John R. Gray

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

Abstract. 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 locusts 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 locusts 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.

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

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.

Habituated visual neurons in locusts remain sensitive to novel looming objects

SUMMARY 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 animals environment.

The state of computer-aided control system design (CACSD)

Introduction to a special issue consisting of a sample of the broad range of research activities, seeking to provide theoretical foundations and software engineering tools to help control engineers understand and overcome challenges in building computer-controlled devices. >

Visual stimuli induced by self-motion and object-motion modify odour-guided flight of male moths (Manduca sexta L.).

SUMMARY Animals rely on multimodal sensory integration for proper orientation within their environment. For example, odour-guided behaviours often require appropriate integration of concurrent visual cues. To gain a further understanding of mechanisms underlying sensory integration in odour-guided behaviour, our study examined the effects of visual stimuli induced by self-motion and object-motion on odour-guided flight in male M. sexta. By placing stationary objects (pillars) on either side of a female pheromone plume, moths produced self-induced visual motion during odour-guided flight. These flights showed a reduction in both ground and flight speeds and inter-turn interval when compared with flight tracks without stationary objects. Presentation of an approaching 20 cm disc, to simulate object-motion, resulted in interrupted odour-guided flight and changes in flight direction away from the pheromone source. Modifications of odour-guided flight behaviour in the presence of stationary objects suggest that visual information, in conjunction with olfactory cues, can be used to control the rate of counter-turning. We suggest that the behavioural responses to visual stimuli induced by object-motion indicate the presence of a neural circuit that relays visual information to initiate escape responses. These behavioural responses also suggest the presence of a sensory conflict requiring a trade-off between olfactory and visually driven behaviours. The mechanisms underlying olfactory and visual integration are discussed in the context of these behavioural responses.

Effects of heat stress on axonal conduction in the locust flight system

Abstract Pretreatment of tissues or whole organisms with high, sublethal temperatures (heat shock) induces thermotolerance to normally lethal temperatures. It is of interest whether heat shock induces protection of neuronal function at normally lethal temperatures by investigating effects of heat shock on the temperature sensitivity of neuronal parameters in the locust flight system. The rhythm frequency of the deafferented flight motor was measured as well as the conduction velocity and amplitude of extracellularly recorded action potentials conveyed along the forewing stretch receptor axon. Measurements were made at temperatures ranging from 10 to 50°C in heat shocked and control animals. The deafferented rhythm was less sensitive to temperature changes above 35°C in heat shocked animals. The conduction velocity and relative amplitude of action potentials conveyed along the stretch receptor axon were less sensitive to temperature increases above 20°C in heat shocked animals. These data suggest that heat shock conserves the operation of the flight system at high temperatures. This may be accomplished by a decrease in the thermosensitivity of the conduction velocity and amplitude of action potentials within the central flight circuitry. The latter effect may serve to protect synaptic interactions and thus allow the circuitry to operate within optimal parameters.

A looming-sensitive pathway responds to changes in the trajectory of object motion

Two identified locust neurons, the lobula giant movement detector (LGMD) and its postsynaptic partner, the descending contralateral movement detector (DCMD), constitute one motion-sensitive pathway in the visual system that responds preferentially to objects that approach on a direct collision course and are implicated in collision-avoidance behavior. Previously described responses to the approach of paired objects and approaches at different time intervals (Guest BB, Gray JR. J Neurophysiol 95: 1428-1441, 2006) suggest that this pathway may also be affected by more complicated movements in the locusts visual environment. To test this possibility we presented stationary locusts with disks traveling along combinations of colliding (looming), noncolliding (translatory), and near-miss trajectories. Distinctly different responses to different trajectories and trajectory changes demonstrate that DCMD responds to complex aspects of local visual motion. DCMD peak firing rates associated with the time of collision remained relatively invariant after a trajectory change from translation to looming. Translatory motion initiated in the frontal visual field generated a larger peak firing rate relative to object motion initiated in the posterior visual field, and the peak varied with simulated distance from the eye. Transition from translation to looming produced a transient decrease in the firing rate, whereas transition away from looming produced a transient increase. The change in firing rate at the time of transition was strongly correlated with unique expansion parameters described by the instantaneous angular acceleration of the leading edge and subtense angle of the disk. However, response time remained invariant. While these results may reflect low spatial resolution of the compound eye, they also suggest that this motion-sensitive pathway may be capable of monitoring dynamic expansion properties of objects that change the trajectory of motion.

Spatiotemporal stimulus properties modulate responses to trajectory changes in a locust looming-sensitive pathway

The lobula giant movement detector (LGMD) and descending contralateral movement detector (DCMD) constitute one motion-sensitive pathway in the locust visual system that is implicated in collision-avoidance behaviors. While this pathway is thought to respond preferentially to objects approaching on a direct collision course, emerging studies suggest the firing rate is able to monitor more complicated movements that would occur under natural conditions. While previous studies have compared the response of the DCMD to objects on collision courses that travel at different speeds, velocity has not been manipulated for other simple or compound trajectories. Here we test the possibility that the LGMD/DCMD pathway is capable of responding uniquely to complex aspects of object motion, including translation and trajectory changes at different velocities. We found that the response of the DCMD to translational motion initiated in the caudal visual field was a low-amplitude peak in firing rate that occurred before the object crossed 90° azimuth that was invariant to different object velocities. Direct looms at different velocities resulted in peak firing rates that occurred later in time and with greater amplitude for higher velocities. In response to transitions from translational motion to a collision course, the firing rate change depended on both the location within the visual field and the velocity. These results suggest that this pathway is capable of conveying information about multiple properties of a moving objects trajectory.

Activity of the forewing stretch receptor in immature and mature adult locusts

Maturation of the flight system of Locusta migratoria occurs during the first two weeks following imaginal ecdysis. One aspect of maturation is an increase in the wingbeat frequency from about 13 Hz to about 23 Hz. We investigated physiological and anatomical mechanisms that may contribute to this process. The difference between the frequencies of the central flight rhythms of immature and mature deafferented preparations was not as great as that between the wingbeat frequencies of immature and mature intact animals. Results from static and dynamic wing elevation showed that the intensity of the forewing stretch receptor response to a given stimulus increased during maturation. The diameter of the main stretch receptor axon was larger and the conduction velocity of signals conveyed along the forewing stretch receptor and the dorsal longitudinal motoneuron was faster in mature than in immature animals. We conclude that during maturation of the flight system the forewing stretch receptor responds to wing elevation with a higher frequency signal that reaches the central circuitry faster. These findings are discussed in the context of a model that describes the influence of stretch receptor input on wingbeat frequency along with other potential mechanisms involved in flight maturation.

Bilateral flight muscle activity predicts wing kinematics and 3-dimensional body orientation of locusts responding to looming objects

SUMMARY We placed locusts in a wind tunnel using a loose tether design that allowed for motion in all three rotational degrees of freedom during presentation of a computer-generated looming disc. High-speed video allowed us to extract wing kinematics, abdomen position and 3-dimensional body orientation. Concurrent electromyographic (EMG) recordings monitored bilateral activity from the first basalar depressor muscles (m97) of the forewings, which are implicated in flight steering. Behavioural responses to a looming disc included cessation of flight (wings folded over the body), glides and active steering during sustained flight in addition to a decrease and increase in wingbeat frequency prior to and during, respectively, an evasive turn. Active steering involved shifts in bilateral m97 timing, wing asymmetries and whole-body rotations in the yaw (ψ), pitch (χ) and roll (η) planes. Changes in abdomen position and hindwing asymmetries occurred after turns were initiated. Forewing asymmetry and changes in η were most highly correlated with m97 spike latency. Correlations also increased as the disc approached, peaking prior to collision. On the inside of a turn, m97 spikes occurred earlier relative to forewing stroke reversal and bilateral timing corresponded to forewing asymmetry as well as changes in whole-body rotation. Double spikes in each m97 occurred most frequently at or immediately prior to the time the locusts turned, suggesting a behavioural significance. These data provide information on mechanisms underlying 3-dimensional flight manoeuvres and will be used to drive a closed loop flight simulator to study responses of motion-sensitive visual neurons during production of realistic behaviours.