Neurons forming optic glomeruli compute figure-ground discriminations in Drosophila.

Many animals rely on visual figure-ground discrimination to aid in navigation, and to draw attention to salient features like conspecifics or predators. Even figures that are similar in pattern and luminance to the visual surroundings can be distinguished by the optical disparity generated by their relative motion against the ground, and yet the neural mechanisms underlying these visual discriminations are not well understood. We show in flies that a diverse array of figure-ground stimuli containing a motion-defined edge elicit statistically similar behavioral responses to one another, and statistically distinct behavioral responses from ground motion alone. From studies in larger flies and other insect species, we hypothesized that the circuitry of the lobula--one of the four, primary neuropiles of the fly optic lobe--performs this visual discrimination. Using calcium imaging of input dendrites, we then show that information encoded in cells projecting from the lobula to discrete optic glomeruli in the central brain group these sets of figure-ground stimuli in a homologous manner to the behavior; "figure-like" stimuli are coded similar to one another and "ground-like" stimuli are encoded differently. One cell class responds to the leading edge of a figure and is suppressed by ground motion. Two other classes cluster any figure-like stimuli, including a figure moving opposite the ground, distinctly from ground alone. This evidence demonstrates that lobula outputs provide a diverse basis set encoding visual features necessary for figure detection.

Olfactory neuromodulation of motion vision circuitry in Drosophila.

It is well established that perception is largely multisensory; often served by modalities such as touch, vision, and hearing that detect stimuli emanating from a common point in space; and processed by brain tissue maps that are spatially aligned. However, the neural interactions among modalities that share no spatial stimulus domain yet are essential for robust perception within noisy environments remain uncharacterized. Drosophila melanogaster makes its living navigating food odor plumes. Odor acts to increase the strength of gaze-stabilizing optomotor reflexes to keep the animal aligned within an invisible plume, facilitating odor localization in free flight. Here, we investigate the cellular mechanism for cross-modal behavioral interactions. We characterize a wide-field motion-selective interneuron of the lobula plate that shares anatomical and physiological similarities with the "Hx" neuron identified in larger flies. Drosophila Hx exhibits cross-modal enhancement of visual responses by paired odor, and presynaptic inputs to the lobula plate are required for behavioral odor tracking but are not themselves the target of odor modulation, nor is the neighboring wide-field "HSE" neuron. Octopaminergic neurons mediating increased visual responses upon flight initiation also show odor-evoked calcium modulations and form connections with Hx dendrites. Finally, restoring synaptic vesicle trafficking within the octopaminergic neurons of animals carrying a null mutation for all aminergic signaling is sufficient to restore odor-tracking behavior. These results are the first to demonstrate cellular mechanisms underlying visual-olfactory integration required for odor localization in fruit flies, which may be representative of adaptive multisensory interactions across taxa.

Method and software for using m-sequences to characterize parallel components of higher-order visual tracking behavior in Drosophila.

A moving visual figure may contain first-order signals defined by variation in mean luminance, as well as second-order signals defined by constant mean luminance and variation in luminance envelope, or higher-order signals that cannot be estimated by taking higher moments of the luminance distribution. Separating these properties of a moving figure to experimentally probe the visual subsystems that encode them is technically challenging and has resulted in debated mechanisms of visual object detection by flies. Our prior work took a white noise systems identification approach using a commercially available electronic display system to characterize the spatial variation in the temporal dynamics of two distinct subsystems for first- and higher-order components of visual figure tracking. The method relied on the use of single pixel displacements of two visual stimuli according to two binary maximum length shift register sequences (m-sequences) and cross-correlation of each m-sequence with time-varying flight steering measurements. The resultant spatio-temporal action fields represent temporal impulse responses parameterized by the azimuthal location of the visual figure, one STAF for first-order and another for higher-order components of compound stimuli. Here we review m-sequence and reverse correlation procedures, then describe our application in detail, provide Matlab code, validate the STAFs, and demonstrate the utility and robustness of STAFs by predicting the results of other published experimental procedures. This method has demonstrated how two relatively modest innovations on classical white noise analysis--the inclusion of space as a way to organize response kernels and the use of linear decoupling to measure the response to two channels of visual information simultaneously--could substantially improve our basic understanding of visual processing in the fly.

Figure-ground discrimination behavior in Drosophila. I. Spatial organization of wing-steering responses.

The behavioral algorithms and neural subsystems for visual figure-ground discrimination are not sufficiently described in any model system. The fly visual system shares structural and functional similarity with that of vertebrates and, like vertebrates, flies robustly track visual figures in the face of ground motion. This computation is crucial for animals that pursue salient objects under the high performance requirements imposed by flight behavior. Flies smoothly track small objects and use wide-field optic flow to maintain flight-stabilizing optomotor reflexes. The spatial and temporal properties of visual figure tracking and wide-field stabilization have been characterized in flies, but how the two systems interact spatially to allow flies to actively track figures against a moving ground has not. We took a systems identification approach in flying Drosophila and measured wing-steering responses to velocity impulses of figure and ground motion independently. We constructed a spatiotemporal action field (STAF) - the behavioral analog of a spatiotemporal receptive field - revealing how the behavioral impulse responses to figure tracking and concurrent ground stabilization vary for figure motion centered at each location across the visual azimuth. The figure tracking and ground stabilization STAFs show distinct spatial tuning and temporal dynamics, confirming the independence of the two systems. When the figure tracking system is activated by a narrow vertical bar moving within the frontal field of view, ground motion is essentially ignored despite comprising over 90% of the total visual input.

Higher-order figure discrimination in fly and human vision.

Visually-guided animals rely on their ability to stabilize the panorama and simultaneously track salient objects, or figures, that are distinct from the background in order to avoid predators, pursue food resources and mates, and navigate spatially. Visual figures are distinguished by luminance signals that produce coherent motion cues as well as more enigmatic 'higher-order' statistical features. Figure discrimination is thus a complex form of motion vision requiring specialized neural processing. In this minireview, we will highlight recent advances in understanding the perceptual, behavioral, and neurophysiological basis of higher-order figure detection in flies, much of which is grounded in the historical perspective and mechanistic underpinnings of human psychophysics.

Flies dynamically anti-track, rather than ballistically escape, aversive odor during flight.

Tracking distant odor sources is crucial to foraging, courtship and reproductive success for many animals including fish, flies and birds. Upon encountering a chemical plume in flight, Drosophila melanogaster integrates the spatial intensity gradient and temporal fluctuations over the two antennae, while simultaneously reducing the amplitude and frequency of rapid steering maneuvers, stabilizing the flight vector. There are infinite escape vectors away from a noxious source, in contrast to a single best tracking vector towards an attractive source. Attractive and aversive odors are segregated into parallel neuronal pathways in flies; therefore, the behavioral algorithms for avoidance may be categorically different from tracking. Do flies plot random ballistic or otherwise variable escape vectors? Or do they instead make use of temporally dynamic mechanisms for continuously and directly avoiding noxious odors in a manner similar to tracking appetitive ones? We examine this question using a magnetic tether flight simulator that permits free yaw movements, such that flies can actively orient within spatially defined odor plumes. We show that in-flight aversive flight behavior shares all of the key features of attraction such that flies continuously 'anti-track' the noxious source.

Figure tracking by flies is supported by parallel visual streams.

Visual figures may be distinguished based on elementary motion or higher-order non-Fourier features, and flies track both. The canonical elementary motion detector, a compact computation for Fourier motion direction and amplitude, can also encode higher-order signals provided elaborate preprocessing. However, the way in which a fly tracks a moving figure containing both elementary and higher-order signals has not been investigated. Using a novel white noise approach, we demonstrate that (1) the composite response to an object containing both elementary motion (EM) and uncorrelated higher-order figure motion (FM) reflects the linear superposition of each component; (2) the EM-driven component is velocity-dependent, whereas the FM component is driven by retinal position; (3) retinotopic variation in EM and FM responses are different from one another; (4) the FM subsystem superimposes saccadic turns upon smooth pursuit; and (5) the two systems in combination are necessary and sufficient to predict the full range of figure tracking behaviors, including those that generate no EM cues at all. This analysis requires an extension of the model that fly motion vision is based on simple elementary motion detectors and provides a novel method to characterize the subsystems responsible for the pursuit of visual figures.

Silicon nanoparticles as hyperpolarized magnetic resonance imaging agents.

Magnetic resonance imaging of hyperpolarized nuclei provides high image contrast with little or no background signal. To date, in vivo applications of prehyperpolarized materials have been limited by relatively short nuclear spin relaxation times. Here, we investigate silicon nanoparticles as a new type of hyperpolarized magnetic resonance imaging agent. Nuclear spin relaxation times for a variety of Si nanoparticles are found to be remarkably long, ranging from many minutes to hours at room temperature, allowing hyperpolarized nanoparticles to be transported, administered, and imaged on practical time scales. Additionally, we demonstrate that Si nanoparticles can be surface functionalized using techniques common to other biologically targeted nanoparticle systems. These results suggest that Si nanoparticles can be used as a targetable, hyperpolarized magnetic resonance imaging agent with a large range of potential applications.