophila Taste Circuit

Department of Molecular and Cell Biology and Helen Wills Neuroscience Institute, 291 Life Sciences Addition, University of California, Berkeley, Berkeley, CA 94720, USA.
Neuron (Impact Factor: 15.05). 03/2009; 61(3):373-84. DOI: 10.1016/j.neuron.2008.12.033
Source: PubMed

ABSTRACT

Tastes elicit innate behaviors critical for directing animals to ingest nutritious substances and reject toxic compounds, but the neural basis of these behaviors is not understood. Here, we use a neural silencing screen to identify neurons required for a simple Drosophila taste behavior and characterize a neural population that controls a specific subprogram of this behavior. By silencing and activating subsets of the defined cell population, we identify the neurons involved in the taste behavior as a pair of motor neurons located in the subesophageal ganglion (SOG). The motor neurons are activated by sugar stimulation of gustatory neurons and inhibited by bitter compounds; however, experiments utilizing split-GFP detect no direct connections between the motor neurons and primary sensory neurons, indicating that further study will be necessary to elucidate the circuitry bridging these populations. Combined, these results provide a general strategy and a valuable starting point for future taste circuit analysis.

Full-text preview

Available from: ncbi.nlm.nih.gov
  • Source
    • "As expected from the intermingling of the four subtypes, T5 dendrites imaged using the T4/T5 driver line responded specifically to OFF edges but responded strongly to motion in all directions (Figures 1C and 1F). Since we did not have a driver line that expressed in only one T5 subtype, we adapted a stochastic labeling approach to isolate the responses of single dendrites (Gordon and Scott, 2009; Gruntman and Turner, 2013). We used a Flippase-based mosaic method to label a subset of T4 and T5 neurons (Figures 1D and S1E). "
    [Show abstract] [Hide abstract]
    ABSTRACT: Detecting the orientation and movement of edges in a scene is critical to visually guided behaviors of many animals. What are the circuit algorithms that allow the brain to extract such behaviorally vital visual cues? Using in vivo two-photon calcium imaging in Drosophila, we describe direction selective signals in the dendrites of T4 and T5 neurons, detectors of local motion. We demonstrate that this circuit performs selective amplification of local light inputs, an observation that constrains motion detection models and confirms a core prediction of the Hassenstein-Reichardt correlator (HRC). These neurons are also orientation selective, responding strongly to static features that are orthogonal to their preferred axis of motion, a tuning property not predicted by the HRC. This coincident extraction of orientation and direction sharpens directional tuning through surround inhibition and reveals a striking parallel between visual processing in flies and vertebrate cortex, suggesting a universal strategy for motion processing.
    Full-text · Article · Oct 2015 · Neuron
  • Source
    • "To identify brain regions required for energy balance in Drosophila larvae, we used a collection of 650 neuronal enhancer-trap GAL4 lines (generous gift of Ulrike Heberlein; see (Gordon and Scott, 2009)) to overexpress a dominant-negative allele of shibire (shi DN ) (Moline et al., 1999), the Drosophila ortholog of dynamin, which prevents synaptic transmission. We screened these lines using a sensitive and robust density-based assay for larval body fat (Reis et al., 2010), and isolated 63 lines with a " floating " phenotype in combination with UAS-shi DN (Table 1 ), suggestive of a requirement for those neurons in body fat regulation. "
    [Show abstract] [Hide abstract]
    ABSTRACT: The brain plays a critical yet incompletely understood role in regulating organismal fat. We performed a neuronal silencing screen in Drosophila larvae to identify brain regions required to maintain proper levels of organismal fat. When used to modulate synaptic activity in specific brain regions, the enhancer-trap driver line E347 elevated fat upon neuronal silencing, and decreased fat upon neuronal activation. Unbiased sequencing revealed that Arc1 mRNA levels increase upon E347 activation. We had previously identified Arc1 mutations in a high-fat screen. Here we reveal metabolic changes in Arc1 mutants consistent with a high-fat phenotype and an overall shift toward energy storage. We find that Arc1-expressing cells neighbor E347 neurons, and manipulating E347 synaptic activity alters Arc1 expression patterns. Elevating Arc1 expression in these cells decreased fat, a phenocopy of E347 activation. Finally, loss of Arc1 prevented the lean phenotype caused by E347 activation, suggesting that Arc1 activity is required for E347 control of body fat. Importantly, neither E347 nor Arc1 manipulation altered energy-related behaviors. Our results support a model wherein E347 neurons induce Arc1 in specific neighboring cells to prevent excess fat accumulation. Copyright © 2015. Published by Elsevier Inc.
    Full-text · Article · Jul 2015 · Developmental Biology
  • Source
    • "Fly strains were maintained on standard Drosophila medium at 19 – 25 ° C. The following transgenic lines were used in this study: (1) Gr5a-LexA::VP16 (Gordon & Scott, 2009), (2) NP763-GAL4 (Yoshihara & Ito, 2000; Hayashi et al., 2002), (3) R12C04-GAL4 (Jenett et al., 2012), (4) R20G06-GAL4 (Jenett et al., 2012), (5) R77C10-GAL4 (Jenett et al., 2012), (6) R73G10-GAL4 (Jenett et al., 2012), (7) UAS-DsRed S197Y (Verkhusha et al., 2001), (8) lexAop-spGFP11:: "
    [Show abstract] [Hide abstract]
    ABSTRACT: Although the gustatory system provides animals with sensory cues important for food choice and other critical behaviors, little is known about neural circuitry immediately following gustatory sensory neurons (GSNs). Here, we identify and characterize a bilateral pair of gustatory second-order neurons in Drosophila. Previous studies identified GSNs that relay taste information to distinct subregions of the primary gustatory center (PGC) in the gnathal ganglia (GNG). To identify candidate gustatory second-order neurons (G2Ns) we screened ∼5,000 GAL4 driver strains for lines that label neural fibers innervating the PGC. We then combined GRASP (GFP reconstitution across synaptic partners) with presynaptic labeling to visualize potential synaptic contacts between the dendrites of the candidate G2Ns and the axonal terminals of Gr5a-expressing GSNs, which are known to respond to sucrose. Results of the GRASP analysis, followed by a single cell analysis by FLPout recombination, revealed a pair of neurons that contact Gr5a axon terminals in both brain hemispheres, and send axonal arborizations to a distinct region outside the PGC but within the GNG. To characterize the input and output branches, respectively, we expressed fluorescence-tagged acetylcholine receptor subunit (Dα7) and active-zone marker (Brp) in the G2Ns. We found that G2N input sites overlaid GRASP-labeled synaptic contacts to Gr5a neurons, while presynaptic sites were broadly distributed throughout the neurons' arborizations. GRASP analysis and further tests with the Syb-GRASP method suggested that the identified G2Ns receive synaptic inputs from Gr5a-expressing GSNs, but not Gr66a-expressing GSNs, which respond to caffeine. The identified G2Ns relay information from Gr5a-expressing GSNs to distinct regions in the GNG, and are distinct from other, recently identified gustatory projection neurons, which relay information about sugars to a brain region called the antennal mechanosensory and motor center (AMMC). Our findings suggest unexpected complexity for taste information processing in the first relay of the gustatory system.
    Full-text · Article · May 2015 · Journal of neurogenetics
Show more