Orthopteran DCMD neuron: a reevaluation of responses to moving objects. II. Critical cues for detecting approaching objects.

1. We examine the critical image cues that are used by the locust visual system for the descending contralateral motion detector (DCMD) neuron to distinguish approaching from receding objects. Images were controlled by computer and presented on an electrostatic monitor. 2. Changes in overall luminance elicited much smaller and briefer responses from the DCMD than objects that appeared to approach the eye. Although a decrease in overall luminance might boost the response to an approaching dark object, movement of edges of the image is more important. 3. When two pairs of lines, in a cross-hairs configuration, were moved apart and then together again, the DCMD showed no preference for divergence compared with convergence of edges. A directional response was obtained by either making the lines increase in extent during divergence and decrease in extent during convergence; or by continually increasing the velocity of line movement during divergence and decreasing velocity during convergence. 4. The DCMD consistently gave a larger response to growing than to shrinking solid rectangular images. An increase compared with a decrease in the extent of edge in an image is, therefore, an important cue for the directionality of the response. For single moving edges of fixed extent, the neuron gave the largest response to edges that subtended 15 degrees at the eye. 5. The DCMD was very sensitive to the amount by which an edge traveled between frames on the display screen, with the largest responses generated by 2.5 degrees of travel. This implies that the neurons in the optic lobe that drive this movement-detecting system have receptive fields of about the same extent as a single ommatidium. 6. For edges moving up to 250 degree/s, the excitation of the DCMD increases with velocity. The response to an edge moving at a constant velocity adapts rapidly, in a manner that depends on velocity. Movement over one part of the retina can adapt the subsequent response to movement over another part of the retina. 7. For the DCMD to track and continue to respond to the image of an approaching object, the edges of the image must continually increase in velocity. This is the second important stimulus cue. 8. Edges of opposite contrasts (light-dark compared with dark-light) are processed in separate pathways that inhibit each other. This would contribute to the reduction of responses to wide-field movements.     

Responses of a looming-sensitive neuron to compound and paired object approaches

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.     

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 locust's 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.     

Arousal facilitates collision avoidance mediated by a looming sensitive visual neuron in a flying locust

Locusts have two large collision-detecting neurons, the descending contralateral movement detectors (DCMDs) that signal object approach and trigger evasive glides during flight. We sought to investigate whether vision for action, when the locust is in an aroused state rather than a passive viewer, significantly alters visual processing in this collision-detecting pathway. To do this we used two different approaches to determine how the arousal state of a locust affects the prolonged periods of high-frequency spikes typical of the DCMD response to approaching objects that trigger evasive glides. First, we manipulated arousal state in the locust by applying a brief mechanical stimulation to the hind leg; this type of change of state occurs when gregarious locusts accumulate in high-density swarms. Second, we examined DCMD responses during flight because flight produces a heightened physiological state of arousal in locusts. When arousal was induced by either method we found that the DCMD response recovered from a previously habituated state; that it followed object motion throughout approach; and--most important--that it was significantly more likely to generate the maintained spike frequencies capable of evoking gliding dives even with extremely short intervals (1.8 s) between approaches. Overall, tethered flying locusts responded to 41% of simulated approaching objects (sets of 6 with 1.8 s ISI). When we injected epinastine, the neuronal octopamine receptor antagonist, into the hemolymph responsiveness declined to 12%, suggesting that octopamine plays a significant role in maintaining responsiveness of the DCMD and the locust to visual stimuli during flight.     

Spatial distribution of inputs and local receptive field properties of a wide-field, looming sensitive neuron

The lobula giant movement detector (LGMD) in the locust visual system and its target neuron, the descending contralateral movement detector (DCMD), respond to approaching objects looming on a collision course with the animal. They thus provide a good model to study the cellular and network mechanisms underlying the sensitivity to this specific class of behaviorally relevant stimuli. We determined over an entire locust eye the density distribution of optical axes describing the spatial organization of local inputs to the visual system and compared it with the sensitivity distribution of the LGMD/DCMD to local motion stimuli. The density of optical axes peaks in the equatorial region of the frontal eye. Local motion sensitivity, however, peaks in the equatorial region of the caudolateral visual field and only correlates positively with the dorso-ventral density of optical axes. On local stimulation, both the velocity tuning and the response latency of the LGMD/DCMD depend on stimulus position within the visual field. Spatial and temporal integration experiments in which several local motion stimuli were activated either simultaneously or at fixed delays reveal that the LGMD processes local motion in a strongly sublinear way. Thus the neuron's integration properties seem to depend on several factors including its dendritic morphology, the local characteristics of afferent fiber inputs, and inhibition mediated by different pathways or by voltage-gated conductances. Our study shows that the selectivity of this looming sensitive neuron to approaching objects relies on more complex biophysical mechanisms than previously thought.     

Development of gaze tracking of small and large objects

A longitudinal study was designed to address the relationships between the smooth pursuit (SP) and the optokinetic response (OKR). Eye and head movements were measured in infants between 7 and 14 weeks of age. They were placed in front of a moving object subtending visual angles of 2.5, 5, 7, 14, 21, 28, and 35 degrees. The object oscillated sinusoidally along a horizontal path with a frequency of 0.25 Hz and an amplitude of +/-25 degrees visual angle. It was found that the number of saccades was dependent on object size: at 6 and 9 weeks of age there were more saccades for the smallest objects. With increasing age, the number of saccades decreased. The composite eye movement gain (smooth tracking + saccades) did not change with age but for the 6.5-week group the gain was higher for smaller objects. The gain of the smooth eye tracking increased with age and showed no dependency on object size. In conclusion, the results do not support the concept of two separate systems, the OKR and the SP, each of them processing eye tracking of small and large objects. Finally, it was observed that two infants at 6.5 weeks of age who used considerable head movements did not inhibit the vestibular-ocular response.     

Voluntary smooth eye movements with foveally stabilized targets

Summary We investigated the capacity of 6 humans to make voluntary smooth eye movements with a horizontally stabilized foveal point target. When the target was viewed on a dark field, all subjects were able to make smooth oscillatory eye movements when they attempted to imitate their own normal pursuit of sinusoidal target movement (0.2–0.7 Hz) directly preceding the stabilization on the fovea. The frequency of the imitating eye movement was in general lower than the frequency of normal pursuit by 2–35%. While fixating a foveally stabilized point target superimposed on a large, sinusoidally moving non-stabilized background, all subjects were able to make either no eye movements, eye movements nearly in phase with or eye movements nearly in counterphase with the background movement depending on the instruction to imagine the target as head-stationary, moving in phase, or moving in counterphase with the background. The accuracy of the frequency of the smooth eye movement with the stabilized target on the moving background was higher than during imitation of pursuit on the dark field but the precision of the frequency was lower than during normal pursuit. When the background moved pseudo-randomly all subjects could voluntarily inhibit their smooth eye movements or could make smooth eye movements in phase with the background. Only 2 subjects showed a limited ability to make smooth eye movements opposite to the pseudo-random background movement. The results suggest that with predictable background movement the volition of the subject rather than the movement of the background determines the eye movements when the subject looks at the foveally stabilized target.     

Visual motion due to eye movements helps guide the hand

Movement of the body, head, or eyes with respect to the world creates one of the most common yet complex situations in which the visuomotor system must localize objects. In this situation, vestibular, proprioceptive, and extra-retinal information contribute to accurate visuomotor control. The utility of retinal motion information, on the other hand, is questionable, since a single pattern of retinal motion can be produced by any number of head or eye movements. Here we investigated whether retinal motion during a smooth pursuit eye movement contributes to visuomotor control. When subjects pursued a moving object with their eyes and reached to the remembered location of a separate stationary target, the presence of a moving background significantly altered the endpoints of their reaching movements. A background that moved with the pursuit, creating a retinally stationary image (no retinal slip), caused the endpoints of the reaching movements to deviate in the direction of pursuit, overshooting the target. A physically stationary background pattern, however, producing retinal image motion opposite to the direction of pursuit, caused reaching movements to become more accurate. The results indicate that background retinal motion is used by the visuomotor system in the control of visually guided action.     

From following edges to pursuing objects

Primates can generate accurate, smooth eye-movement responses to moving target objects of arbitrary shape and size, even in the presence of complex backgrounds and/or the extraneous motion of non-target objects. Most previous studies of pursuit have simply used a spot moving over a featureless background as the target and have thus neglected critical issues associated with the general problem of recovering object motion. Visual psychophysicists and theoreticians have shown that, for arbitrary objects with multiple features at multiple orientations, object-motion estimation for perception is a complex, multi-staged, time-consuming process. To examine the temporal evolution of the motion signal driving pursuit, we recorded the tracking eye movements of human observers to moving line-figure diamonds. We found that pursuit is initially biased in the direction of the vector average of the motions of the diamond's line segments and gradually converges to the true object-motion direction with a time constant of approximately 90 ms. Furthermore, transient blanking of the target during steady-state pursuit induces a decrease in tracking speed, which, unlike pursuit initiation, is subsequently corrected without an initial direction bias. These results are inconsistent with current models in which pursuit is driven by retinal-slip error correction. They demonstrate that pursuit models must be revised to include a more complete visual afferent pathway, which computes, and to some extent latches on to, an accurate estimate of object direction over the first hundred milliseconds or so of motion.     

Time-dependent activation of feed-forward inhibition in a looming-sensitive neuron

The lobula giant movement detector (LGMD) is an identified neuron in the locust visual system that responds preferentially to objects approaching on a collision course with the animal. For such looming stimuli, the LGMD firing rate gradually increases, peaks, and decays toward the end of approach. The LGMD receives both excitatory and feed-forward inhibitory inputs on distinct branches of its dendritic tree, but little is known about the contribution of feed-forward inhibition to its response properties. We used picrotoxin, a chloride channel blocker, to selectively block feed-forward inhibition to the LGMD. We then computed differences in firing rate and membrane potential between control and picrotoxin conditions to study the activation of feed-forward inhibition. For looming stimuli, a significant activation of inhibition was observed early, as objects exceeded on average approximately 23 degrees in angular extent at the retina. Inhibition then increased in parallel with excitation over the remainder of approach trials. Experiments in which the final angular size of the approaching objects was systematically varied revealed that the relative activation of excitation and inhibition remains well balanced over most of the course of looming trials. Feed-forward inhibition actively contributed to the termination of the response to approaching objects and was particularly effective for large or slowly moving objects. Suddenly appearing and receding objects activated excitation and feed-forward inhibition nearly simultaneously, in contrast to looming stimuli. Under these conditions, the activation of excitation and feed-forward inhibition was weaker than for approaching objects, suggesting that both are preferentially tuned to approaching objects. These results support a phenomenological model of multiplication within the LGMD and provide new constraints for biophysical models of its responses to looming and receding stimuli.     

Role of an identified looming-sensitive neuron in triggering a flying locust's escape

Flying locusts perform a characteristic gliding dive in response to predator-sized stimuli looming from one side. These visual looming stimuli trigger trains of spikes in the descending contralateral movement detector (DCMD) neuron that increase in frequency as the stimulus gets nearer. Here we provide evidence that high-frequency (>150 Hz) DCMD spikes are involved in triggering the glide: the DCMD is the only excitatory input to a key gliding motor neuron during a loom; DCMD-mediated EPSPs only summate significantly in this motor neuron when they occur at >150 Hz; when a looming stimulus ceases approach prematurely, high-frequency DCMD spikes are removed from its response and the occurrence of gliding is reduced; and an axon important for glide triggering descends in the nerve cord contralateral to the eye detecting a looming stimulus, as the DCMD does. DCMD recordings from tethered flying locusts showed that glides follow high-frequency spikes in a DCMD, but analyses could not identify a feature of the DCMD response alone that was reliably associated with glides in all trials. This was because, for a glide to be triggered, the high-frequency spikes must be timed appropriately within the wingbeat cycle to coincide with wing elevation. We interpret this as flight-gating of the DCMD response resulting from rhythmic modulation of the flight motor neuron's membrane potential during flight. This means that the locust's escape behavior can vary in response to the same looming stimulus, meaning that a predator cannot exploit predictability in the locust's collision avoidance behavior.     

Observation of a finger or an object movement primes imitative responses differentially

Behavioural advantages for imitation of human movements over movements instructed by other visual stimuli are attributed to an 'action observation-execution matching' (AOEM) mechanism. Here, we demonstrate that priming/exogenous cueing with a videotaped finger movement stimulus (S1) produces specific congruency effects in reaction times (RTs) of imitative responses to a target movement (S2) at defined stimulus onset asynchronies (SOAs). When contrasted with a moving object at an SOA of 533 ms, only a human movement is capable of inducing an effect reminiscent of 'inhibition of return' (IOR), i.e. a significant advantage for imitation of a subsequent incongruent as compared to a congruent movement. When responses are primed by a finger movement at SOAs of 533 and 1,200 ms, inhibition of congruent or facilitation of incongruent responses, respectively, is stronger as compared to priming by a moving object. This pattern does not depend on whether S2 presents a finger movement or a moving object, thus effects cannot be attributed to visual similarity between S1 and S2. We propose that, whereas both priming by a finger movement and a moving object induces processes of spatial orienting, solely observation of a human movement activates AOEM. Thus, S1 immediately elicits an imitative response tendency. As an overt imitation of S1 is inadequate in the present setting, the response is inhibited which, in turn, modulates congruency effects.     

Responses of monkey nucleus of the optic tract neurons during pursuit and fixation.

We recorded 101 neurons in the nucleus of the optic tract (NOT) of 3 rhesus monkeys. The neurons were tested in a variety of oculomotor paradigms. This report focusses on the modulation of NOT neuronal activity during smooth pursuit eye movements. A small horizontally moving spot (less than 1 degrees) elicited a directionally specific response during fixation and revealed thereby the extent of the receptive fields. During pursuit NOT neurons are coding for target slip. If eye speed exceeds target speed the direction of retinal slip is reversed and in accordance with their directional sensitivity NOT neurons immediately change their activity. This result proves the slip transfer function as well as the independence from eye movement signals of NOT neurons. During pursuit across a structured background some neurons are still coding for target slip whereas other neurons are coding for background slip. These two groups of neurons can also be distinguished by their response during fixation. The response of a target slip neuron to a background movement is cancelled, whereas the response of a background neuron is not affected by fixation. There is no difference in size of receptive fields for these two groups of neurons. We conclude from our findings that directionally selective cells in the monkey NOT may provide input to the pursuit system as well as to the optokinetic system. This dichotomy may also be reflected in different efferent projections: to the nucleus reticularis tegmenti pontis and to the inferior olive, respectively. A similar notion was introduced by the late Maekawa for the rabbit's NOT.     

A comparison of visual responses to object- and ego-motion in the macaque superior temporal polysensory area

The responses of visual movement-sensitive neurons in the anterior superior temporal polysensory area (STPa) of monkeys were studied during object-motion, ego-motion and during both together. The majority of the cells responded only to the image of a moving object against a stationary background and failed to respond to the retinal movement of the same object (against the same background) caused by the monkey's ego-motion. All the tested cells continued responding to the object-motion during ego-motion in the opposite direction. By contrast, most cells failed to respond to the motion of an object when the observer and object moved at the same speed and direction (eliminating observer-relative motion cues). The results indicate that STPa cells compute motion relative to the observer and suggest an influence of reference signals (vestibular, somatosensory or retinal) in the discrimination of ego- and object-motion. The results extend observations indicating that STPa cells are selective for visual motion originating from the movements of external objects and unresponsive to retinal changes correlated with the observer's own movements.     

Grasping trapezoidal objects

When grasping rectangular or circular objects with a precision grip the digits close in on the object in opposite directions. In doing so the digits move perpendicular to the local surface orientation as they approach opposite sides of the object. This perpendicular approach is advantageous for accurately placing the digits. Trapezoidal objects have non-parallel surfaces so that moving the digits in opposite directions would make the digits approach the contact surfaces at an angle that is not 90°. In this study we examined whether this happens, or whether subjects tend to approach trapezoidal objects’ surfaces perpendicularly. We used objects of different sizes and with different surface slants. Subjects tended to approach the object’s surfaces orthogonally, suggesting that they aim for an optimal precision of digit placement rather than simply closing their hand as it reaches the object.     

Motion distorts visual space: shifting the perceived position of remote stationary objects

To perceive the relative positions of objects in the visual field, the visual system must assign locations to each stimulus. This assignment is determined by the object's retinal position, the direction of gaze, eye movements, and the motion of the object itself. Here we show that perceived location is also influenced by motion signals that originate in distant regions of the visual field. When a pair of stationary lines are flashed, straddling but not overlapping a rotating radial grating, the lines appear displaced in a direction consistent with that of the grating's motion, even when the lines are a substantial distance from the grating. The results indicate that motion's influence on position is not restricted to the moving object itself, and that even the positions of stationary objects are coded by mechanisms that receive input from motion-sensitive neurons.     

Functional properties of grasping-related neurons in the dorsal premotor area F2 of the macaque monkey

We investigated the properties of neurons located in the distal forelimb field of dorsal premotor area F2 of macaque monkey using a behavioral paradigm for studying the neuronal discharge during observation (object fixation condition) and grasping of different 3-dimensional objects with and without visual guidance of the movement (movement in light and movement in dark conditions, respectively). The main result is that almost all studied neurons were selective for both the type of prehension and the wrist orientation required for grasping an object. Three categories of neurons were found: purely motor, visually modulated, and visuomotor neurons. The discharge of purely motor neurons was not affected by either object presentation or by the visual feedback of the hand approaching to and interacting with the object. Visually modulated neurons presented a different discharge in the 2 movement conditions, this determining a decrease in selectivity for the grip and wrist orientation in the movement in dark condition. Visuomotor neurons typically discharged during the object fixation task even in the absence of any grasping movement. Nine of them also displayed a different discharge rate between the 2 movement conditions. Congruence was observed between the neuron response during the most effective type of prehension and the neuron response during observation of the object requiring that particular prehension. These results indicate an important role of F2 in the control of goal-related hand movements.     

Smooth pursuit eye movements elicited by somatosensory stimulation

Smooth pursuit eye movements approaching the qualitative and quantitative characteristics of those elicited by a moving visual target were obtained in complete darkness with a moving tactile stimulus. Pursuit eye movements in response to tactile stimulation have longer latencies to onset and to offset of pursuit, are more often interrupted by saccades, and provide less accurate stimulus localization than those in response to moving visual stimuli. The evocation of pursuit eye movements by a somatosensory input suggests that within the appropriate velocity domain a spatially changing sensory input from any modality may be sufficient to elicit ocular pursuit.     

Time to contact and the control of manual prehension

In the present study, a kinematic analysis was made of unconstrained, natural prehension movements directed toward an object approaching the observer on a conveyor belt at one of three constant velocities, from one of three different directions (head-on or along the fronto-parallel plane coming either from the subject′s left or right). Subjects were required to grasp the object when it reached a target located 20 cm directly in front of the hand′s start position. The kinematic analysis revealed that both the transport and grasp components of the movement changed in response to the experimental manipulations, but did so in a manner that guaranteed that, for objects approaching from a given direction, hand closure would begin at a constant time prior to object contact (regardless of the object’s approach speed). The kinematic analysis also revealed, however, that the onset of hand closure began earlier with objects approaching from the right than from other directions – an effect which would not be predicted if time to contact was the key variable controlling the onset of hand closure. These results, then, lend only partial support to the theory that temporal coordination between the transport and grasp components of prehension is ensured through their common dependence on time to contact information. Received: 20 September 1996 / Accepted: 16 June 1997     

Speed quantification and tracking of moving objects in adaptive optics scanning laser ophthalmoscopy

Microscopic features of the human retina can be resolved noninvasively using an adaptive optics scanning laser ophthalmoscope (AOSLO). We describe an improved method to track and quantify the speed of moving objects in AOSLO videos, which is necessary for characterizing the hemodynamics of retinal capillaries. During video acquisition, the objects of interest are in constant motion relative to the background tissue (object motion). The background tissue is in constant motion relative to the AOSLO, due to continuous eye motion during video recordings (eye motion). The location at which AOSLO acquires data is also in continuous motion, since the imaging source is swept in a raster scan across the retina (raster scanning). We show that it is important to take into consideration the combination of object motion, eye motion, and raster scanning for accurate quantification of object speeds. The proposed methods performed well on both experimental AOSLO videos as well as synthetic videos generated by a virtual AOSLO. These methods improve the accuracy of methods to investigate hemodynamics using AOSLO imaging.