Eye contact and arousal: the effects of stimulus duration

The present study investigated the effect of stimulus duration on skin conductance responses (SCRs) evoked by different gaze directions of a live person. In two separate parts of the experiment, either two fixed stimulus durations (2 s and 5 s) or a participant-controlled stimulus duration was used. The results showed that the eye contact evoked enhanced SCRs compared to averted gaze or closed eyes conditions irrespective of the presentation time. Subjective evaluations of approach-avoidance-tendencies indicated that the direct gaze elicited either approach or avoidance, depending on the participant. Participants who had evaluated a direct gaze-condition as approachable were found to be more emotionally stabile than those who had evaluated the same condition as avoidable. In the self-timing condition, averted gaze was looked at longer than direct gaze. Our results suggest that direct gaze, also when encountered only briefly like in every-day social encounterings, increases autonomic sympathetic arousal.     

Vestibular and non-vestibular contributions to eye movements that compensate for head rotations during viewing of near targets

Geometry dictates that when subjects view a near target during head rotation the eyes must rotate more than the head. The relative contribution to this compensatory response by adjustment of the vestibulo-ocular reflex gain (Gvor), visual tracking mechanisms including prediction, and convergence is debated. We studied horizontal eye movements induced by sinusoidal 0.2–2.8 Hz, en-bloc yaw rotation as ten normal humans viewed a near target that was either earth-fixed (EFT) or head-fixed (HFT). For EFT, group median gain was 1.49 at 0.2 Hz declining to 1.08 at 2.8 Hz. For HFT, group median gain was 0.03 at 0.2 Hz increasing to 0.71 at 2.8 Hz. By applying transient head perturbations (peak acceleration >1,000° s^–2) during sinusoidal rotation, we determined that Gvor was similar during either EFT or HFT conditions, and contributed only ~75% to the compensatory response. We confirmed that retinal image slip contributed to the compensatory response by demonstrating reduced gain during EFT viewing under strobe illumination. Gain also declined during sum-of-sines head rotations, confirming the contribution of predictive mechanisms. The gain of compensatory eye movements was similar during monocular or binocular viewing, although vergence angle was greater during binocular viewing. Comparison with previous studies indicates that mechanisms for generation of eye rotations during near viewing depend on head stimulus type (rotation or translation), waveform (transient or sinusoidal), and the species being tested.     

Single unit activity in the frontal eye fields of unanesthetized monkeys during eye and head movement

Summary Single unit activity in the frontal eye field was investigated in unanesthetized monkeys during eye and head movement. Two types of cells (I and II) were found. Type I fired during voluntary saccadic movement occuring in a given direction and also during the fast phase of optokinetic and vestibular nystagmus. Cells of this type were silent during smooth pursuit movement and the slow phase of nystagmus. It was found that the firing pattern of Type I cells was maintained irrespective of head movement.Type II cells fired during smooth pursuit eye movements and the slow phase of nystagmus; these units displayed a steady discharge when the eyes were oriented in a specific position. Also this type of cell maintained its characteristic discharge during head movement. A separate population of frontal eye field cells was found to be exclusively related to head turning.     

Task-dependent effects of social attention on saccadic reaction times

Previous research has shown that saccadic reaction times (SRTs) are shorter when a stimulus is flashed on the same side as the observed gaze direction of another individual. The gaze imitation hypothesis contends that observed gaze evokes the preparation of a saccade toward the same direction. Previous studies of this phenomenon have employed pro-saccade tasks in which the instructed saccade is directed toward the stimulus. In agreement with previous findings, we found that SRTs on pro-saccade trials were shorter when the stimulus appeared in the same direction as observed gaze. Here we also included anti-saccade trials in which subjects were required to look-away from a stimulus and toward its mirror position in the opposite visual field. The gaze imitation hypothesis predicts that subjects will have shorter SRTs on anti-saccade trials in which the stimulus appears opposite the observed gaze direction because they will have prepared already a saccade in that direction. However, contrary to the prediction of the gaze imitation hypothesis, we found that subjects had shorter SRTs on anti-saccade trials when the stimulus appeared in the same direction as observed gaze. Moreover, subjects also made more pro-saccade errors on anti-saccade trials in which the stimulus was presented opposite the observed gaze direction. The results of our study indicate that subjects prepared a saccade in the same direction as observed gaze on pro-saccade trials but opposite the observed gaze direction on anti-saccade trials. These findings suggest that the effect of social gaze cues on SRTs is task dependent.     

Correlates of motor planning and postsaccadic fixation in the macaque monkey lateral geniculate nucleus

There is significant controversy regarding the ability of the primate visual system to construct stable percepts from a never-ending stream of brief fixations and rapid saccadic eye movements. In this study, we examined the timing and occurrence of perisaccadic modulation of LGN single-unit activity in awake-behaving macaque monkeys while they made spontaneous saccades in the dark and made visually guided saccades to discrete stimuli located outside the receptive field. Our hypothesis was that the activity of LGN cells is modulated by efference copies of motor plans to produce saccadic eye movements and that this modulation depends neither on the presence of feedforward visual information nor on a corollary discharge of signals directing saccadic eye movements. On average, 25% of LGN cells demonstrated significant perisaccadic modulation. This modulation consisted of a moderate suppression of activity that began more than 100 ms prior to the initiation of a saccadic eye movement and continued beyond the termination of the saccadic eye movement. This suppression was followed by a large enhancement of activity after the eyes arrived at the next fixation. Although members of all three LGN relay cell classes (magnocellular, parvocellular, and koniocellular) demonstrated significant saccade-related suppression and enhancement of activity, more cells demonstrated postsaccadic enhancement (25%) than perisaccadic suppression (17%). In no case did the timing of the modulation coincide directly with saccade duration. The degree of modulation observed did not vary with LGN cell class, LGN receptive field center location, center sign (ON-center or OFF-center), or saccade latency or velocity. The time course of modulation did, however, vary with saccade size such that suppression was longer for longer saccades. The fact that activity from a percentage of LGN cells from all cell classes was modulated in relationship to saccadic eye movements in the absence of direct visual stimulation suggests that this modulation is a general phenomenon not tied to specific types of visual stimuli. Similarly, because the onset of the modulation preceded eye movements by more than 100 ms, it is likely that this modulation reflects higher order motor-planning rather than a corollary of mechanisms in direct control of eye movements themselves. Finally, the fact that the largest modulation is a postsaccadic enhancement of activity may suggest that perisaccadic modulations are designed more for the facilitation of visual information processing once the eyes land at a new location than for filtering unwanted visual stimuli.     

Vestibular guidance of active head movements

Vestibular sensors provide precise and timely information about head velocity in space. It is well established that this information is used to stabilize eyes, head and body against movements from outside, i.e., passive movements. Here, we investigate whether vestibular information also helps to monitor and guide active head movements during gaze shifts. We measured head movements during large gaze shifts toward briefly flashed targets in humans with complete vestibular loss (vestibular subjects) and in healthy controls before and after increasing their head moment of inertia. Whereas normally head movements oscillate neither in vestibular subjects nor in controls, the increase in head moment of inertia caused marked head oscillations only in vestibular subjects. We conclude that vestibular information plays an important role in the on-line guidance of active head movements and helps to correct for unexpected changes such as additional torque imposed by an increase in moment of inertia.     

Cell responses to vertical and horizontal retinal disparities in the monkey visual cortex

Because of the horizontal separation of both ocular globes, the projection angles are slightly different. These differences are commonly termed retinal disparities. Vertical and horizontal retinal disparities occur constantly in normal life. We have investigated the responses of single cells in cortical areas V1 and V2 of behaving Macaca mulatta monkeys to retinal disparities by using dynamic random dot stereograms. Our findings show that cortical visual cells are sensitive to both vertical and horizontal disparities. To calculate the distance between two objects in a three-dimensional space from horizontal disparities, it is necessary to know the fixation distance. It has been suggested that the horizontal gradient of vertical disparity contains information to estimate the fixation distance and therefore to scale horizontal disparities. We suggest that these cells sensitive to horizontal and vertical disparities represent a neural mechanism that provides information to the visual system in order to achieve a correct eye alignment and depth perception.     

Organization of the neurons of origin of the descending pathways from the ferret superior colliculus

The superior colliculus (SC), through its descending projections to the brainstem and spinal cord, is involved in initiating sensory-driven orienting behaviors. Ferrets are carnivores that hunt both above and below ground using visual (and auditory) cues in the daylight but non-visual cues in darkness and in subterranean environments. The present investigation sought to determine whether the ferret SC shows organizational features similar to those found in other visually dominant animals (e.g. cats), or whether characteristics of colliculi from non-visually dominant animals (e.g. rodents) prevail. Injection of retrograde tracer into the identified targets of the colliculus (cervical spinal cord, the contralateral pontomedullary reticular formation, or the ipsilateral pontine reticular formation) labeled tectospinal, crossed tectoreticular, and ipsilateral tectoreticular neurons, respectively, within the adult ferret SC. Labeled tectospinal and crossed tectoreticular neurons were far outnumbered by neurons with ipsilateral reticular projections. Like those of their visually dominant relatives, ferret tectospinal neurons were well represented throughout the anterior-posterior extent of the SC and crossed tectoreticular neurons tended to be distributed more broadly across the intermediate gray layer than those of rodents. Thus, even though ferrets perform well as subterranean predators where non-visual cues initiate orienting behaviors, these anatomical characteristics indicate that their colliculi are organized similar to that of their visually dominant, carnivorous relatives.     

Velocity characteristics of smooth pursuit eye movements to different patterns of target motion

Summary Horizontal smooth pursuit eye movements were recorded in normal subjects in response to different patterns of target motion that was either periodic or not. Periodic patterns were triangular and sinusoidal waves. Non-periodic patterns were ramps with either constant or sinusoidally varying velocity. In both cases, several different amplitudes and peak velocities were considered. The experimental results indicate that (a) the performance of the smooth pursuit system depends on the spatio-temporal characteristics of target motion, (b) the relationship between smooth pursuit eye velocity and target velocity during the tracking of constant velocity ramps is strongly nonlinear with a saturation depending on the amplitude of target excursion, (c) in the remaining experimental conditions, there is a linear behaviour up to target velocities of 75 deg/s with a gain of about 0.9.     

Occipital Alpha Activity as a Measure of Retinal Involvement in Oculomotor Control

Two experiments were carried out to test the hypothesis that a reduction of alpha energy in the occipital EEG reflects an increased dependency of oculomotor control on retinal feedback. In an ocular pursuit task subjects followed a target with their eyes. The target either moved in a repetitive, predictable pattern or varied unpredictably. Subjects were instructed to minimize eye-tracking errors during the task, and performance feedback was provided. Oculomotor control depends on retinal feedback during on-target performance in the unpredictable condition and during error correction in both conditions. However, subjects' on-target performance in the predictable condition may involve some degree of automatic control, which is less dependent on retinal feedback. As expected, alpha activity was maximal in this condition. In a second experiment, alpha activity was shown not to reflect impaired information processing, since here again alpha was greatest during correct on-target performance in the predictable condition, while reaction times (to visual stimuli presented in the moving target) were shortest in this condition and appeared to be independent of the amount of alpha during stimulus presentation.     

Response of cat retinal ganglion cells to motion of visual texture

Summary Responses of retinal ganglion cells to motion of large fields of visual texture were recorded in the lightly anaesthetised, immobilized cat. Brisk sustained and brisk transient, on- or off-centre, units gave a modulated response to texture motion. The pattern of temporal modulation of the response was dependent upon the particular configuration (sample) of texture crossing the receptive field. The magnitude of the response depended on the size of the receptive field centre. For all units, whether sustained or transient the magnitude of response to a textured field of fixed angular subtense declined as centre-diameter increased from 0.9 deg. For brisk units the response magnitude levelled off for centre sizes smaller than 0.9 deg. Responses to texture were confined spatially to the region of the receptive field, and the overall characteristics of this response were due to interactions between the centre and surround mechanisms of the receptive field. In brisk transient units, no evoked response was evident when texture motion was confined to regions well away from the receptive field of the unit, i.e. no periphery or shift effect could be demonstrated. The results support previous suggestions that the differential sensitivity to texture motion evident in cortical neurones must be due to intra-cortical processing.Supported by Project Grant G978/558/N from the Medical Research Council     

Listing's law for eye,head and arm movements and their synergistic control

Summary We have recorded eye, head, and upper arm rotations in five healthy human subjects using the three-dimensional search coil technique. Our measurements show that the coordination of eye and head movements during gaze shifts within ± 25 deg relative to the forward direction is organized by restricting the rotatory trajectories of the two systems to almost parallel planes. These so-called Listing planes for eye-in-space and head-in-space rotations are workspace-oriented, not body-fixed. Eye and head trajectories in their respective planes are closely related in direction and amplitude. For pointing or grasping, the rotatory trajectories of the arm are also restricted to a workspace-oriented Listing plane. During visually guided movements, arm follows gaze, and the nine-dimensional rotatory configuration space for eye-head-arm-synergies (three degrees of freedom for each system) is reduced to a two-dimensional plane in the space of quaternion vectors.     

Gaze displacement and inter-segmental coordination during large whole body voluntary rotations

Displacements of the visual axis and multi-segmental (eye-to-foot) coordination in the yaw plane were studied in ten human subjects (Ss) during voluntary reorientations to illuminated targets of eccentricities up to 180°. We also investigated how knowledge of target location modifies the movement pattern. Eccentric targets (outbound trials) elicited eye, head, trunk and foot movements at latencies ca. 0.5, 0.6, 0.7 and 1.1 s, respectively. Knowledge of target location (return trials) reduced latencies for foot and trunk (but not eye and head) thus eye, head and trunk moved more en bloc. In most trials, the initial gaze shift fell short of the target and more than 50% of the visual angle was covered by the sum of vestibular nystagmic fast phases and head-in-space displacement, until target fixation. This indicates that during large gaze shifts the ‘anticompensatory’ role of the vestibulo-ocular reflex in target acquisition is prominent. During some predictable trials Ss acquired targets with a single large gaze shift, shortening target acquisition time by more than 200 ms. In these, gaze velocity (trunk-in-space + head-on-trunk + eye-in-orbit) remained often fairly constant for durations of up to 500 ms, suggesting that gaze velocity is a controlled parameter. Such pattern occurred during trunk mobilization, thus eye velocity co-varied with head-in-space rather than head-on-trunk velocity. Foot rotations were stereotyped and of constant frequency, suggesting they are generated by locomotor pattern generators. However, knowledge of target location reduced foot latencies indicating that local and supraspinal mechanisms interact for foot control. We propose that a single controller is responsible for the coupling of the multiple body segments and gaze velocity control during gaze shifts.     

Perceiving a stable world during active rotational and translational head movements

When a person moves through the world, the associated visual displacement of the environment in the opposite direction is not usually seen as external movement but rather as a changing view of a stable world. We measured the amount of visual motion that can be tolerated as compatible with the perception of moving within a stable world during active, sinusoidal, translational and rotational head movement. Head movements were monitored by means of a low-latency, mechanical head tracker and the information was used to update a helmet-mounted visual display. A variable gain was introduced between the head tracker and the display. Ten subjects adjusted this gain until the visual display appeared stable during sinusoidal yaw, pitch and roll head rotations and naso-occipital, inter-aural and dorso-ventral translations at 0.5 Hz. Each head movement was tested with movement either orthogonal to or parallel with gravity. A wide spread of gains was accepted as stable (0.8 to 1.4 for rotation and 1.1 to 1.8 for translation). The gain most likely to be perceived as stable was greater than that required by the geometry (1.2 for rotation; 1.4 for translation). For rotational motion, the mean gains were the same for all axes. For translation there was no effect of whether the movement was inter-aural (mean gain 1.6) or dorso-ventral (mean gain 1.5) and no effect of the relative orientation of the translation direction relative to gravity. However translation in the naso-occipital direction was associated with more closely veridical settings (mean gain 1.1) and narrower standard deviations than in other directions. These findings are discussed in terms of visual and non-visual contributions to the perception of an earth-stable environment during active head movement.     

Visual signals contribute to the coding of gaze direction

Accurate information about gaze direction is required to direct the hand towards visual objects in the environment. In the present experiments, we tested whether retinal inputs affect the accuracy with which healthy subjects indicate their gaze direction with the unseen index finger after voluntary saccadic eye movements. In experiment 1, subjects produced a series of back and forth saccades (about eight) of self-selected magnitudes before positioning the eyes in a self-chosen direction to the right. The saccades were produced while facing one of four possible visual scenes: (1) complete darkness, (2) a scene composed of a single light-emitting diode (LED) located at 18 degrees to the right, (3) a visually enriched scene made up of three LEDs located at 0 degrees, 18 degrees and 36 degrees to the right, or (4) a normally illuminated scene where the lights in the experimental room were turned on. Subjects were then asked to indicate their gaze direction with their unseen index finger. In the conditions where the visual scenes were composed of LEDs, subjects were instructed to foveate or not foveate one of the LEDs with their last saccade. It was therefore possible to compare subjects' accuracy when pointing in the direction of their gaze in conditions with and without foveal stimulation. The results showed that the accuracy of the pointing movements decreased when subjects produced their saccades in a dark environment or in the presence of a single LED compared to when the saccades were generated in richer visual environments. Visual stimulation of the fovea did not increase subjects' accuracy when pointing in the direction of their gaze compared to conditions where there was only stimulation of the peripheral retina. Experiment 2 tested how the retinal signals could contribute to the coding of eye position after saccadic eye movements. More specifically, we tested whether the shift in the retinal image of the environment during the saccades provided information about the reached position of the eyes. Subjects produced their series of saccades while facing a visual environment made up of three LEDs. In some trials, the whole visual scene was displaced either 4.5 degrees to the left or 3 degrees to the right during the primary saccade. These displacements created mismatches between the shift of the retinal image of the environment and the extent of gaze deviation. The displacements of the visual scene were not perceived by the subjects because they occurred near the peak velocity of the saccade (saccadic suppression phenomenon). Pointing accuracy was not affected by the unperceived shifts of the visual scene. The results of these experiments suggest that the arm motor system receives more precise information about gaze direction when there is retinal stimulation than when there is none. They also suggest that the most relevant factor in defining gaze direction is not the retinal locus of the visual stimulation (that is peripheral or foveal) but rather the amount of visual information. Finally, the results suggest an enhanced egocentric encoding of gaze direction by the retinal inputs and do not support a retinotopic model for encoding gaze direction.     

Involvement of the head and trunk during gaze reorientation during standing and treadmill walking

As individuals stand or walk in an environment their gaze may be reoriented from one location to another in response to auditory or visual stimuli. In order to reorient gaze, the eyes and/or the head and trunk must rotate. However, what determines the exact degree of rotation of each segment while standing or walking is not fully understood. In the current study we show that when participants were asked to reorient their gaze towards light cues positioned at eccentric locations of up to 90° while standing or walking on a treadmill their eyes and head mainly facilitated the action. Rotations of the head-in-space were similar for both tasks, but the rotation of the shoulders- and hips-in-space were lower for the treadmill walking condition. It is argued that this difference in the level of head-on-trunk rotation during the two tasks is controlled by the vestibular feedback loop. The regulation of this feedback loop is performed by the cerebellum in response to the level of threat to postural stability.     

The influence of stimulus direction and eccentricity on pro- and anti-saccades in humans

We examined the sensory and motor influences of stimulus eccentricity and direction on saccadic reaction times (SRTs), direction-of-movement errors, and saccade amplitude for stimulus-driven (prosaccade) and volitional (antisaccade) oculomotor responses in humans. Stimuli were presented at five eccentricities, ranging from 0.5° to 8°, and in eight radial directions around a central fixation point. At 0.5° eccentricity, participants showed delayed SRT and increased direction-of-movement errors consistent with misidentification of the target and fixation points. For the remaining eccentricities, horizontal saccades had shorter mean SRT than vertical saccades. Stimuli in the upper visual field trigger overt shifts in gaze more easily and faster than in the lower visual field: prosaccades to the upper hemifield had shorter SRT than to the lower hemifield, and more anti-saccade direction-of-movement errors were made into the upper hemifield. With the exception of the 0.5° stimuli, SRT was independent of eccentricity. Saccade amplitude was dependent on target eccentricity for prosaccades, but not for antisaccades within the range we tested. Performance matched behavioral measures described previously for monkeys performing the same tasks, confirming that the monkey is a good model for the human oculomotor function. We conclude that an upper hemifield bias lead to a decrease in SRT and an increase in direction errors.     

Human gaze shifts in which head and eyes are not initially aligned

Most studies of rapid orienting gaze shifts generated by combined eye and head movements have focused on an experimental condition in which gaze displacements are started with the subject's eyes in the normal straight-ahead position in the orbit. Such an experimental approach does not permit a clear identification of the input signal to the head motor system, because target offset angle is the same for both the eye and head. We have studied gaze shifts in human subjects which began with the visual axis straight ahead relative to the body (i.e., gaze or line of sight aligned with body sagittal plane) and with head offset from straight ahead at various angular positions. In our experimental conditions, the amplitude of head movement during a gaze shift was nearly equal to the angular distance between the target position and the starting head position (target-re-head), even though subjects were not specifically instructed to move their heads. This observation contrasts with other published reports in the literature showing considerable varibility amongst subjects in the amplitude of head rotation within a given task and between tasks. The difference may be related to the initial conditions which required subjects to align the eye and head on specific starting targets, since others have shown that requiring head alignment enhances head displacement. The amplitude of the saccadic eye movement was not determined by either the target's position relative to the starting eye or head positions. The value that best described the eye movement amplitude was the eye position in the orbit at the end of the saccade. This was nearly equal to target-rehead until a saturation eye position in the orbit was attained.     

Optokinetic nystagmus and afternystagmus in human beings: relationship to nonlinear processing of information about retinal slip

Summary In four normal human subjects we measured eye movements during full-field optokinetic stimulation (10–220 deg/s) and determined the relationship among retinal-slip velocity (drum velocity minus slow-phase eye velocity), the slow-phase velocity of optokinetic nystagmus (OKN) and the initial value of the slow-phase velocity of optokinetic afternystagmus (OKAN) measured in darkness. OKN and OKAN were maximum (63–84 and 11–19 deg/s, respectively) when retinal slip ranged from 30–100 deg/s. For higher values of retinal slip, OKN and OKAN fell (in 3 subjects) or reached a plateau (in the fourth). The amplitude of OKAN in human beings was much less than that reported in monkeys. The shape, however, of the curve relating retinal slip to the amplitude of OKAN was similar to that of monkeys. Furthermore, in both cases the curve resembles that obtained by plotting the results of experimental recordings of neural discharge in the nucleus of the optic tract as a function of retinal slip. These results imply that the processing of visual information for generation of OKAN is similar in monkeys and human beings but that the gain of the system is much less in human beings. We also found that fixation of a small target during optokinetic stimulation nearly completely prevented the development of OKAN while fixation of a small target for short periods after optokinetic stimulation did not alter the pattern of decay of OKAN. Thus, fixation may actively prevent the coupling of visual information into the velocity-storage mechanism.     

Influence of eye and head position on the vestibulo-ocular reflex

Summary For the vestibulo-ocular reflex (VOR) to function properly, namely to ensure a stable retinal image under all circumstances, it should be able to take into account varying eye positions in the orbit and varying orientations of the head with respect to the axis about which it is rotating. We tested this capability by quantifying the gain and the time constant of the horizontal component of the VOR during rotation about an earth vertical axis when the line of sight (optical axis) was moved out of the plane of head rotation — either by rotating the eyes up or down in the orbit or by pitching the head up or down with respect to earth-horizontal. In either case the gain of the horizontal component of the VOR was attenuated precisely by the cosine of the angle made between the optical axis and the plane of head rotation. Furthermore, if the head was pitched up or down but the eye rotated oppositely in the orbit so as to keep the line of sight in the plane of head rotation the gain of the horizontal component of the VOR was the same value as with the head and eyes both straight ahead. In contrast, the time constant of the VOR varied only as a function of the orientation of the head and not as a function of eye position in the orbit. During rotation about an earth vertical axis, the time constant was longest (about 18 s) when the head was pitched forward to place the lateral canals near earth-horizontal and shortest (about 11 s) when the head was pitched backward to place the vertical canals near earth-horizontal. Finally, since during rotation in yaw the pattern of stimulation of the lateral and vertical semicircular canals varies with different head orientations one can use measurements of the horizontal component of the VOR, under varying degrees of pitch of the head, to calculate the relative ability of the lateral and vertical semicircular canals to transduce head velocity.Dr. Fetter is a visiting scientist from the Neurologische Universitätsklinik, Eberhard-Karls-Universität, Liebermeisterstr. 18-20, D-7400 Tübingen, Federal Republic of Germany