Sensorimotor integration in the primate superior colliculus. I. Motor convergence

Orienting movements of the eyes and head are made to both auditory and visual stimuli even though in the primary sensory pathways the locations of auditory and visual stimuli are encoded in different coordinates. This study was designed to differentiate between two possible mechanisms for sensory-to-motor transformation. Auditory and visual signals could be translated into common coordinates in order to share a single motor pathway or they could maintain anatomically separate sensory and motor routes for the initiation and guidance of orienting eye movements. The primary purpose of the study was to determine whether neurons in the superior colliculus (SC) that discharge before saccades to visual targets also discharge before saccades directed toward auditory targets. If they do, this would indicate that auditory and visual signals, originally encoded in different coordinates, have been converted into a single coordinate system and are sharing a motor circuit. Trained monkeys made saccadic eye movements to auditory or visual targets while the activity of visual-motor (V-M) cells and saccade-related burst (SRB) cells was monitored. The pattern of spike activity observed during trials in which saccades were made to visual targets was compared with that observed when comparable saccades were made to auditory targets. For most (57 of 59) V-M cells, sensory responses were observed only on visual trials. Auditory stimuli originating from the same region of space did not activate these cells. Yet, of the 72 V-M and SRB cells studied, 79% showed motor bursts prior to saccades to either auditory or visual targets. This finding indicates that visual and auditory signals, originally encoded in retinal and head-centered coordinates, respectively, have undergone a transformation that allows them to share a common efferent pathway for the generation of saccadic eye movements. Saccades to auditory targets usually have lower velocities than saccades of the same amplitude and direction made to acquire visual targets. Since fewer collicular cells are active prior to saccades to auditory targets, one determinant of saccadic velocity may be the number of collicular neurons discharging before a particular saccade.     

Discharge patterns of neurons in the rostral superior colliculus of cat: activity related to fixation of visual and auditory targets

Neurons in the rostral superior colliculus (SC) of alert cats exhibit quasi-sustained discharge patterns related to the fixation of visual targets. Because some SC neurons also respond to auditory stimuli, we investigated whether there is a population of neurons in the rostral SC which is active in relation to fixation of both auditory and visual targets. We identified cells which were active with visual fixation and which continued to discharge if the fixation stimulus was briefly extinguished. The population of neurons exhibited similar discharge characteristics when the fixation stimulus was auditory. Few neurons were significantly more active during fixation of visual targets than during fixation of auditory targets. Most fixation neurons showed a diminished discharge rate during spontaneous (self-generated) saccadic eye movements away from a visual fixation stimulus, regardless of the direction of the saccade. this diminished discharge rate (or pause) typically began, on average, 12.2 ms before saccade onset and the duration of the pause was Ionger than the duration of the saccade. These observations are consistent with the hypothesis that increased discharge of these neurons is related to active fixation and that reductions in their activity are important for the generation of saccades. However, the lack of a precise relationship between pause duration and saccade duration implies that these neurons would be unlikely to project directly to the saccadic burst generator. The mean interval from the beginning of the pauses of fixation neurons to be beginning of the saccades away from fixation targets is also shorter than has been found in brainstem omnipause neurons. By analogy with the concept of a receptive field, agaze position error field depicts the range of gaze position error for which a cell is active. Although fixation neurons appear to encode the magnitude and direction of the error between visual targets and the visual axis, visual error fields at the end of fixating eye movements were significantly larger than those at stimulus onset. For auditory stimuli, this difference was not significant. These observations are compatible with a number of recent experiments indicating that neural signals of eye position are damped or delayed with respect to current eye position.     

Saccadic instabilities and voluntary saccadic behaviour

Primary gaze fixation is never perfectly stable but can be interrupted by involuntary, conjugate saccadic intrusions (SI). SI have a high prevalence in the normal population and are characterised by a horizontal fast eye movement away from the desired eye position, followed, after a variable duration, by a return saccade or drift. Amplitudes are usually below 1° and they often exhibit a directional bias. The aim of the present study was to investigate the aetiology of SI in relation to saccadic behaviour. It was hypothesised that if SI resulted from deficits in the saccadic system (i.e. reduced inhibitory mechanisms), changes in voluntary saccade behaviour may be apparent and related to SI frequency. To examine this, synchrony (no gap), gap, overlap and antisaccade tasks were conducted on ten normal subjects. No significant correlations were found between SI frequency and voluntary saccade latencies, the percentage of express saccades, or the percentage of antisaccade errors. In addition, no significant correlations were found between SI directional biases and saccade latency directional biases, express saccade biases or antisaccade error biases. These results suggest that an underlying alteration to saccadic behaviour is unlikely to be involved in SI production, and that the SI command signal may arise from the influence of attention on an intact saccadic system. Specifically, descending corticofugal signals relating to attention level and orientation may alter the balance between fixation and saccade generation, so determining SI characteristics.     

Express saccades in cat: effects of task and target modality

Saccadic eye movements to visual, auditory, and bimodal targets were measured in four adult cats. Bimodal targets were visual and auditory stimuli presented simultaneously at the same location. Three behavioral tasks were used: a fixation task and two saccadic tracking tasks (gap and overlap task). In the fixation task, a sensory stimulus was presented at a randomly selected location, and the saccade to fixate that stimulus was measured. In the gap and overlap tasks, a second target (hereafter called the saccade target) was presented after the cat had fixated the first target. In the gap task, the fixation target was switched off before the saccade target was turned on; in the overlap task, the saccade target was presented before the fixation target was switched off. All tasks required the cats to redirect their gaze toward the target (within a specified degree of accuracy) within 500 ms of target onset, and in all tasks target positions were varied randomly over five possible locations along the horizontal meridian within the cat's oculomotor range. In the gap task, a significantly greater proportion of saccadic reaction times (SRTs) were less than 125 ms, and mean SRTs were significantly shorter than in the fixation task. With visual targets, saccade latencies were significantly shorter in the gap task than in the overlap task, while, with bimodal targets, saccade latencies were similar in the gap and overlap tasks. On the fixation task, SRTs to auditory targets were longer than those to either visual or bimodal targets, but on the gap task, SRTs to auditory targets were shorter than those to visual or bimodal targets. Thus, SRTs reflected an interaction between target modality and task. Because target locations were unpredictable, these results demonstrate that cats, as well as primates, can produce very short latency goal-directed saccades.     

The Saccadic system more readily co-processes orthogonal than co-linear saccades

Real-life visual tasks such as tracking jumping objects and scanning visual scenes often require a sequence of saccadic eye movements. The ability of the ocular motor system to parallel process saccades has been previously demonstrated. We recorded the monocular eye movements of five normal human subjects using the magnetic search coil technique in a double step paradigm. Initial target jumps were always purely horizontal or purely vertical. We were interested in the latency to onset of the second saccade as a function of direction in relation to the first saccade. When the inter stimulus interval (ISI) was 150 or 180 ms orthogonal second saccades were of significantly shorter latency than second co-linear saccades. When the ISI was 250 ms the latencies of orthogonal and co-linear second saccades were statistically indistinguishable. Based on these findings it is postulated that the ocular motor system can more readily co-process orthogonal than co-linear saccades.     

Saccadic lateropulsion in Wallenberg syndrome: a window to access cerebellar control of saccades?

Saccadic lateropulsion is characterized by an undershoot of contralaterally directed saccades, an overshoot of ipsilaterally directed saccades and an ipsilateral deviation of vertical saccades. In Wallenberg syndrome, it is thought to result from altered signals in the olivo-cerebellar pathway to the oculomotor cerebellar network. In the current study we aimed to determine whether saccadic lateropulsion results from a cerebellar impairment of motor related signals or visuo-spatial related signals. We studied the trajectory, the accuracy, the direction and the amplitude of a variety of vertical and oblique saccades produced by five patients and nine control subjects. Some results are consistent with previous data suggesting altered motor related signals. Indeed, the horizontal error of contralesional saccades in patients increased with the desired horizontal saccade size. Furthermore, the initial directional error measured during the saccadic acceleration phase was smaller than the global directional error, suggesting that the eye trajectory curved progressively. However, some other results suggest that the processes that specify the horizontal spatial goal of the saccades might be impaired in the patients. Indeed, the horizontal error of ipsilesional saccades in patients did not change significantly with the desired horizontal saccade size. In addition, when comparing saccades with similar intended direction, it was found that the directional error was inversely related to the vertical saccade amplitude. Thus we conclude that the cerebellum might be involved both in controlling the motor execution of saccades and in determining the visuo-spatial information about their goal.     

Ocular gaze is anchored to the target of an ongoing pointing movement

It is well known that, typically, saccadic eye movements precede goal-directed hand movements to a visual target stimulus. Also pointing in general is more accurate when the pointing target is gazed at. In this study, it is hypothesized that saccades are not only preceding pointing but that gaze also is stabilized during pointing in humans. Subjects, whose eye and pointing movements were recorded, had to make a hand movement and a saccade to a first target. At arm movement peak velocity, when the eyes are usually already fixating the first target, a new target appeared, and subjects had to make a saccade toward it (dynamical trial type). In the statical trial type, a new target was offered when pointing was just completed. In a control experiment, a sequence of two saccades had to be made, with two different interstimulus intervals (ISI), comparable with the ISIs found in the first experiment for dynamic and static trial types. In a third experiment, ocular fixation position and pointing target were dissociated, subjects pointed at not fixated targets. The results showed that latencies of saccades toward the second target were on average 155 ms longer in the dynamic trial types, compared with the static trial types. Saccades evoked during pointing appeared to be delayed with approximately the remaining deceleration time of the pointing movement, resulting in "normal" residual saccadic reaction times (RTs), measured from pointing movement offset to saccade movement onset. In the control experiment, the latency of the second saccade was on average only 29 ms larger when the two targets appeared with a short ISI compared with trials with long ISIs. Therefore the saccadic refractory period cannot be responsible for the substantially bigger delays that were found in the first experiment. The observed saccadic delay during pointing is modulated by the distance between ocular fixation position and pointing target. The largest delays were found when the targets coincided, the smallest delays when they were dissociated. In sum, our results provide evidence for an active saccadic inhibition process, presumably to keep steady ocular fixation at a pointing target and its surroundings. Possible neurophysiological substrates that might underlie the reported phenomena are discussed.     

Sensorimotor integration in the primate superior colliculus. II. Coordinates of auditory signals

Based on the findings of the preceding paper, it is known that auditory and visual signals have been translated into common coordinates at the level of the superior colliculus (SC) and share a motor circuit involved in the generation of saccadic eye movements. It is not known, however, whether the translation of sensory signals into motor coordinates occurs prior to or within the SC. Nor is it known in what coordinates auditory signals observed in the SC are encoded. The present experiment tested two alternative hypotheses concerning the frame of reference of auditory signals found in the deeper layers of the SC. The hypothesis that auditory signals are encoded in head coordinates predicts that, with the head stationary, the response of auditory neurons will not be affected by variations in eye position but will be determined by the location of the sound source. The hypothesis that auditory responses encode the trajectory of the eye movement required to look to the target (motor error) predicts that the response of auditory cells will depend on both the position of the sound source and the position of the eyes in the orbit. Extracellular single-unit recordings were obtained from neurons in the SC while monkeys made delayed saccades to auditory or visual targets in a darkened room. The coordinates of auditory signals were studied by plotting auditory receptive fields while the animal fixated one of three targets placed 24 degrees apart along the horizontal plane. For 99 of 121 SC cells, the spatial location of the auditory receptive field was significantly altered by the position of the eyes in the orbit. In contrast, the responses of five sound-sensitive cells isolated in the inferior colliculus were not affected by variations in eye position. The possibility that systematic variations in the position of the pinnae associated with different fixation positions could account for these findings was controlled for by plotting auditory receptive fields while the pinnae were mechanically restrained. Under these conditions, the position of the eyes in the orbit still had a significant effect on the responsiveness of collicular neurons to auditory stimuli. The average magnitude of the shift of the auditory receptive field with changes in eye position (12.9 degrees) did not correspond to the magnitude of the shift in eye position (24 degrees). Alternative explanations for this finding were considered. One possibility is that, within the SC, there is a gradual transition from auditory signals in head coordinates to signals in motor error coordinates.(ABSTRACT TRUNCATED AT 400 WORDS)     

Interactions between visually and electrically elicited saccades before and after superior colliculus and frontal eye field ablations in the rhesus monkey

Recent work has shown that humans and monkeys utilize both retinal error and eye position signals to compute the direction and amplitude of saccadic eye movements (Hallett and Lightstone 1976a, b; Mays and Sparks 1980b). The aim of this study was to examine the role the frontal eye fields (FEF) and the superior colliculi (SC) play in this computation. Rhesus monkeys were trained to acquire small, briefly flashed spots of light with saccadic eye movements. During the latency period between target extinction and saccade initiation, their eyes were displaced, in total darkness, by electrical stimulation of either the FEF, the SC or the abducens nucleus area. Under such conditions animals compensated for the electrically induced ocular displacement and correctly reached the visual target area, suggesting that both a retinal error and eye position error signal were computed. The amplitude and direction of the electrically induced saccades depended not only on the site stimulated but also on the amplitude and direction of the eye movement initiated by the animal to acquire the target. When the eye movements initiated by the animal coincided with the saccades initiated by electrical stimulation, the resultant saccade was the weighted average of the two, where one weighing factor was the intensity of the electrical stimulus. Animals did not acquire targets correctly when their eyes were displaced, prior to their intended eye movements, by stimulating in the abducens nucleus area. After bilateral ablation of either the FEF or the SC monkeys were still able to acquire visual targets when their eyes were displaced, prior to saccade initiation, by electrical stimulation of the remaining intact structure. These results suggest that neither the FEF nor the SC is uniquely responsible for the combined computation of the retinal error and the eye position error signals.     

Reversible inactivation of macaque frontal eye field

 The macaque frontal eye field (FEF) is involved in the generation of saccadic eye movements and fixations. To better understand the role of the FEF, we reversibly inactivated a portion of it while a monkey made saccades and fixations in response to visual stimuli. Lidocaine was infused into a FEF and neural inactivation was monitored with a nearby microelectrode. We used two saccadic tasks. In the delay task, a target was presented and then extinguished, but the monkey was not allowed to make a saccade to its location until a cue to move was given. In the step task, the monkey was allowed to look at a target as soon as it appeared. During FEF inactivation, monkeys were severely impaired at making saccades to locations of extinguished contralateral targets in the delay task. They were similarly impaired at making saccades to locations of contralateral targets in the step task if the target was flashed for ≤100 ms, such that it was gone before the saccade was initiated. Deficits included increases in saccadic latency, increases in saccadic error, and increases in the frequency of trials in which a saccade was not made. We varied the initial fixation location and found that the impairment specifically affected contraversive saccades rather than affecting all saccades made into head-centered contralateral space. Monkeys were impaired only slightly at making saccades to contralateral targets in the step task if the target duration was 1000 ms, such that the target was present during the saccade: latency increased, but increases in saccadic error were mild and increases in the frequency of trials in which a saccade was not made were insignificant. During FEF inactivation there usually was a direct correlation between the latency and the error of saccades made in response to contralateral targets. In the delay task, FEF inactivation increased the frequency of making premature saccades to ipsilateral targets. FEF inactivation had inconsistent and mild effects on saccadic peak velocity. FEF inactivation caused impairments in the ability to fixate lights steadily in contralateral space. FEF inactivation always caused an ipsiversive deviation of the eyes in darkness. In summary, our results suggest that the FEF plays major roles in (1) generating contraversive saccades to locations of extinguished or flashed targets, (2) maintaining contralateral fixations, and (3) suppressing inappropriate ipsiversive saccades. Received: 2 February 1996 / Accepted: 26 February 1997     

The assessment of position of stationary targets perceived during saccadic eye movement

Summary The experiment was performed to establish the accuracy with which visual targets perceived during saccadic eye movement are localised. Subjects were presented with the task of executing saccades of 30° plus amplitude, passing through primary gaze, about the time of peak velocity a 5 ms red flash was presented at some random position (up to 30° left or right of centre) on a horizontal visual display. Subjects were required to indicate the direction in which they thought the flash was localised by fixating in that direction. Observations were made under conditions of prolonged total darkness and in the presence of a contrasting background. Measurement was made of saccade velocity and eye displacement as an index of target positions. Eye displacement was linearly scaled with respect to true target direction. Targets were localised with an average error of 5°–6° although the variance was high. No systematic differences were found between conditions or subjects. Error was unrelated to saccade velocity. It is concluded that during saccadic eye movements the appreciation of target position is maintained with an acceptable degree of accuracy.     

Transfer of short-term adaptation in human saccadic eye movements

Controversy exists as to the extent to which the saccadic system, adapted in the so-called gain-shortening paradigm for a particular target configuration, transfers the resulting change in saccade metrics to saccades elicited under different circumstances. In order to further assess this problem, we investigated the properties of human saccadic eye movements after visually induced short-term adaptation under a variety of conditions. We observed that saccades both during and after the adaptation did not significantly change their main sequence properties with respect to the pre-adaptation baseline. Saccade velocity profiles remained normal throughout the experiment, and we obtained no evidence that correction saccades were gradually absorbed in the primary saccade. We found that the effect of the short-term adaptation on saccade metrics is not confined to the particular combination of initial eye position and spatial position of the visual target used to induce the adaptation response. Saccades elicited from different initial positions towards targets with the same retinotopic coordinates as in the adaptation phase yield the same level of adaptation. However, our findings indicate that adaptation is confined to a limited range of saccade vectors around the oculocentric coordinates of the adaptation target (restricted adaptation field). Smaller and larger saccades are endowed with significantly lower adaptation values. Moreover, two further experiments showed that a retinal stimulus is not a prerequisite for adaptation to express itself: First, in a double-step experiment, we dissociated the retinal stimulus vector from the required oculomotor response. Second, we also investigated the effect of visually induced adaptation on auditory evoked saccades. In both tasks the adaptation was transferred to the required motor response. Based on our findings, we conclude that short-term adaptation is expressed at a multisensory stage, where saccadic eye movements are represented as desired eye displacement vectors (motor error). Possible neurophysiological implications are discussed.     

Sensory versus motor information in the control of predictive saccade timing

Humans readily make predictive saccades to periodic alternating targets. This predictive behavior depends on internal monitoring of timing error of past saccades in order to determine the time of initiation of future saccades; our earlier studies have confirmed this by finding correlations between latencies of consecutive predictive saccades. It is natural to consider that timing error is determined by visual detection of the difference between the time the target appears and the time the eyes arrive at the target; this in turn implies that saccades must actually be produced in order for their timing errors to be determined and predictive saccade timing to be established. We tested this hypothesis by having subjects view alternating visual targets while fixating a central target in order to eliminate saccade production. After six alternating target presentations, subjects began tracking the alternating targets. Tracking performance was assessed with an error measure that compared saccade latency and inter-saccade interval with desired values (zero and inter-stimulus interval, respectively). Errors in this Prior Viewing paradigm were compared to those from a conventional De Novo paradigm in which saccades began as soon as the alternating targets were presented. Saccades under Prior Viewing reached a low-error steady predictive state more rapidly than under De Novo tracking. The initial saccade under Prior Viewing had a higher latency than the others, suggesting that this saccade was reactive even though the paradigm is predictable; other reasons for this higher latency include time to disengage from the fixation target and time required to pre-program the initial set of saccades. The results show that visual detection of timing error from an actual motor act (saccades) is not necessary to establish predictive saccadic pacing: sensory-only information from viewing the moving targets can help to establish this predictive state.     

What is the coordinate frame utilized for the generation of express saccades in monkeys?

The latencies of saccades to suddenly appearing eccentric targets can have a bimodal distribution, with an early, express peak, and a late, regular peak (Fischer and Boch 1983, Brain Res 260: 21–26). Express saccades usually are a product of learning. The purpose of this study was to determine whether this learning is specific to the relative position of the target in space, the orbital position of the eye, or the vector of the saccade to be produced. Further, it was asked whether and how the frequency with which express saccades are generated is influenced by the immediately preceding saccadic vector and the familiarity of the targets. To this end, rhesus monkeys were trained to make saccadic eye movements to single targets and to two sequential targets that appeared at various positions relative to the head, relative to the initial fixation spot and relative to each other. The results show that the frequency with which express saccades are generated is determined by the saccadic vector that has to be generated and not by the relative position of a target in space, the orbital position of the eye, the immediately preceding saccadic vector, or the familiarity of the targets.     

The location marker effect. Saccadic latency increases with target eccentricity

Previous studies have shown that the retinal eccentricity of target stimuli has surprisingly little effect on the latency of visually driven saccades. But up until now researchers have addressed this issue by presenting saccadic targets in an unstructured visual field. This contrasts with everyday vision in which eye movements are initiated to stimuli within a cluttered environment. The present experiment compared latencies for target onsets in an empty visual field with a condition in which continuously illuminated location markers "tagged" the possible target locations. Previous reports of no effect of eccentricity on latencies in an unstructured field were replicated. However, a significant effect of eccentricity was found when location markers were used. Interestingly this did not reflect a lengthening of latencies as would be predicted by a reduction in target discriminability. Instead, latencies were relatively facilitated to near-visual onsets in the location marker condition. It is concluded that under more natural viewing conditions the latency of saccades is likely to be modulated by the eccentricity of target stimuli. This effect can be explained by competitive attentional interactions in saccade target selection processes.     

Expression of a re-centering bias in saccade regulation by superior colliculus neurons

In previous studies of saccadic eye movement reaction time, the manipulation of initial eye position revealed a behavioral bias that facilitates the initiation of movements towards the central orbital position. An interesting hypothesis for this re-centering bias suggests that it reflects a visuo-motor optimizing strategy, rather than peripheral muscular constraints. Given that the range of positions that the eyes can take in the orbits delimits the extent of visual exploration by head-fixed subjects, keeping the eyes centered in the orbits may indeed permit flexible orienting responses to engaging stimuli. To investigate the influence of initial eye position on central processes such as saccade selection and initiation, we examined the activity of saccade-related neurons in the primate superior colliculus (SC). Using a simple reaction time paradigm wherein an initially fixated visual stimulus varying in position was extinguished 200 ms before the presentation of a saccadic target, we studied the relationship between initial eye position and neuronal activation in advance of saccade initiation. We found that the magnitude of the early activity of SC neurons, especially during the immediate pre-target period that followed the fixation stimulus disappearance, was correlated with changes in initial eye position. For the great majority of neurons, the pre-target activity increased with changes in initial eye position in the direction opposite to their movement fields, and it was also strongly correlated with the concomitant reduction in reaction time of centripetal saccades directed within their movement fields. Taking into account the correlation with saccadic reaction time, the relationship between neuronal activity and initial eye position remained significant. These results suggest that eye-position-dependent changes in the excitability of SC neurons could represent the neural substrate underlying a re-centering bias in saccade regulation. More generally, the low frequency SC pre-target activity could use eccentric eye position signals to regulate both when and which saccades are produced by promoting the emergence of a high frequency burst of activity that can act as a saccadic command. However, only saccades initiated within ~200 ms of target presentation were associated with SC pre-target activity. This eye-dependent pre-target activation mechanism therefore appears to be restricted to the initiation of saccades with relatively short reaction times, which specifically require the integrity of the SC. Electronic Publication     

Eye movements induced by pontine stimulation: interaction with visually triggered saccades

1. Rhesus monkeys were trained to look to brief visual targets presented in an otherwise darkened room. On some trials, after the visual target was extinguished but before a saccade to it could be initiated, the eyes were driven to another orbital position by microstimulation of the paramedian pontine reticular formation. If, as current models of the saccadic system suggest, a copy of the motor command is used as a feedback signal of eye position, failure to compensate for stimulation-induced movements would indicate that stimulation occurred at a site beyond the point from which the eye position signal was derived. 2. Animals compensated for perturbations of eye position induced by stimulation of most pontine sites by making saccades that directed gaze to the position of the visual target. With stimulation at other pontine sites, compensatory saccades did not occur. 3. Pontine stimulation sometimes triggered, prematurely, impending visually directed saccades. The direction and amplitude of the premature movement depended upon the location of the briefly presented visual target. The amplitude of the premature movement was also a function of the interval between the stimulation train and the impending saccade. These data suggest that input signals for the horizontal and vertical pulse/step generators develop gradually during the presaccadic interval. Saccade trigger signals need to be delayed until the formation of these signals is completed. 4. The implications of these findings for models of the saccadic system are discussed. Robinson's local feedback model of the saccadic system can explain compensation for pontine stimulation-induced changes in eye position but cannot easily account for the failure to compensate for perturbations in eye position produced by stimulation at other sites. Modified versions of Robinson's model, which assume that the input signal to the pulse/step generator is the desired displacement of the eye, can account for both compensation and the failure to compensate since two separate neural integrators are employed. However, these models ignore kinematic arguments that commands to the extraocular muscles must specify the absolute position of the eye in the orbit rather than a relative movement from a previous position.     

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.     

Eye position effects in saccadic adaptation

Saccades are used by the visual system to explore visual space with the high accuracy of the fovea. The visual error after the saccade is used to adapt the control of subsequent eye movements of the same amplitude and direction in order to keep saccades accurate. Saccadic adaptation is thus specific to saccade amplitude and direction. In the present study we show that saccadic adaptation is also specific to the initial position of the eye in the orbit. This is useful, because saccades are normally accompanied by head movements and the control of combined head and eye movements depends on eye position. Many parts of the saccadic system contain eye position information. Using the intrasaccadic target step paradigm, we adaptively reduced the amplitude of reactive saccades to a suddenly appearing target at a selective position of the eyes in the orbitae and tested the resulting amplitude changes for the same saccade vector at other starting positions. For central adaptation positions the saccade amplitude reduction transferred completely to eccentric starting positions. However, for adaptation at eccentric starting positions, there was a reduced transfer to saccades from central starting positions or from eccentric starting positions in the opposite hemifield. Thus eye position information modifies the transfer of saccadic amplitude changes in the adaptation of reactive saccades. A gain field mechanism may explain the eye position dependence found.     

Shortening and prolongation of saccade latencies following microsaccades

When the eyes fixate at a point in a visual scene, small saccades rapidly shift the image on the retina. The effect of these microsaccades on the latency of subsequent large-scale saccades may be twofold. First, microsaccades are associated with an enhancement of visual perception. Their occurrence during saccade target perception could, thus, decrease saccade latencies. Second, microsaccades are likely to indicate activity in fixation-related oculomotor neurons. These represent competitors to saccade-related cells in the interplay of gaze holding and shifting. Consequently, an increase in saccade latencies would be expected after microsaccades. Here, we present evidence for both aspects of microsaccadic impact on saccade latency. In a delayed response task, participants made saccades to visible or memorized targets. First, microsaccade occurrence up to 50 ms before target disappearance correlated with 18 ms (or 8%) faster saccades to memorized targets. Second, if microsaccades occurred shortly (i.e., <150 ms) before a saccade was required, mean saccadic reaction time in visual and memory trials was increased by about 40 ms (or 16%). Hence, microsaccades can have opposite consequences for saccade latencies, pointing at a differential role of these fixational eye movements in the preparation of saccade motor programs.