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Dickson Lab / Publications
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28 Publications

Showing 1-10 of 28 results
07/04/18 | Visual projection neurons mediating directed courtship in Drosophila.
Ribeiro IM, Drews M, Bahl A, Machacek C, Borst A, Dickson BJ
Cell. 2018 Jul 04;174(3):607-21. doi: 10.1016/j.cell.2018.06.020

Many animals rely on vision to detect, locate, and track moving objects. In Drosophila courtship, males primarily use visual cues to orient toward and follow females and to select the ipsilateral wing for courtship song. Here, we show that the LC10 visual projection neurons convey essential visual information during courtship. Males with LC10 neurons silenced are unable to orient toward or maintain proximity to the female and do not predominantly use the ipsilateral wing when singing. LC10 neurons preferentially respond to small moving objects using an antagonistic motion-based center-surround mechanism. Unilateral activation of LC10 neurons recapitulates the orienting and ipsilateral wing extension normally elicited by females, and the potency with which LC10 induces wing extension is enhanced in a state of courtship arousal controlled by male-specific P1 neurons. These data suggest that LC10 is a major pathway relaying visual input to the courtship circuits in the male brain.

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01/11/18 | Persistent activity in a recurrent circuit underlies courtship memory in Drosophila.
Zhao X, Lenek D, Dag U, Dickson B, Keleman K
eLife. 2018 Jan 11;7:. doi: 10.7554/eLife.31425

Recurrent connections are thought to be a common feature of the neural circuits that encode memories, but how memories are laid down in such circuits is not fully understood. Here we present evidence that courtship memory in Drosophila relies on the recurrent circuit between mushroom body gamma (MBg), M6 output, and aSP13 dopaminergic neurons. We demonstrate persistent neuronal activity of aSP13 neurons and show that it transiently potentiates synaptic transmission from MBγ>M6 neurons. M6 neurons in turn provide input to aSP13 neurons, prolonging potentiation of MBγ>M6 synapses over time periods that match short-term memory. These data support a model in which persistent aSP13 activity within a recurrent circuit lays the foundation for a short-term memory.

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03/06/17 | Moonwalker descending neurons mediate visually evoked retreat in Drosophila.
Sen R, Wu M, Branson K, Robie A, Rubin GM, Dickson BJ
Current Biology : CB. 2017 Mar 6;27(5):766-71. doi: 10.1016/j.cub.2017.02.008

Insects, like most animals, tend to steer away from imminent threats [1-7]. Drosophila melanogaster, for example, generally initiate an escape take-off in response to a looming visual stimulus, mimicking a potential predator [8]. The escape response to a visual threat is, however, flexible [9-12] and can alternatively consist of walking backward away from the perceived threat [11], which may be a more effective response to ambush predators such as nymphal praying mantids [7]. Flexibility in escape behavior may also add an element of unpredictability that makes it difficult for predators to anticipate or learn the prey's likely response [3-6]. Whereas the fly's escape jump has been well studied [8, 9, 13-18], the neuronal underpinnings of evasive walking remain largely unexplored. We previously reported the identification of a cluster of descending neurons-the moonwalker descending neurons (MDNs)-the activity of which is necessary and sufficient to trigger backward walking [19], as well as a population of visual projection neurons-the lobula columnar 16 (LC16) cells-that respond to looming visual stimuli and elicit backward walking and turning [11]. Given the similarity of their activation phenotypes, we hypothesized that LC16 neurons induce backward walking via MDNs and that turning while walking backward might reflect asymmetric activation of the left and right MDNs. Here, we present data from functional imaging, behavioral epistasis, and unilateral activation experiments that support these hypotheses. We conclude that LC16 and MDNs are critical components of the neural circuit that transduces threatening visual stimuli into directional locomotor output.

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06/16/16 | Motor control of fly feeding.
McKellar CE
Journal of Neurogenetics. 2016 Jun 16;30(2):101-11. doi: 10.1080/01677063.2016.1177047

Following considerable progress on the molecular and cellular basis of taste perception in fly sensory neurons, the time is now ripe to explore how taste information, integrated with hunger and satiety, undergo a sensorimotor transformation to lead to the motor actions of feeding behavior. I examine what is known of feeding circuitry in adult flies from more than 250 years of work in larger flies and from newer work in Drosophila. I review the anatomy of the proboscis, its muscles and their functions (where known), its motor neurons, interneurons known to receive taste inputs, interneurons that diverge from taste circuitry to provide information to other circuits, interneurons from other circuits that converge on feeding circuits, proprioceptors that influence the motor control of feeding, and sites of integration of hunger and satiety on feeding circuits. In spite of the several neuron types now known, a connected pathway from taste inputs to feeding motor outputs has yet to be found. We are on the threshold of an era where these individual components will be assembled into circuits, revealing how nervous system architecture leads to the control of behavior.

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06/01/16 | Editorial overview: Neurobiology of sex.
Dulac C, Dickson BJ
Current Opinion in Neurobiology. 2016 Jun;38:A1-3. doi: 10.1016/j.conb.2016.06.001
01/28/16 | Visualization and quantification for interactive analysis of neural connectivity in Drosophila.
Swoboda N, Moosburner J, Bruckner S, Yu J, Dickson BJ, Bühler K
Computer Graphics Forum. 2016 Jan 28:. doi: 10.1111/cgf.12792

Neurobiologists investigate the brain of the common fruit fly Drosophila melanogaster to discover neural circuits and link them to complex behaviour. Formulating new hypotheses about connectivity requires potential connectivity information between individual neurons, indicated by overlaps of arborizations of two or more neurons. As the number of higher order overlaps (i.e. overlaps of three or more arborizations) increases exponentially with the number of neurons under investigation, visualization is impeded by clutter and quantification becomes a burden. Existing solutions are restricted to visual or quantitative analysis of pairwise overlaps, as they rely on precomputed overlap data. We present a novel tool that complements existing methods for potential connectivity exploration by providing for the first time the possibility to compute and visualize higher order arborization overlaps on the fly and to interactively explore this information in both its spatial anatomical context and on a quantitative level. Qualitative evaluation by neuroscientists and non-experts demonstrated the utility and usability of the tool.

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01/07/16 | Adaptive and background-aware GAL4 expression enhancement of co-registered confocal microscopy images.
Trapp M, Schulze F, Novikov AA, Tirian L, J Dickson B, Bühler K
Neuroinformatics. 2016 Jan 7;14(2):221-33. doi: 10.1007/s12021-015-9289-y

GAL4 gene expression imaging using confocal microscopy is a common and powerful technique used to study the nervous system of a model organism such as Drosophila melanogaster. Recent research projects focused on high throughput screenings of thousands of different driver lines, resulting in large image databases. The amount of data generated makes manual assessment tedious or even impossible. The first and most important step in any automatic image processing and data extraction pipeline is to enhance areas with relevant signal. However, data acquired via high throughput imaging tends to be less then ideal for this task, often showing high amounts of background signal. Furthermore, neuronal structures and in particular thin and elongated projections with a weak staining signal are easily lost. In this paper we present a method for enhancing the relevant signal by utilizing a Hessian-based filter to augment thin and weak tube-like structures in the image. To get optimal results, we present a novel adaptive background-aware enhancement filter parametrized with the local background intensity, which is estimated based on a common background model. We also integrate recent research on adaptive image enhancement into our approach, allowing us to propose an effective solution for known problems present in confocal microscopy images. We provide an evaluation based on annotated image data and compare our results against current state-of-the-art algorithms. The results show that our algorithm clearly outperforms the existing solutions.

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09/09/15 | Connecting neural codes with behavior in the auditory system of Drosophila.
Clemens J, Girardin CC, Coen P, Guan X, Dickson BJ, Murthy M
Neuron. 2015 Sep 9;87(6):1332-43. doi: 10.1016/j.neuron.2015.08.014

Brains are optimized for processing ethologically relevant sensory signals. However, few studies have characterized the neural coding mechanisms that underlie the transformation from natural sensory information to behavior. Here, we focus on acoustic communication in Drosophila melanogaster and use computational modeling to link natural courtship song, neuronal codes, and female behavioral responses to song. We show that melanogaster females are sensitive to long timescale song structure (on the order of tens of seconds). From intracellular recordings, we generate models that recapitulate neural responses to acoustic stimuli. We link these neural codes with female behavior by generating model neural responses to natural courtship song. Using a simple decoder, we predict female behavioral responses to the same song stimuli with high accuracy. Our modeling approach reveals how long timescale song features are represented by the Drosophila brain and how neural representations can be decoded to generate behavioral selectivity for acoustic communication signals.

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02/02/15 | Neuronal control of Drosophila walking direction.
Bidaye SS, Machacek C, Wu Y, Dickson BJ
Science. 2014 Apr 4;344(6179):97-101. doi: 10.1126/science.1249964

Most land animals normally walk forward but switch to backward walking upon sensing an obstacle or danger in the path ahead. A change in walking direction is likely to be triggered by descending "command" neurons from the brain that act upon local motor circuits to alter the timing of leg muscle activation. Here we identify descending neurons for backward walking in Drosophila--the MDN neurons. MDN activity is required for flies to walk backward when they encounter an impassable barrier and is sufficient to trigger backward walking under conditions in which flies would otherwise walk forward. We also identify ascending neurons, MAN, that promote persistent backward walking, possibly by inhibiting forward walking. These findings provide an initial glimpse into the circuits and logic that control walking direction in Drosophila.

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07/21/14 | Abdominal-B neurons control Drosophila virgin female receptivity.
Bussell JJ, Yapici N, Zhang SX, Dickson BJ, Vosshall LB
Current Biology. 2014 Jul 21;24(14):1584-95. doi: 10.1016/j.cub.2014.06.011

BACKGROUND: Female sexual receptivity offers an excellent model for complex behavioral decisions. The female must parse her own reproductive state, the external environment, and male sensory cues to decide whether to copulate. In the fly Drosophila melanogaster, virgin female receptivity has received relatively little attention, and its neural circuitry and individual behavioral components remain unmapped. Using a genome-wide neuronal RNAi screen, we identify a subpopulation of neurons responsible for pausing, a novel behavioral aspect of virgin female receptivity characterized in this study.

RESULTS: We show that Abdominal-B (Abd-B), a homeobox transcription factor, is required in developing neurons for high levels of virgin female receptivity. Silencing adult Abd-B neurons significantly decreased receptivity. We characterize two components of receptivity that are elicited in sexually mature females by male courtship: pausing and vaginal plate opening. Silencing Abd-B neurons decreased pausing but did not affect vaginal plate opening, demonstrating that these two components of female sexual behavior are functionally separable. Synthetic activation of Abd-B neurons increased pausing, but male courtship song alone was not sufficient to elicit this behavior.

CONCLUSIONS: Our results provide an entry point to the neural circuit controlling virgin female receptivity. The female integrates multiple sensory cues from the male to execute discrete motor programs prior to copulation. Abd-B neurons control pausing, a key aspect of female sexual receptivity, in response to male courtship.

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