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5 Publications

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    08/08/13 | A directional tuning map of Drosophila elementary motion detectors.
    Maisak MS, Haag J, Ammer G, Serbe E, Meier M, Leonhardt A, Schilling T, Bahl A, Rubin GM, Nern A, Dickson BJ, Reiff DF, Hopp E, Borst A
    Nature. 2013 Aug 8;500(7461):212-6. doi: 10.1038/nature12320

    The extraction of directional motion information from changing retinal images is one of the earliest and most important processing steps in any visual system. In the fly optic lobe, two parallel processing streams have been anatomically described, leading from two first-order interneurons, L1 and L2, via T4 and T5 cells onto large, wide-field motion-sensitive interneurons of the lobula plate. Therefore, T4 and T5 cells are thought to have a pivotal role in motion processing; however, owing to their small size, it is difficult to obtain electrical recordings of T4 and T5 cells, leaving their visual response properties largely unknown. We circumvent this problem by means of optical recording from these cells in Drosophila, using the genetically encoded calcium indicator GCaMP5 (ref. 2). Here we find that specific subpopulations of T4 and T5 cells are directionally tuned to one of the four cardinal directions; that is, front-to-back, back-to-front, upwards and downwards. Depending on their preferred direction, T4 and T5 cells terminate in specific sublayers of the lobula plate. T4 and T5 functionally segregate with respect to contrast polarity: whereas T4 cells selectively respond to moving brightness increments (ON edges), T5 cells only respond to moving brightness decrements (OFF edges). When the output from T4 or T5 cells is blocked, the responses of postsynaptic lobula plate neurons to moving ON (T4 block) or OFF edges (T5 block) are selectively compromised. The same effects are seen in turning responses of tethered walking flies. Thus, starting with L1 and L2, the visual input is split into separate ON and OFF pathways, and motion along all four cardinal directions is computed separately within each pathway. The output of these eight different motion detectors is then sorted such that ON (T4) and OFF (T5) motion detectors with the same directional tuning converge in the same layer of the lobula plate, jointly providing the input to downstream circuits and motion-driven behaviours.

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    08/07/13 | A visual motion detection circuit suggested by Drosophila connectomics.
    Takemura S, Bharioke A, Lu Z, Nern A, Vitaladevuni S, Rivlin PK, Katz WT, Olbris DJ, Plaza SM, Winston P, Zhao T, Horne JA, Fetter RD, Takemura S, Blazek K, Chang L, Ogundeyi O, Saunders MA, Shapiro V, Sigmund C, Rubin GM, Scheffer LK, Meinertzhagen IA, Chklovskii DB
    Nature. 2013 Aug 7;500(7461):175–81. doi: doi:10.1038/nature12450

    Animal behaviour arises from computations in neuronal circuits, but our understanding of these computations has been frustrated by the lack of detailed synaptic connection maps, or connectomes. For example, despite intensive investigations over half a century, the neuronal implementation of local motion detection in the insect visual system remains elusive. Here we develop a semi-automated pipeline using electron microscopy to reconstruct a connectome, containing 379 neurons and 8,637 chemical synaptic contacts, within the Drosophila optic medulla. By matching reconstructed neurons to examples from light microscopy, we assigned neurons to cell types and assembled a connectome of the repeating module of the medulla. Within this module, we identified cell types constituting a motion detection circuit, and showed that the connections onto individual motion-sensitive neurons in this circuit were consistent with their direction selectivity. Our results identify cellular targets for future functional investigations, and demonstrate that connectomes can provide key insights into neuronal computations.

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    07/10/13 | Contributions of the 12 neuron classes in the fly lamina to motion vision.
    Tuthill JC, Nern A, Stephen L. Holtz , Rubin GM, Reiser MB
    Neuron. 07/2013;79:128-140. doi: http://dx.doi.org/10.1016/j.neuron.2013.05.024

    Motion detection is a fundamental neural computation performed by many sensory systems. In the fly, local motion computation is thought to occur within the first two layers of the visual system, the lamina and medulla. We constructed specific genetic driver lines for each of the 12 neuron classes in the lamina. We then depolarized and hyperpolarized each neuron type and quantified fly behavioral responses to a diverse set of motion stimuli. We found that only a small number of lamina output neurons are essential for motion detection, while most neurons serve to sculpt and enhance these feedforward pathways. Two classes of feedback neurons (C2 and C3), and lamina output neurons (L2 and L4), are required for normal detection of directional motion stimuli. Our results reveal a prominent role for feedback and lateral interactions in motion processing and demonstrate that motion-dependent behaviors rely on contributions from nearly all lamina neuron classes.

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    06/08/13 | Essential role of the mushroom body in context-dependent CO2 avoidance in Drosophila.
    Bräcker LB, Siju KP, Varela N, Aso Y, Zhang M, Hein I, Vasconcelos ML, Grunwald Kadow IC
    Current Biology. 2013 Jul 8;23(13):1228-34. doi: 10.1016/j.cub.2013.05.029

    Internal state as well as environmental conditions influence choice behavior. The neural circuits underpinning state-dependent behavior remain largely unknown. Carbon dioxide (CO2) is an important olfactory cue for many insects, including mosquitoes, flies, moths, and honeybees [1]. Concentrations of CO2 higher than 0.02% above atmospheric level trigger a strong innate avoidance in the fly Drosophila melanogaster [2, 3]. Here, we show that the mushroom body (MB), a brain center essential for olfactory associative memories [4-6] but thought to be dispensable for innate odor processing [7], is essential for CO2 avoidance behavior only in the context of starvation or in the context of a food-related odor. Consistent with this, CO2 stimulation elicits Ca(2+) influx into the MB intrinsic cells (Kenyon cells: KCs) in vivo. We identify an atypical projection neuron (bilateral ventral projection neuron, biVPN) that connects CO2 sensory input bilaterally to the MB calyx. Blocking synaptic output of the biVPN completely abolishes CO2 avoidance in food-deprived flies, but not in fed flies. These findings show that two alternative neural pathways control innate choice behavior, and they are dependent on the animal’s internal state. In addition, they suggest that, during innate choice behavior, the MB serves as an integration site for internal state and olfactory input.

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    01/23/13 | Multiple interactions control synaptic layer specificity in the Drosophila visual system.
    Pecot MY, Tadros W, Nern A, Bader M, Chen Y, Zipursky SL
    Neuron. 2013 Jan 23;77(2):299-310. doi: 10.1016/j.neuron.2012.11.007

    How neurons form synapses within specific layers remains poorly understood. In the Drosophila medulla, neurons target to discrete layers in a precise fashion. Here we demonstrate that the targeting of L3 neurons to a specific layer occurs in two steps. Initially, L3 growth cones project to a common domain in the outer medulla, overlapping with the growth cones of other neurons destined for a different layer through the redundant functions of N-Cadherin (CadN) and Semaphorin-1a (Sema-1a). CadN mediates adhesion within the domain and Sema-1a mediates repulsion through Plexin A (PlexA) expressed in an adjacent region. Subsequently, L3 growth cones segregate from the domain into their target layer in part through Sema-1a/PlexA-dependent remodeling. Together, our results and recent studies argue that the early medulla is organized into common domains, comprising processes bound for different layers, and that discrete layers later emerge through successive interactions between processes within domains and developing layers.

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