Head Saccades Research Articles

Chapter 35 Immediate saccadic substitution for deficits in dynamic vestibular reflexes of frogs with selective peripheral lesions

Immediately after the section of one horizontal canal nerve compensatory head movements in the horizontal plane are unidirectional in the dark but symmetrical in amplitude in the light. Responses towards the ‘weak’ (intact) side are saccadic. These head saccades are accompanied by smaller ocular quick phases in the opposite direction. Both head saccades and ocular quick phases are still present even after a bilateral section of the horizontal canal nerves or after removal of both labyrinths. The main sequences of eye-head quick phases and of head saccades are very similar in intact and bilaterally lesioned frogs, indicating that vestibulo-ocular and vestibulocollic reflexes must be suppressed during these fast head movements. The occurrence of these head saccades depends on head-velocity-related proprioceptive signals. This input is facilitated after section of the horizontal canal nerve. Head saccades supplement weak but unaltered optokinetic reflexes at higher frequencies to an extent that compensatory head movements in response to sinusoidal table oscillations are symmetrical in spite of acute unilateral reflex deficits. In some of the chronic hemilabyrinthectomized frogs the vestibulocollic reflexes recovered to an extent that the head slow phase was fast enough to trigger head saccades even in the dark.

The role of compensatory eye and head movements for gaze stabilization in the unrestrained frog

Compensatory eye, head and gaze movements of unrestrained frogs were recorded simultaneously in response to table movements in the light. Passive displacement was compensated with a gain between 0.55 and 0.85, depending on stimulus amplitude. At small stimulus amplitudes gaze was stabilized exclusively by compensatory eye movements. At larger stimulus amplitudes compensatory head movements contributed up to 80% gaze stabilization. The contribution of compensatory eye movements became increasingly more restricted to those brief transient periods, at which head velocity changed only slowly in response to a change in stimulus direction or velocity. The wave forms of both eye and head movements exhibited characteris and complementary distortions. Their combination, the gaze wave form compensated almost exactly in phase for the imposed passive displacement in space. Head saccades of small amplitude were rather well compensated by fast eye movements in the opposite direction, with the result that the combined gaze movement was smooth. The occurrence of these compensatory fast eye movements depended neither upon the function of the labyrinthine organs nor upon retinal image slip.

The accuracy of head saccades under monaural and binaural listening conditions

Literature examining head motion and auditory function has typically focused upon whether changes in position facilitate auditory spatial performance. The present experiment addresses the reverse of this question by attempting to quantify the spatial characteristics of the head saccade itself, in the context of various localization tasks. Horizontal head position was measured every 16 ms as both binaural and monaural listeners turned to face a sound source located along an arc of + or −60 deg azimuth. The signals were 0.5‐, 2.0‐, and 3.7‐kHz tones presented at 40 dB SPL. Both single pulse and pulse train conditions were employed. Resolution was best with speakers near the subjects median plane for binaural conditions, and on the side opposite the occluded ear in monaural conditions. Precision of the final head position could be predicted by the frequency used. The current results follow known auditory spatial functions and support the 81‐year‐old hypothesis that while binaural localization is superior to monaural, given the opportunity to move one's head in the presence of an ongoing acoustic signal, monaural listeners may still be quite accurate. [Work supported by NIH.]

Lobula plate and ocellar interneurons converge onto a cluster of descending neurons leading to neck and leg motor neuropil in Calliphora erythrocephala

In the fly, Calliphora erythrocephala, a cluster of three Y-shaped descending neurons (DNOVS 1–3) receives ocellar interneuron and vertical cell (VS4–9) terminals. Synaptic connections to one of them (DNOVS 1) are described. In addition, three types of small lobula plate vertical cell (sVS) and one type of contralateral horizontal neuron (Hc) terminate at DNOVS 1, as do two forms of ascending neurons derived from thoracic ganglia. A contralateral neuron, with terminals in the opposite lobula plate, arises at the DNOVS cluster and is thought to provide heterolateral interaction between the VS4–9 output of one side to the VS4–9 dendrites of the other. DNOVS 2 and 3 extend through pro-, meso-, and metathoracic ganglia, branching ipsilaterally within their tract and into the inner margin of leg motor neuropil of each ganglion. DNOVS 1 terminates as a stubby ending in the dorsal prothoracic ganglion onto the main dendritic trunks of neck muscle motor neurons. Convergence of VS and ocellar interneurons to DNOVS 1 comprises a second pathway from the visual system to the neck motor, the other being carried by motor neurons arising in the brain. Their significance for saccadic head movement and the stabilization of the retinal image is discussed.

Saccadic head movements of the praying mantis, with particular reference to visual and proprioceptive information

ABSTRACT. Horizontal head movements of the praying mantis, Sphodromantis lineola Burm., were recorded continuously. They responded to the presence of a live blowfly prey in the antero‐lateral visual field with a rapid saccadic head movement. The angular movement of a fixation saccade was correlated positively to the displacement of the prey from the prothoracic midline. Saccade magnitude and velocity are related. After the stimulus moved out of the visual field, the mantis made a second saccadic head movement, a return saccade towards the body midline. We observed return saccades in which the head overshot or undershot the body midline, as well as saccades which returned the head exactly to its initial position. In 92% of trials with intact mantids, the return movement succeeded eventually in rotating the head back to its initial position, whereas after removal of the neck hair plates this occurred in only 47% of trials. There is a consistent relation between saccade extent and velocity. Velocities of return saccades were slower than those of fixation saccades. It is suggested that sensory inputs from the neck hair plate proprioceptors modify both the magnitude and the angular velocity of fixation and return saccadic head movements.

Foveal fixation and tracking in the praying mantis

1. Visually guided head and body movements of restrained and freely moving mantids (Tenodera australasiae) have been studied by means of closed circuit television. Interest was concentrated on the different roles of the fovea and the periphery of the eye in controlling visuo-motor behaviour. 2. The peripheral eye is mainly responsible for the detection of novel objects (preferably potential prey) and the generation of ballistic (open-loop) saccadic head movements (Fig. 2) which bring the target image to the fovea (Figs. 3, 4, 5, 6). 3. Measurements on monocular animals show that the fovea ofeach eye is encircled by a saccade sensitive periphery (Figs. 5, 6). In other words each eye is capable of measuring any retinal position of the target image in a coordinate system whose origin is at the fovea. Based on this finding, a hypothesis, which is outlined in Sect. IV.7, suggests that the binocular coordination during fixation, tracking and distance estimation is based on the comparison of angular coordinates extracted by each eye from the position vector of the target. 4. Moving targets which have been fixated are held in the fovea either by smooth or saccadic tracking eye movements. The degree to which either tracking strategy is employed depends mainly on the features of the background, but to some extent also on the velocity of the target. 5. Targets which move against a homogeneous background are tracked by smooth eye movements (Fig. 7). Low target angular velocities are closely matched by the eye velocity. At high target speeds the head lags increasingly behind the target and saccades are periodically required to reduce the position error relative to the fovea. 6. Smooth pursuit eye movements, evoked either by a single target (Fig. 7) or a disrupted background (Fig. 8), are affected primarily by the velocity of the retinal image. While the effects of target and background are similar in this respect, they differ in others. Small objects in the foreground, subtending an angle of only a few degrees on the retina, evoke strong pursuit responses only when they resemble typical prey and project onto the fovea (Fig. 9). On the other hand, the image stabilisation of the background is a stereotyped response that can be evoked whenever a large part of the background moves across the visual field (Fig. 10a). Moreover, responses caused by a moving target in the fovea, and movements of the background in the periphery, are not combined additively (Fig. 10b). The foveal tracking response is weighted more strongly, but because the target is usually small, compared with the background, competing background motion can suppress smooth foveal tracking almost completely. 7. This limitation imposed upon the smooth pursuit system by the presence of a disrupted background (either a stripe pattern in the experimental set-up or grass and other plants in a natural setting) is avoided by the adoption of a strategy of saccadic tracking (Figs. 11, 12, 15, 16). This also applies for the tracking which immediately precedes the catching of prey (Fig. 15). Therefore, the stabilisation of the target image in place on the fovea is not a prerequisite for a successful strike. 8. Up to target angular velocities of about 100 °/s, saccadic tracking is predictive, i.e. the saccades have adequate amplitudes to bring the fovea right on target at the instant the saccade is completed (Fig. 13). This implies that the saccadic system processes not only position information of the target but velocity information as well. It is suggested that this velocity information is provided by the smooth pursuit system. Saccadic tracking would then reflect interactions of two circuits, the velocity coding circuit which in the presence of a homogeneous background also generates smooth pursuit head movements, and the position coding circuit which in the absence of target movement is able to generate saccades on its own.

Sound localization by the barn owl (Tyto alba) measured with the search coil technique

The dynamics and accuracy of sound localization by the barn owl (Tyto alba) were studied by exploiting the natural head-orienting response of the owl to novel sound stimuli. Head orientation and movement were measured using an adaptation of the search coil technique which provided continuous high resolution azimuthal and elevational information during the behavior. The owls responded to sound sources with a quick, stereotyped head saccade; the median latency of the response was 100 ms, and its maximum angular velocity was 790°/s. The head saccade terminated at a fixation point which was used to quantify the owl's sound localization accuracy. When the sound target was located frontally, the owl's localization error was less than 2° in azimuth and elevation. This accuracy is superior to that of all terrestrial animals tested to date, including man. When the owls were performing open-loop localization (stimulus off before response begins), their localization errors increased as the angular distance to the target increased. Under closed-loop conditions (stimulus on throughout response), the owls again committed their smallest errors when localizing frontal targets, but their errors increased only out to target angles of 30°. At target angles greater than 30°, the owl's localization errors were independent of target location. The owl possesses a frontal region wherein its auditory system has maximum angular acuity. This region is coincident with the owl's visual axis.

Saccadic head movements in mantids

1. Mantids visually orient to prey objects by means of rapid saccadic head movements which serve to image the target on the anterior regions of the large compound eyes. Small stationary flashes of light subtending 30′ of arc were used to elicit head movements. The topography of the saccade was studied by photographic and optoelectronic analysis. 2. High speed photography was utilized to study the temporal properties of individual saccades. The latency of the response ranged from a minimum of 0.15 s to a maximum of 1.0 s. Maximum angular velocities of 400 deg/s were achieved with large amplitude saccades. 3. Single stationary flashes produced saccades with latencies ranging from 0.30 to 1.0 s. When a saccade was not elicited by a single flash, a subsequent flash in an area 1.8° removed from the first would often evoke a response. The saccades produced by such multiple flashes yielded latency values ranging from 0.15 to 0.30 s. It, therefore, appears that a single stationary flash may potentiate the effects of subsequent stimulation. 4. The head orientation following a saccade is linearly related to the position of the stimulus. As previously described by Mittelstaedt (1957), the slope of the function relating head position to stimulus angle is less than unity. Slope values ranging from 0.65 to 0.83 were obtained in this study. 5. Orientation is dependent on the direction of the head movement. Large amplitude saccades directed laterally to a given stimulus location produce final head orientations which differ from those produced by saccades elicited to the same location but from the opposite direction. 6. For saccades proceeding in the same direction, final head orientation is independent of prior head orientation. 7. Visual feedback is unimportant in determining the final head position. Saccades elicited by stimuli whose duration was shorter than the mantid's reaction time produced the same final head angle as those saccades elicited by long duration stimuli. 8. After an initial large amplitude saccade was elicited, a small amplitude correction saccade often could be obtained by a second flash in the same location. Correction saccades were equally likely to occur following saccades elicited by long duration stimuli or short duration stimuli. Since reorienting saccades did occur following initial saccades produced by long duration stimuli, it must be concluded that visual feedback is not utilized to “home-inon” the target.