Inhibition of saccade initiation by preceding smooth pursuit

In this study, we investigated the influence of smooth-pursuit eye movements on saccade initiation in response to a sudden jump of a continuously moving target. We replicated the finding by Tanaka et al. (1998) that saccadic eye movements in the direction opposite to preceding pursuit have longer latencies than those in the same direction. We confirmed that this asymmetry is indeed due to an inhibitory effect of smooth pursuit on saccade initiation in the opposite direction rather than facilitation of saccade initiation in the same direction. The inhibitory effect decreased strongly when subjects knew the jump direction in advance. This supports the notion that the prolonged latencies of backward saccades are not due to orbital mechanics or low-level motor processing. Furthermore, we found that the range of saccade directions inhibited by a pursuit movement is broad, covering all directions that did not have the same horizontal component as the pursuit direction. This is in contrast with the predictions of "Inhibition of Saccade Return" (ISR, Hooge and Frens 2000), which is restricted to a smaller confined area. Electronic Publication     

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.     

Effects of neck muscles vibration on the perception of the head and trunk midline position

The present study focused on the influence of neck vibration on the perception of the head and trunk midline position (orientation and localization). The orientation of the head and trunk was investigated by the rolling adjustment of a rod on their midline while their localization was investigated by the adjustment of the position of a visual dot as being straight-ahead the eyes or the sternum. The first experiment investigated whether a head–trunk dissociation was induced by the unilateral vibration of neck muscles in upright and restrained subjects. Results showed that the subjective orientation and localization of whole-body midline were shifted toward the vibrated side. The second experiment determined the effect of the neck muscles vibration when the subjects were lying on their side. The effect of vibration disappeared when the side of vibration was opposed to the side of postural inclination and it was stronger than in the upright position when the side of vibration and the side of postural inclination were congruent. Whereas, results suggested that the input from neck muscle proprioceptors participates directly to the elaboration of the egocentric space, the question may be raised as to how the sensory cues interacted in their contribution to the neural generation of an egocentric, body centred coordinate system.     

Attentional shift by gaze is triggered without awareness

Reflexive attentional shift in response to another individual’s gaze direction has been reported, but it remains unknown whether this process can occur subliminally. We investigated this issue using facial stimuli consisting of drawings (Experiment 1) and photographs (Experiment 2). The gaze direction was expressed by the eye gaze direction (Experiment 1), and the eye gaze and head direction (Experiment 2). The gaze cue was presented either supraliminally or subliminally in the center of the visual field, before target presentation in the periphery. The task for participants was to localize the target as soon as possible. The reaction time needed to localize the target was consistently shorter for valid than invalid gaze cues for both types of gaze cues in both subliminal and supraliminal conditions. These findings indicate that attentional shift can be triggered even without awareness in response to another individual’s eye gaze or head direction.     

Allocentric cues do not always improve whole body reaching performance

The aim of this investigation was to gain further insight into control strategies used for whole body reaching tasks. Subjects were requested to step and reach to remembered target locations in normal room lighting (LIGHT) and complete darkness (DARK) with their gaze directed toward or eccentric to the remembered target location. Targets were located centrally at three different heights. Eccentric anchors for gaze direction were located at target height and initial target distance, either 30° to the right or 20° to the left of target location. Control trials, where targets remained in place, and remembered target trials were randomly presented. We recorded movements of the hand, eye and head, while subjects stepped and reached to real or remembered target locations. Lateral, vertical and anterior–posterior (AP) hand errors and eye location, and gaze direction deviations were determined relative to control trials. Final hand location errors varied by target height, lighting condition and gaze eccentricity. Lower reaches in the DARK compared to the LIGHT condition were common, and when matched with a tendency to reach above the low target, help explain more accurate reaches for this target in darkness. Anchoring the gaze eccentrically reduced hand errors in the AP direction and increased errors in the lateral direction. These results could be explained by deviations in eye locations and gaze directions, which were deemed significant predictors of final reach errors, accounting for a 17–47% of final hand error variance. Results also confirmed a link between gaze deviations and hand and head displacements, suggesting that gaze direction is used as a common input for movement of the hand and body. Additional links between constant and variable eye deviations and hand errors were common for the AP direction but not for lateral or vertical directions. When combined with data regarding hand error predictions, we found that subjectsȁ9 alterations in body movement in the AP direction were associated with AP adjustments in their reach, but final hand position adjustments were associated with gaze direction alterations for movements in the vertical and horizontal directions. These results support the hypothesis that gaze direction provides a control signal for hand and body movement and that this control signal is used for movement direction and not amplitude.     

The anti-orienting phenomenon revisited: effects of gaze cues on antisaccade performance

When the eye gaze of a face is congruent with the direction of an upcoming target, saccadic eye movements of the observer towards that target are generated more quickly, in comparison with eye gaze incongruent with the direction of the target. This work examined the conflict in an antisaccade task, when eye gaze points towards the target, but the saccadic eye movement should be triggered in the opposite direction. In a gaze cueing paradigm, a central face provided an attentional gaze cue towards the target or away from the target. Participants (N = 38) generated pro- and antisaccades to peripheral targets that were congruent or incongruent with the previous gaze cue. Paradoxically, facilitatory effects of a gaze cue towards the target were observed for both the pro- and antisaccade tasks. The results are consistent with the idea that eye gaze cues are processed in the task set that is compatible with the saccade programme. Thus, in an antisaccade paradigm, participants may anti-orient with respect to the gaze cue, resulting in faster saccades on trials when the gaze cue is towards the target. The results resemble a previous observation by Fischer and Weber (Exp Brain Res 109:507–512, 1996) using low-level peripheral cues. The current study extends this finding to include central socially communicative cues.     

Attentional shifts by gaze direction in voluntary orienting: evidence from a microsaccade study

Shifts in spatial attention can be induced by the gaze direction of another. However, it is unclear whether gaze direction influences the allocation of attention by reflexive or voluntary orienting. The present study was designed to examine which type of attentional orienting is elicited by gaze direction. We conducted two experiments to answer this question. In Experiment 1, we used a modified Posner paradigm with gaze cues and measured microsaccades to index the allocation of attention. We found that microsaccade direction followed cue direction between 200 and 400 ms after gaze cues were presented. This is consistent with the latencies observed in other microsaccade studies in which voluntary orienting is manipulated, suggesting that gaze direction elicits voluntary orienting. However, Experiment 1 did not separate voluntary and reflexive orienting directionally, so in Experiment 2, we used an anticue task in which cue direction (direction to allocate attention) was the opposite of gaze direction (direction of gaze in depicted face). The results in Experiment 2 were consistent with those from Experiment 1. Microsaccade direction followed the cue direction, not gaze direction. Taken together, these results indicate that the shift in spatial attention elicited by gaze direction is voluntary orienting.     

Visuomotor mental rotation of saccade direction

This investigation studied the latencies of saccadic eye movements that were directed away from a target by a variable angular distance, which was given by instruction. Such a movement presumably requires an intentional, visuomotor mental rotation of the saccade vector, resulting in prolonged reaction times. From a study on the control of directed hand movements, it has been hypothesized that all visuomotor and visual mental rotation tasks share a common processing stage. We tested this hypothesis with a saccade task in which subjects shifted their gaze either towards (0°, pro-saccade), or 30, 60, 90, 120, 150, or 180° (anti-saccade) away from a randomly cued position on an imaginary clock face. With four different cueing conditions, latencies increased monotonically with required gaze shift from 0–150°, thus exhibiting a mental rotation latency pattern. However, we also found anti-saccades faster than 150° gaze shift and slower rotation speeds with peripheral cues than with central cues. Together with the overall shallower latency increase compared with previous findings with mental rotation tasks, these results cast doubt on the notion of a common, central processing mechanism for the different types of tasks. Received: 11 August 1998 / Accepted: 9 February 1999     

The coordination of eye, head, and arm movements during rapid gaze orienting and arm pointing

This study aimed to investigate the coordination of multiple control actions involved in human horizontal gaze orienting or arm pointing to a common visual target. The subjects performed a visually triggered reaction time task in three conditions: (1) gaze orienting with a combined eye saccade and head rotation (EH), (2) arm pointing with gaze orienting by an eye saccade without head rotation (EA), and (3) arm pointing with gaze orienting by a combined eye saccade and head rotation (EHA). The subjects initiated eye movement first with nearly constant latencies across all tasks, followed by head movement in the EH task, by arm movement in the EA task, and by head and then arm movements in the EHA task. The differences of onset times between eye and head movements in the EH task, and between eye and arm movements in the EA task, were both preserved in the EHA task, leading to an eye-to-head-to-arm sequence. The onset latencies of eye and head in the EH task, eye and arm in the EA task, and eye, head and arm in the EHA task, were all positively correlated on a trial-by-trial basis. In the EHA task, however, the correlation coefficients of eye–head coupling and of eye–arm coupling were reduced and increased, respectively, compared to those estimated in the two-effector conditions (EH, EA). These results suggest that motor commands for different motor effectors are linked differently to achieve coordination in a task-dependent manner.     

Observing human interaction with physical devices

Triggering of saccades depends on the task: in the gap task, fixation point switches off and target appears after a gap period; in the overlap task, target appears while fixation point is still on. Saccade latencies are shorter in the gap task, due to fixation disengagement and advanced movement preparation during the gap. The two modes of initiation are also hypothesized to be subtended by different cortical-subcortical circuits. This study tested whether interleaving the two tasks modifies latencies, due to switching between different modes of triggering. Two groups of healthy participants (21–29 vs. 39–55 years) made horizontal and vertical saccades in gap, overlap, and mixed tasks; saccades were recorded with the Eyelink. Both groups showed shorter latencies in the gap task, i.e. a robust gap effect and systematic differences between directions. For young adults, interleaving tasks made the latencies shorter or longer depending on direction, while for middle-age adults, latencies became longer for all directions. Our observations can be explained in the context of models such as that of Brown et al. (Neural Netw 17:471–510, 2004), which proposed that different combinations of frontal eye field (FEF) layers, interacting with cortico-subcortical areas, control saccade triggering in gap and overlap trials. Moreover, we suggest that in early adulthood, the FEF is functioning optimally; frequent changes of activity in the FEF can be beneficial, leading to shorter latencies, at least for some directions. However, for middle-age adults, frequent changes of activity of a less optimally functioning FEF can be time consuming. Studying the alternation of gap and overlap tasks provides a fine tool to explore development, aging and disease. M. Vernet and Z. Kapoula contributed equally to this work.     

Is there a direct link between gaze perception and joint attention behaviours? Effects of gaze contrast polarity on oculomotor behaviour

Previous studies have found that attention is oriented in the direction of other people’s gaze suggesting that gaze perception is related to the mechanisms of joint attention. However, the role of the perception of gaze direction on joint attention has been challenged. We investigated the effects of disrupting gaze perception on the orienting of observers’ attention, in particular, whether orienting to gaze direction is affected by the disruptive effect of negative contrast polarity on gaze perception. A dynamic distracting gaze was presented to observers performing an endogenous saccadic task. Gaze perception was manipulated by reversing the contrast polarity between the sclera and the iris. With positive display polarity, eye movement recordings showed shorter saccadic latencies when the direction of the instructed saccade matched the direction of the distracting gaze, and a substantial number of erroneous saccades towards the direction of the perceived gaze when the latter did not match the instruction. Crucially, such effects were not found when gaze contrast polarity was reversed and gaze perception was impaired. These results extend previous studies by demonstrating the existence of a direct link between joint attention and the perception of gaze direction, and show how orienting of attention to other people’s gaze can be suppressed.     

Eye movements affirm: automatic overt gaze and arrow cueing for typical adults and adults with autism spectrum disorder

People with autism spectrum disorder (ASD) show reduced interest towards social aspects of the environment and a lesser tendency to follow other people’s gaze in the real world. However, most studies have shown that people with ASD do respond to eye-gaze cues in experimental paradigms, though it is possible that this behaviour is based on an atypical strategy. We tested this possibility in adults with ASD using a cueing task combined with eye-movement recording. Both eye gaze and arrow pointing distractors resulted in overt cueing effects, both in terms of increased saccadic reaction times, and in proportions of saccades executed to the cued direction instead of to the target, for both participant groups. Our results confirm previous reports that eye gaze cues as well as arrow cues result in automatic orienting of overt attention. Moreover, since there were no group differences between arrow and eye gaze cues, we conclude that overt attentional orienting in ASD, at least in response to centrally presented schematic directional distractors, is typical.     

注视方向和性别二态线索对面孔吸引力的影响

目的:考察有无情侣身份的大学生对不同注视方向和性别二态线索的面孔吸引力的评价.方法:采用Fan-taMorph 4.0软件通过性别二态技术操作性别二态线索,并通过Adobe PhotoshopTM来形成不同注视方向的面孔刺激.结果:被试对正视面孔的吸引力评价显著高于斜视面孔;被试对男性化的面孔的正视吸引力评价显著高于女性化面孔;无情侣的被试对正视面孔的吸引力评价显著高于有情侣的被试.结论:被试对正视的偏好符合进化的适应性;对男性化面孔正视的偏好与传统的性别角色模式理论的观点相一致;无情侣被试对正视的偏好符合进化中对择偶努力有效配置的适应.     

A quantitative study of auditory-evoked saccadic eye movements in two dimensions

We investigated the properties of human saccadic eye movements evoked by acoustic stimuli in the two-dimensional frontal plane. These movements proved to be quite accurate, both in azimuth and in elevation, grovided the sound source spectrum had a broad bandwidth and a sufficiently long duration. If the acoustic target was a tone, the azimuth of the saccadic end points remained equally accurate, whereas the elevation of the response was related to the frequency of the tone, rather than to the physical position of the target. Saccade elevation accuracy also declined substantially for short-duration noise bursts, although response elevation remained highly correlated with target elevation. The latencies of auditory saccades depended on the amplitude, but not on the direction of the eye movement, suggesting a polar coordinate origin of auditory saccade initiation. We also observed that the trajectories of auditory saccades were often substantially curved. Both a qualitative and a model-based analysis showed that this curvature corrected for errors in the initial direction of the saccade. The latter analysis also suggested that the kinematic properties of auditory saccades could be described by the superposition of two overlapping saccadic eye movements, hypothesized to be based on binaural difference cues and monaural spectral cues in the auditory signal, respectively. It is argued that, although the audio-oculomotor system has to operate in a feedforward way, it must nevertheless have access to an accurate representation of actual and desired eye position. Different models underlying the generation of auditory saccades are discussed.     

Developmental differences in cognitive control of socio-affective processing

We examined developmental differences in cognitive control in the context of distracting communicative cues varying in socio-affective significance. Adults and children (6-13 years) performed a Stroop-type task that required manual responses to a target word (LEFT/RIGHT) in the context of to-be-ignored spatial cues that were symbolic (arrow pointing left or right), social (left/right averted eye gaze in faces), or socio-emotional (happy, angry and fearful faces with left/right averted eye gaze). On the basis of the finding that accuracy was lower in the context of spatially incongruent than congruent cues, it was concluded that spatial direction, cued by both arrows and eye gaze, interfered with response selection. Interference did not differ between adults and children indicating that cognitive control of spatial attention directed by symbolic and social information is mature by 6 years. Interference from averted eye gaze was insensitive to the valence of facial emotion in adults and in children between 6-9 but not 10-13 years. Older children showed more interference from averted eye gaze in angry faces than younger children or adults. Thus, cognitive control of socio-affective processing differs in the preadolescent years relative to earlier in late childhood and adulthood.     

Developmental Differences in Cognitive Control of Socio-Affective Processing

We examined developmental differences in cognitive control in the context of distracting communicative cues varying in socio-affective significance. Adults and children (6–13 years) performed a Stroop-type task that required manual responses to a target word (LEFT/RIGHT) in the context of to-be-ignored spatial cues that were symbolic (arrow pointing left or right), social (left/right averted eye gaze in faces), or socio-emotional (happy, angry and fearful faces with left/right averted eye gaze). On the basis of the finding that accuracy was lower in the context of spatially incongruent than congruent cues, it was concluded that spatial direction, cued by both arrows and eye gaze, interfered with response selection. Interference did not differ between adults and children indicating that cognitive control of spatial attention directed by symbolic and social information is mature by 6 years. Interference from averted eye gaze was insensitive to the valence of facial emotion in adults and in children between 6–9 but not 10–13 years. Older children showed more interference from averted eye gaze in angry faces than younger children or adults. Thus, cognitive control of socio-affective processing differs in the preadolescent years relative to earlier in late childhood and adulthood.     

Differential influence of attention on gaze and head movements

A salient peripheral cue can capture attention, influencing subsequent responses to a target. Attentional cueing effects have been studied for head-restrained saccades; however, under natural conditions, the head contributes to gaze shifts. We asked whether attention influences head movements in combined eye-head gaze shifts and, if so, whether this influence is different for the eye and head components. Subjects made combined eye-head gaze shifts to horizontal visual targets. Prior to target onset, a behaviorally irrelevant cue was flashed at the same (congruent) or opposite (incongruent) location at various stimulus-onset asynchrony (SOA) times. We measured eye and head movements and neck muscle electromyographic signals. Reaction times for the eye and head were highly correlated; both showed significantly shorter latencies (attentional facilitation) for congruent compared with incongruent cues at the two shortest SOAs and the opposite pattern (inhibition of return) at the longer SOAs, consistent with attentional modulation of a common eye-head gaze drive. Interestingly, we also found that the head latency relative to saccade onset was significantly shorter for congruent than that for incongruent cues. This suggests an effect of attention on the head separate from that on the eyes.     

Combined eye-head gaze shifts to visual and auditory targets in humans

We studied the characteristics of combined eye-head gaze shifts in human subjects to determine whether they used similar strategies when looking at visual (V), auditory (A), and combined (V+A) targets located at several target eccentricities along the horizontal meridian. Subjects displayed considerable variability in the combinations of eye and head movement used to orient to the targets, ranging from those who always aligned their head close to the target, to those who relied predominantly on eye movements and only moved their head when the target was located beyond the limits of ocular motility. For a given subject, there was almost no variability in the amount of eye and head movement in the three target conditions (V, A, V+A). The time to initiate a gaze shift was influenced by stimulus modality and eccentricity. Auditory targets produced the longest latencies when located centrally (less than 20° eccentricity), whereas visual targets evoked the longest latencies when located peripherally (greater than 40° eccentricity). Combined targets (V+A) elicited the shortest latency reaction times at all eccentricities. The peak velocity of gaze shifts was also affected by target modality. At eccentricities between 10 and 30°, peak gaze velocity was greater for movements to visual targets than for movements to auditory targets. Movements to the combined target were of comparable speed with movements to visual targets. Despite the modality-specific differences in reaction latency and peak gaze velocity, the consistency of combinations of eye and head movement within subjects suggests that visual and auditory signals are remapped into a common reference frame for controlling orienting gaze shifts. A likely candidate is the deeper layers of the superior colliculus, because visual and auditory signals converge directly onto the neurons projecting to the eye and head premotor centers.     

Cervico-ocular coordination during neck rotation is distorted in people with whiplash-associated disorders

People with whiplash-associated disorders (WAD) not only suffer from neck/head pain, but commonly report deficits in eye movement control. Recent work has highlighted a strong relationship between eye and neck muscle activation in pain-free subjects. It is possible that WAD may disrupt the intricate coordination between eye and neck movement. Electromyographic activity (EMG) of muscles that rotate the cervical spine to the right (left sternocleidomastoid, right obliquus capitis inferior (OI), right splenius capitis (SC) and right multifidus (MF)) was recorded in nine people with chronic WAD. Cervical rotation was performed with five gaze conditions involving different gaze directions relative to cervical rotation. The relationship between eye position/movement and neck muscle activity was contrasted with previous observations from pain-free controls. Three main differences were observed in WAD. First, the superficial muscle SC was active with both directions of cervical rotation in contrast to activity only with right rotation in pain-free controls. Second, activity of OI and MF varied between directions of cervical rotation, unlike the non-direction-specific activity in controls. Third, the effect of horizontal gaze direction on neck muscle EMG was augmented compared to controls. These observations provide evidence of redistribution of activity between neck muscles during cervical rotation and increased interaction between eye and neck muscle activity in people with WAD. These changes in cervico-ocular coordination may underlie clinical symptoms reported by people with WAD that involve visual deficits and changes in function during cervical rotation such as postural control.     

Gaze stabilization during dynamic posturography in normal and vestibulopathic humans

Dynamic posturography by measurement of center of pressure (COP) is a widely employed technique for evaluating the vestibular system. However, the relationship of COP motion to vestibulo-ocular reflex (VOR) function and image stability on the retina has not been determined previously. To assess these relationships, we report gaze, head, and trunk stability during dynamic posturography in 11 normal volunteers, 7 subjects with unilateral vestibular lesions, and 3 subjects with bilateral vestibular lesions. Posturographic tasks consisted of standing still and standing on a platform that was sliding (0.2 Hz), tilting (0.1 Hz), or covered with a foam cushion 6 cm thick while tilting (0.1 Hz). Each perturbation was imposed in the anterior-posterior and repeated in the medial-lateral direction, in both light and darkness. Subjects viewed (or in darkness remembered) a target located 50, 100, or 500 cm distant. COP, angular eye position, and angular and linear orbit and trunk positions were measured using magnetic search coils and flux gate magnetometer sensors. With the target visible, the velocity of image motion on the retina was on average always less than 1°/s, well within the range consistent with high visual acuity. In darkness, gaze velocity increased for normal and vestibulopathic subjects. During tilt, vestibulopathic subjects had a significantly greater gaze velocity than controls. Gain of the angular VOR (eye velocity/head velocity) was significantly lower in darkness than in light and in vestibulopathic as compared to control subjects. Gain of the VOR was significantly correlated with gaze instability, but variation in VOR gain accounted for only 20–40% of the variance. In darkness, the velocity of the COP was significantly greater in vestibulopathic than control subjects for every condition tested. In light, this difference was small and often not significant. Although spectral analysis of the COP indicated frequencies above 1 Hz that were not observed in motion of the trunk and orbit, root mean square (RMS) velocities of the trunk and orbit in the horizontal plane were higher in darkness and in vestibulopathic subjects, mirroring COP findings. Only in vestibulopathic subjects tested in darkness was there a correlation between COP velocity and gaze velocity; COP velocity was otherwise uncorrelated with gaze. Gaze velocity was greater with near than with distant targets. Vertical VOR gain was higher with near targets. No other significant effects of target distance were found. Head movement strategy, VOR gain, and COP were all unaffected by target proximity. These data show that gaze velocity measurements during dynamic posturography in darkness are sensitive to vestibular loss. With a visible target, both COP and gaze stability of vestibulopathic subjects are difficult to distinguish from normal. During visual feedback, it is likely that image stabilization over the range of frequencies tested is achieved through better head stability and through visual tracking, allowing vestibulopathic subjects to maintain adequate visual acuity. Received: 25 November 1997 / Accepted: 24 April 1998