Visual Projection Neurons Mediating Directed Courtship in Drosophila.

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.

Matched function of the neuropil processing optic flow in flies and crabs: the lobula plate mediates optomotor responses in Neohelice granulata.

When an animal rotates (whether it is an arthropod, a fish, a bird or a human) a drift of the visual panorama occurs over its retina, termed optic flow. The image is stabilized by compensatory behaviours (driven by the movement of the eyes, head or the whole body depending on the animal) collectively termed optomotor responses. The dipteran lobula plate has been consistently linked with optic flow processing and the control of optomotor responses. Crabs have a neuropil similarly located and interconnected in the optic lobes, therefore referred to as a lobula plate too. Here we show that the crabs' lobula plate is required for normal optomotor responses since the response was lost or severely impaired in animals whose lobula plate had been lesioned. The effect was behaviour-specific, since avoidance responses to approaching visual stimuli were not affected. Crabs require simpler optic flow processing than flies (because they move slower and in two-dimensional instead of three-dimensional space), consequently their lobula plates are relatively smaller. Nonetheless, they perform the same essential role in the visual control of behaviour. Our findings add a fundamental piece to the current debate on the evolutionary relationship between the lobula plates of insects and crustaceans.

Direction Selective Neurons Responsive to Horizontal Motion in a Crab Reflect an Adaptation to Prevailing Movements in Flat Environments.

All animals need information about the direction of motion to be able to track the trajectory of a target (prey, predator, cospecific) or to control the course of navigation. This information is provided by direction selective (DS) neurons, which respond to images moving in a unique direction. DS neurons have been described in numerous species including many arthropods. In these animals, the majority of the studies have focused on DS neurons dedicated to processing the optic flow generated during navigation. In contrast, only a few studies were performed on DS neurons related to object motion processing. The crab Neohelice is an established experimental model for the study of neurons involved in visually-guided behaviors. Here, we describe in male crabs of this species a new group of DS neurons that are highly directionally selective to moving objects. The neurons were physiologically and morphologically characterized by intracellular recording and staining in the optic lobe of intact animals. Because of their arborization in the lobula complex, we called these cells lobula complex directional cells (LCDCs). LCDCs also arborize in a previously undescribed small neuropil of the lateral protocerebrum. LCDCs are responsive only to horizontal motion. This nicely fits in the behavioral adaptations of a crab inhabiting a flat, densely crowded environment, where most object motions are generated by neighboring crabs moving along the horizontal plane.SIGNIFICANCE STATEMENT Direction selective (DS) neurons are key to a variety of visual behaviors including, target tracking (preys, predators, cospecifics) and course control. Here, we describe the physiology and morphology of a new group of remarkably directional neurons exclusively responsive to horizontal motion in crabs. These neurons arborize in the lobula complex and in a previously undescribed small neuropil of the lateral protocerebrum. The strong sensitivity of these cells for horizontal motion represents a clear example of functional neuronal adaptation to the lifestyle of an animal inhabiting a flat environment.

The impulse response of optic flow-sensitive descending neurons to roll m-sequences.

When animals move through the world, their own movements generate widefield optic flow across their eyes. In insects, such widefield motion is encoded by optic lobe neurons. These lobula plate tangential cells (LPTCs) synapse with optic flow-sensitive descending neurons, which in turn project to areas that control neck, wing and leg movements. As the descending neurons play a role in sensorimotor transformation, it is important to understand their spatio-temporal response properties. Recent work shows that a relatively fast and efficient way to quantify such response properties is to use m-sequences or other white noise techniques. Therefore, here we used m-sequences to quantify the impulse responses of optic flow-sensitive descending neurons in male Eristalis tenax hoverflies. We focused on roll impulse responses as hoverflies perform exquisite head roll stabilizing reflexes, and the descending neurons respond particularly well to roll. We found that the roll impulse responses were fast, peaking after 16.5-18.0 ms. This is similar to the impulse response time to peak (18.3 ms) to widefield horizontal motion recorded in hoverfly LPTCs. We found that the roll impulse response amplitude scaled with the size of the stimulus impulse, and that its shape could be affected by the addition of constant velocity roll or lift. For example, the roll impulse response became faster and stronger with the addition of excitatory stimuli, and vice versa. We also found that the roll impulse response had a long return to baseline, which was significantly and substantially reduced by the addition of either roll or lift.

Differential Tuning to Visual Motion Allows Robust Encoding of Optic Flow in the Dragonfly.

Visual cues provide an important means for aerial creatures to ascertain their self-motion through the environment. In many insects, including flies, moths, and bees, wide-field motion-sensitive neurons in the third optic ganglion are thought to underlie such motion encoding; however, these neurons can only respond robustly over limited speed ranges. The task is more complicated for some species of dragonflies that switch between extended periods of hovering flight and fast-moving pursuit of prey and conspecifics, requiring motion detection over a broad range of velocities. Since little is known about motion processing in these insects, we performed intracellular recordings from hawking, emerald dragonflies (Hemicordulia spp.) and identified a diverse group of motion-sensitive neurons that we named lobula tangential cells (LTCs). Following prolonged visual stimulation with drifting gratings, we observed significant differences in both temporal and spatial tuning of LTCs. Cluster analysis of these changes confirmed several groups of LTCs with distinctive spatiotemporal tuning. These differences were associated with variation in velocity tuning in response to translated, natural scenes. LTCs with differences in velocity tuning ranges and optima may underlie how a broad range of motion velocities are encoded. In the hawking dragonfly, changes in LTC tuning over time are therefore likely to support their extensive range of behaviors, from hovering to fast-speed pursuits.SIGNIFICANCE STATEMENT Understanding how animals navigate the world is an inherently difficult and interesting problem. Insects are useful models for understanding neuronal mechanisms underlying these activities, with neurons that encode wide-field motion previously identified in insects, such as flies, hawkmoths, and butterflies. Like some Dipteran flies, dragonflies exhibit complex aerobatic behaviors, such as hovering, patrolling, and aerial combat. However, dragonflies lack halteres that support such diverse behavior in flies. To understand how dragonflies might address this problem using only visual cues, we recorded from their wide-field motion-sensitive neurons. We found these differ strongly in the ways they respond to sustained motion, allowing them collectively to encode the very broad range of velocities experienced during diverse behavior.

The diversity of lobula plate tangential cells (LPTCs) in the Drosophila motion vision system.

To navigate through the environment, animals rely on visual feedback to control their movements relative to their surroundings. In dipteran flies, visual feedback is provided by the wide-field motion-sensitive neurons in the visual system called lobula plate tangential cells (LPTCs). Understanding the role of LPTCs in fly behaviors can address many fundamental questions on how sensory circuits guide behaviors. The blowfly was estimated to have ~ 60 LPTCs, but only a few have been identified in Drosophila. We conducted a Gal4 driver screen and identified five LPTC subtypes in Drosophila, based on their morphological characteristics: LPTCs have large arborizations in the lobula plate and project to the central brain. We compared their morphologies to the blowfly LPTCs and named them after the most similar blowfly cells: CH, H1, H2, FD1 and FD3, and V1. We further characterized their pre- and post-synaptic organizations, as well as their neurotransmitter profiles. These anatomical features largely agree with the anatomy and function of their likely blowfly counterparts. Nevertheless, several anatomical details indicate the Drosophila LPTCs may have more complex functions. Our characterization of these five LPTCs in Drosophila will facilitate further functional studies to understand their roles in the visual circuits that instruct fly behaviors.

Active membrane conductances and morphology of a collision detection neuron broaden its impedance profile and improve discrimination of input synchrony.

How neurons filter and integrate their complex patterns of synaptic inputs is central to their role in neural information processing. Synaptic filtering and integration are shaped by the frequency-dependent neuronal membrane impedance. Using single and dual dendritic recordings in vivo, pharmacology, and computational modeling, we characterized the membrane impedance of a collision detection neuron in the grasshopper Schistocerca americana. This neuron, the lobula giant movement detector (LGMD), exhibits consistent impedance properties across frequencies and membrane potentials. Two common active conductances gH and gM, mediated respectively by hyperpolarization-activated cyclic nucleotide-gated (HCN) channels and by muscarine-sensitive M-type K+ channels, promote broadband integration with high temporal precision over the LGMD's natural range of membrane potentials and synaptic input frequencies. Additionally, we found that a model based on the LGMD's branching morphology increased the gain and decreased the delay associated with the mapping of synaptic input currents to membrane potential. More generally, this was true for a wide range of model neuron morphologies, including those of neocortical pyramidal neurons and cerebellar Purkinje cells. These findings show the unexpected role played by two widespread active conductances and by dendritic morphology in shaping synaptic integration.NEW & NOTEWORTHY Neuronal filtering and integration of synaptic input patterns depend on the electrochemical properties of dendrites. We used an identified collision detection neuron in grasshoppers to examine how its morphology and two conductances affect its membrane impedance in relation to the computations it performs. The neuronal properties examined are ubiquitous and therefore promote a general understanding of neuronal computations, including those in the human brain.

M current regulates firing mode and spike reliability in a collision-detecting neuron.

All animals must detect impending collisions to escape and reliably discriminate them from nonthreatening stimuli, thus preventing false alarms. Therefore, it is no surprise that animals have evolved highly selective and sensitive neurons dedicated to such tasks. We examined a well-studied collision-detection neuron in the grasshopper ( Schistocerca americana) using in vivo electrophysiology, pharmacology, and computational modeling. This lobula giant movement detector (LGMD) neuron is excitable by inputs originating from each ommatidia of the compound eye. It possesses many intrinsic properties that increase its selectivity to objects approaching on a collision course, including switching between burst and nonburst firing. In this study, we demonstrate that the LGMD neuron exhibits a large M current, generated by noninactivating K+ channels, that shortens the temporal window of dendritic integration, regulates a firing mode switch between burst and isolated spiking, increases the precision of spike timing, and increases the reliability of spike propagation to downstream motor centers. By revealing how the M current increases the LGMD's ability to detect impending collisions, our results suggest that similar channels may play an analogous role in other collision detection circuits. NEW & NOTEWORTHY The ability to reliably detect impending collisions is a critical survival skill. The nervous systems of many animals have developed dedicated neurons for accomplishing this task. We used a mix of in vivo electrophysiology and computational modeling to investigate the role of M potassium channels within one such collision-detecting neuron and show that through regulation of burst firing and enhancement of spiking reliability, the M current increases the ability to detect impending collisions.

Morphology of visual projection neurons supplying premotor area in the brain of the silkmoth Bombyx mori.

Sex pheromones orient male moths toward conspecific female moths; the presence of visual information modulates this behavior. In the current study, we explore candidate neuronal pathways for the interaction between vision and the locomotor signal for pheromone orientation. We describe the connectivity between visual neuropils and brain premotor centers, the posterior slope (PS) and the lateral accessory lobe (LAL), in the silkmoth Bombyx mori. Using a single-cell labeling technique, we analyze visual projection neurons supplying these areas. Neurons from both the medulla and lobula complex projected to the PS but only the neurons originating in the lobula complex had additional processes to the LAL. Further, we identified populations of putative feedback neurons from the premotor centers to the optic lobe. Neurons originating in the PS were likely to project to the medulla, whereas those originating in the LAL were likely to project to the lobula complex. The anatomical study contributes to further understanding of integration of visual information on the locomotor control in the insect brain.

Cellular mechanisms for integral feedback in visually guided behavior.

Sensory feedback is a ubiquitous feature of guidance systems in both animals and engineered vehicles. For example, a common strategy for moving along a straight path is to turn such that the measured rate of rotation is zero. This task can be accomplished by using a feedback signal that is proportional to the instantaneous value of the measured sensory signal. In such a system, the addition of an integral term depending on past values of the sensory input is needed to eliminate steady-state error [proportional-integral (PI) control]. However, the means by which nervous systems implement such a computation are poorly understood. Here, we show that the optomotor responses of flying Drosophila follow a time course consistent with temporal integration of horizontal motion input. To investigate the cellular basis of this effect, we performed whole-cell patch-clamp recordings from the set of identified visual interneurons [horizontal system (HS) cells] thought to control this reflex during tethered flight. At high stimulus speeds, HS cells exhibit steady-state responses during flight that are absent during quiescence, a state-dependent difference in physiology that is explained by changes in their presynaptic inputs. However, even during flight, the membrane potential of the large-field interneurons exhibits no evidence for integration that could explain the behavioral responses. However, using a genetically encoded indicator, we found that calcium accumulates in the terminals of the interneurons along a time course consistent with the behavior and propose that this accumulation provides a mechanism for temporal integration of sensory feedback consistent with PI control.