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1.  Multilevel control of run orientation in Drosophila larval chemotaxis 
Chemotaxis is a powerful paradigm to study how orientation behavior is driven by sensory stimulation. Drosophila larvae navigate odor gradients by controlling the duration of their runs and the direction of their turns. Straight runs and wide-amplitude turns represent two extremes of a behavioral continuum. Here we establish that, on average, runs curl toward the direction of higher odor concentrations. We find that the orientation and strength of the local odor gradient perpendicular to the direction of motion modulates the orientation of individual runs in a gradual manner. We discuss how this error-correction mechanism, called weathervaning, contributes to larval chemotaxis. We use larvae with a genetically modified olfactory system to demonstrate that unilateral function restricted to a single olfactory sensory neuron (OSN) is sufficient to direct weathervaning. Our finding that bilateral sensing is not necessary to control weathervaning highlights the role of temporal sampling. A correlational analysis between sensory inputs and behavioral outputs suggests that weathervaning results from low-amplitude head casts implemented without interruption of the run. In addition, we report the involvement of a sensorimotor memory arising from previous reorientation events. Together, our results indicate that larval chemotaxis combines concurrent orientation strategies that involve complex computations on different timescales.
doi:10.3389/fnbeh.2014.00038
PMCID: PMC3923145  PMID: 24592220
active sensing; chemotaxis; Drosophila larva; sensorimotor integration; stereo-olfaction; weathervaning
2.  Correction: Automated Tracking of Animal Posture and Movement during Exploration and Sensory Orientation Behaviors 
PLoS ONE  2012;7(10):10.1371/annotation/5bef5b0a-9b48-4e85-8df5-a46793f6c701.
doi:10.1371/annotation/5bef5b0a-9b48-4e85-8df5-a46793f6c701
PMCID: PMC3473080
3.  Automated Tracking of Animal Posture and Movement during Exploration and Sensory Orientation Behaviors 
PLoS ONE  2012;7(8):e41642.
Background
The nervous functions of an organism are primarily reflected in the behavior it is capable of. Measuring behavior quantitatively, at high-resolution and in an automated fashion provides valuable information about the underlying neural circuit computation. Accordingly, computer-vision applications for animal tracking are becoming a key complementary toolkit to genetic, molecular and electrophysiological characterization in systems neuroscience.
Methodology/Principal Findings
We present Sensory Orientation Software (SOS) to measure behavior and infer sensory experience correlates. SOS is a simple and versatile system to track body posture and motion of single animals in two-dimensional environments. In the presence of a sensory landscape, tracking the trajectory of the animal's sensors and its postural evolution provides a quantitative framework to study sensorimotor integration. To illustrate the utility of SOS, we examine the orientation behavior of fruit fly larvae in response to odor, temperature and light gradients. We show that SOS is suitable to carry out high-resolution behavioral tracking for a wide range of organisms including flatworms, fishes and mice.
Conclusions/Significance
Our work contributes to the growing repertoire of behavioral analysis tools for collecting rich and fine-grained data to draw and test hypothesis about the functioning of the nervous system. By providing open-access to our code and documenting the software design, we aim to encourage the adaptation of SOS by a wide community of non-specialists to their particular model organism and questions of interest.
doi:10.1371/journal.pone.0041642
PMCID: PMC3415430  PMID: 22912674
4.  Active sampling and decision making in Drosophila chemotaxis 
Nature Communications  2011;2:441-.
The ability to respond to chemical stimuli is fundamental to the survival of motile organisms, but the strategies underlying odour tracking remain poorly understood. Here we show that chemotaxis in Drosophila melanogaster larvae is an active sampling process analogous to sniffing in vertebrates. Combining computer-vision algorithms with reconstructed olfactory environments, we establish that larvae orient in odour gradients through a sequential organization of stereotypical behaviours, including runs, stops, lateral head casts and directed turns. Negative gradients, integrated during runs, control the timing of turns. Positive gradients detected through high-amplitude head casts determine the direction of individual turns. By genetically manipulating the peripheral olfactory circuit, we examine how orientation adapts to losses and gains of function in olfactory input. Our findings suggest that larval chemotaxis represents an intermediate navigation strategy between the biased random walks of Escherichia Coli and the stereo-olfaction observed in rats and humans.
Drosophila melanogaster larvae demonstrate chemotaxis towards odours but their navigation mechanism is poorly understood. Using computer-vision tracking, Gomez-Marin et al. show that larvae ascend odour gradients using an active sampling strategy that is analogous to sniffing in vertebrates.
doi:10.1038/ncomms1455
PMCID: PMC3265367  PMID: 21863008
5.  Mechanisms of Odor-Tracking: Multiple Sensors for Enhanced Perception and Behavior 
Early in evolution, the ability to sense and respond to changing environments must have provided a critical survival advantage to living organisms. From bacteria and worms to flies and vertebrates, sophisticated mechanisms have evolved to enhance odor detection and localization. Here, we review several modes of chemotaxis. We further consider the relevance of a striking and recurrent motif in the organization of invertebrate and vertebrate sensory systems, namely the existence of two symmetrical olfactory sensors. By combining our current knowledge about the olfactory circuits of larval and adult Drosophila, we examine the molecular and neural mechanisms underlying robust olfactory perception and extend these analyses to recent behavioral studies addressing the relevance and function of bilateral olfactory input for gradient detection. Finally, using a comparative theoretical approach based on Braitenberg's vehicles, we speculate about the relationships between anatomy, circuit architecture and stereotypical orientation behaviors.
doi:10.3389/fncel.2010.00006
PMCID: PMC2854573  PMID: 20407585
drosophila melanogaster; olfaction; bilateral; chemotaxis; orientation behavior; sensory perception
6.  A circuit supporting concentration-invariant odor perception in Drosophila 
Journal of Biology  2009;8(1):9.
Background
Most odors are perceived to have the same quality over a large concentration range, but the neural mechanisms that permit concentration-invariant olfactory perception are unknown. In larvae of the vinegar fly Drosophila melanogaster, odors are sensed by an array of 25 odorant receptors expressed in 21 olfactory sensory neurons (OSNs). We investigated how subsets of larval OSNs with overlapping but distinct response properties cooperate to mediate perception of a given odorant across a range of concentrations.
Results
Using calcium imaging, we found that ethyl butyrate, an ester perceived by humans as fruity, activated three OSNs with response thresholds that varied across three orders of magnitude. Whereas wild-type larvae were strongly attracted by this odor across a 500-fold range of concentration, individuals with only a single functional OSN showed attraction across a narrower concentration range corresponding to the sensitivity of each ethyl butyrate-tuned OSN. To clarify how the information carried by different OSNs is integrated by the olfactory system, we characterized the response properties of local inhibitory interneurons and projection neurons in the antennal lobe. Local interneurons only responded to high ethyl butyrate concentrations upon summed activation of at least two OSNs. Projection neurons showed a reduced response to odors when summed input from two OSNs impinged on the circuit compared to when there was only a single functional OSN.
Conclusions
Our results show that increasing odor concentrations induce progressive activation of concentration-tuned olfactory sensory neurons and concomitant recruitment of inhibitory local interneurons. We propose that the interplay of combinatorial OSN input and local interneuron activation allows animals to remain sensitive to odors across a large range of stimulus intensities.
doi:10.1186/jbiol108
PMCID: PMC2656214  PMID: 19171076

Results 1-6 (6)