Virtual reality (VR) environments are increasingly being used by neuroscientists to simulate natural events and social interactions. VR creates interactive, multimodal sensory stimuli that offer unique advantages over other approaches to neuroscientific research and applications. VR's compatibility with imaging technologies such as functional MRI allows researchers to present multimodal stimuli with a high degree of ecological validity and control while recording changes in brain activity. Therapists, too, stand to gain from progress in VR technology, which provides a high degree of control over the therapeutic experience. Here we review the latest advances in VR technology and its applications in neuroscience research.

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Virtual reality in neuroscience research and therapy

Viability and electrophysiology of neural cell structures generated by the inkjet printing method.

Insects locate many resources important to survival by tracking along wind-borne odor plumes to their source. It is well known that plumes are patchy distributions of high concentration packets of odor interspersed with clean air, not smooth Gaussian distributions of odor intensity. This realization has been crucial to our understanding of plume-tracking behavior, because insect locomotory movements and sensory processing typically take place in the range of tens to hundreds of milliseconds, permitting them to respond to the rapid changes in odor concentration they experience in plumes. Because odor plumes are not comprised of smooth concentration gradients, they cannot provide the directional information necessary to allow plume-tracking insects to steer toward the source. Many experiments have shown that, in the species examined, successful source location requires two sensory inputs: the presence of the attractive odor and the detection of the direction of the wind bearing that odor. All plume-tracking insects use the wind direction as the primary directional cue that enables them to steer their movements toward the odor source. Experimental manipulations of the presence and absence of the odor, and the presence, absence, or direction of the wind during plume tracking, have begun to resolve the relationship between these two sensory inputs and how they shape the maneuvers we observe. Experiments, especially those undertaken in the natural wind and odor environments of the organisms in question and those directed at understanding the neural processing that underlie plume tracking, promise to enhance our understanding of this remarkable behavior.

Navigational Strategies Used by Insects to Find Distant, Wind-Borne Sources of Odor

The colony-level phenotype of an insect society emerges from interactions between large numbers of individuals that may differ considerably in their morphology, physiology, and behavior. The proximate and ultimate mechanisms that allow this complex integrated system to form are not fully known, and understanding the evolution of social life strategies is a major topic in systems biology. In solitary insects, behavior, sensory tuning, and reproductive physiology are linked. These associations are controlled in part by pleiotropic networks that organize the sequential expression of phases in the reproductive cycle. Here we explore whether similar associations give rise to different behavioral phenotypes in a eusocial worker caste. We document that the pleiotropic genetic network that controls foraging behavior in functionally sterile honey bee workers (Apis mellifera) has a reproductive component. Associations between behavior, physiology, and sensory tuning in workers with different foraging strategies indicate that the underlying genetic architectures were designed to control a reproductive cycle. Genetic circuits that make up the regulatory “ground plan” of a reproductive strategy may provide powerful building blocks for social life. We suggest that exploitation of this ground plan plays a fundamental role in the evolution of social insect societies.

https://www.pnas.org/content/pnas/101/31/11350.full.pdf

Reproductive ground plan may mediate colony-level selection effects on individual foraging behavior in honey bees

Flies rely heavily on visual feedback for several aspects of flight control. As a fly approaches an object, the image projected across its retina expands, providing the fly with visual feedback that can be used either to trigger a collision-avoidance maneuver or a landing response. To determine how a fly makes the decision to land on or avoid a looming object, we measured the behaviors generated in response to an expanding image during tethered flight in a visual closed-loop flight arena. During these experiments, each fly varied its wing-stroke kinematics to actively control the azimuth position of a 15°×15° square within its visual field. Periodically, the square symmetrically expanded in both the horizontal and vertical directions. We measured changes in the fly's wing-stroke amplitude and frequency in response to the expanding square while optically tracking the position of its legs to monitor stereotyped landing responses. Although this stimulus could elicit both the landing responses and collision-avoidance reactions, separate pathways appear to mediate the two behaviors. For example, if the square is in the lateral portion of the fly's field of view at the onset of expansion, the fly increases stroke amplitude in one wing while decreasing amplitude in the other, indicative of a collision-avoidance maneuver. In contrast, frontal expansion elicits an increase in wing-beat frequency and leg extension, indicative of a landing response. To further characterize the sensitivity of these responses to expansion rate, we tested a range of expansion velocities from 100 to 10000° s^(-1). Differences in the latency of both the collision-avoidance reactions and the landing responses with expansion rate supported the hypothesis that the two behaviors are mediated by separate pathways. To examine the effects of visual feedback on the magnitude and time course of the two behaviors, we presented the stimulus under open-loop conditions, such that the fly's response did not alter the position of the expanding square. From our results we suggest a model that takes into account the spatial sensitivities and temporal latencies of the collision-avoidance and landing responses, and is sufficient to schematically represent how the fly uses integration of motion information in deciding whether to turn or land when confronted with an expanding object.

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Collision-avoidance and landing responses are mediated by separate pathways in the fruit fly, Drosophila melanogaster.

We recorded the activity of the right and left descending contralateral movement detectors responding to 10-cm (small) or 20-cm (large) computer-generated spheres approaching along different trajectories in the locust's frontal field of view. In separate experiments we examined the steering responses of tethered flying locusts to identical stimuli. The descending contralateral movement detectors were more sensitive to variations in target trajectory in the horizontal plane than in the vertical plane. Descending contralateral movement detector activity was related to target trajectory and to target size and was most sensitive to small objects converging on a direct collision course from above and to one side. Small objects failed to induce collision avoidance manoeuvres whereas large objects produced reliable collision avoidance responses. Large targets approaching along a converging trajectory produced steering responses that were either away from or toward the side of approach of the object, whereas targets approaching along trajectories that were offset from the locust's mid-longitudinal body axis primarily evoked responses away from the target. We detected no differences in the discharge properties of the descending contralateral movement detector pair that could account for the different collision avoidance behaviours evoked by varying the target size and trajectories. We suggest that descending contralateral movement detector properties are better suited to predator evasion than collision avoidance.

Activity of descending contralateral movement detector neurons and collision avoidance behaviour in response to head-on visual stimuli in locusts.

Neurons in the locust visual system encode approaches of looming stimuli and are implicated in production of escape behaviours. The lobula giant movement detector (LGMD) and its postsynaptic partner, the descending contralateral movement detector (DCMD) compute characteristics of expanding edges across the locust eye during a loom and DCMD synapses onto motor elements associated with behaviour. We identified another descending interneuron within the locust ventral nerve cord. We named this neuron the late DCMD (LDCMD) as it responds later during an approach, with the firing rate peaking at about the time of collision. LDCMD produced lower amplitude, broader action potentials that were associated with an afterhyperpolarization, whereas DCMD action potentials showed a brief afterhyperpolarization often followed by an afterdepolarization. Within the mesothoracic ganglion, the primary LDCMD axon located adjacent to the DCMD axon, was thinner and lacked collateral projections to the lateral region of the neuropil. When compared with DCMD, LDCMD fired with fewer spikes during a loom and showed weaker habituation to repeated approaches. Coincidence of LDCMD and DCMD firing increased during object approach. Our findings indicate the presence of an additional motion-sensitive descending neuron in the locust that encodes temporally distinct properties of an approaching object.

A pair of motion-sensitive neurons in the locust encode approaches of a looming object

A method for recording behavior and multineuronal CNS activity from tethered insects flying in virtual space.

The lobula giant movement detector (LGMD) and its target neuron, the descending contralateral movement detector (DCMD), constitute a motion-sensitive pathway in the locust visual system that responds preferentially to objects approaching on a collision course. LGMD receptive field properties, anisotropic distribution of local retinotopic inputs across the visual field, and localized habituation to repeated stimuli suggest that this pathway should be sensitive to approaches of individual objects within a complex visual scene. We presented locusts with compound looming objects while recording from the DCMD to test the effects of nonuniform edge expansion on looming responses. We also presented paired objects approaching from different regions of the visual field at nonoverlapping, closely timed and simultaneous approach intervals to study DCMD responses to multiple looming stimuli. We found that looming compound objects evoked characteristic responses in the DCMD and that the time of peak firing was consistent with predicted values based on a weighted ratio of the half size of each distinct object edge and the absolute approach velocity. We also found that the azimuthal position and interval of paired approaches affected DCMD firing properties and that DCMDs responded to individual objects approaching within 106 ms of each other. Moreover, comparisons between individual and paired approaches revealed that overlapping approaches are processed in a strongly sublinear manner. These findings are consistent with biophysical mechanisms that produce nonlinear integration of excitatory and feed-forward inhibitory inputs onto the LGMD that have been shown to underlie responses to looming stimuli.

https://www.physiology.org/doi/pdf/10.1152/jn.01037.2005

Responses of a Looming-Sensitive Neuron to Compound and Paired Object Approaches

Many animals must contend with visual cues that provide information about the spatiotemporal dynamics of multiple objects in their environment. Much research has been devoted to understanding how an identified pair of interneurons in the locust, the Descending Contralateral Movement Detectors (DCMDs), respond to objects on an impending collision course. However, little is known about how these neurons respond when challenged with multiple, looming objects of different complex shapes. I presented locusts with objects resembling either another locust or a bird approaching on a direct collision course at 3 m s-1 while recording from the DCMD axon within the mesothoracic ganglion. Stimulus presentations were designed to test: (i) whether DCMD habituation was related to the frequency of approach, (ii) if habituated DCMDs were able to respond to a novel stimulus and (iii) if non-looming motion within complex objects (internal object motion) during approach affects habituation. DCMD responses to simulated locusts or birds habituated more when the time interval between consecutive approaches within similar sequences decreased from 34 s to 4 s. Strongly habituated DCMDs were, however, able to respond to the same object approaching along a new trajectory or to a larger object approaching along the same trajectory. Habituation was not affected by internal object motion. These data are consistent with earlier findings that DCMD habituation occurs at localized synapses, which permits maintained sensitivity to multiple objects in the animal's environment.

John R. Gray

Papers

Activity of descending contralateral movement detector neurons and collision avoidance behaviour in response to head-on visual stimuli in locusts.

A pair of motion-sensitive neurons in the locust encode approaches of a looming object

A method for recording behavior and multineuronal CNS activity from tethered insects flying in virtual space.

Responses of a Looming-Sensitive Neuron to Compound and Paired Object Approaches

Habituated visual neurons in locusts remain sensitive to novel looming objects.