A.J. van Opstal

Spatial and temporal factors determine auditory-visual interactions in human saccadic eye movements

In this paper, we show that human saccadic eye movements toward a visual target are generated with a reduced latency when this target is spatially and temporally aligned with an irrelevant auditory nontarget. This effect gradually disappears if the temporal and/or spatial alignment of the visual and auditory stimuli are changed. When subjects are able to accurately localize the auditory stimulus in two dimensions, the spatial dependence of the reduction in latency depends on the actual radial distance between the auditory and the visual stimulus. If, however, only the azimuth of the sound source can be determined by the subjects, the horizontal target separation determines the strength of the interaction. Neither saccade accuracy nor saccade kinematics were affected in these paradigms. We propose that, in addition to an aspecific warning signal, the reduction of saccadic latency is due to interactions that take place at a multimodal stage of saccade programming, where theperceived positions of visual and auditory stimuli are represented in a common frame of reference. This hypothesis is in agreement with our finding that the saccades often are initially directed to the average position of the visual and the auditory target, provided that their spatial separation is not too large. Striking similarities with electrophysiological findings on multisensory interactions in the deep layers of the midbrain superior colliculus are discussed.

Collicular ensemble coding of saccades based on vector summation

The superior colliculus in the monkey contains a topographically organized representation of the target in its upper layers and saccade-related activity in its deeper layers. Since collicular movement fields are quite large, a considerable region of the colliculus is active whenever a saccade is made. We have modelled the collicular role in saccade generation based on the idea, proposed earlier in the literature, that each movement cell causes a movement tendency in the direction of the external world point which it represents in the collicular map. The model is organized as follows: An anisotropic logarithmic mapping transforms retinal coordinates into collicular coordinates. A two-dimensional Gaussian function describes the spatial extent of the movement-related activity in the deeper layers. An efferent mapping function specifies how the direction and the size of the movement contribution of each colliculus neuron depends on its location and its firing rate. The total saccade is the vector sum of the individual cell contributions. This very simple model (seven fixed parameters) has been used to simulate metrical properties of saccades: in response to visual targets; in response to electrical stimulation in one colliculus, and after a colliculus lesion. Model performance appears to be remarkably realistic but cannot account for some border effects and responses to double stimulation. Suggestions on how the model can be improved and extended will be presented.

Human eye-head coordination in two dimensions under different sensorimotor conditions

Abstract The coordination between eye and head movements during a rapid orienting gaze shift has been investigated mainly when subjects made horizontal movements towards visual targets with the eyes starting at the centre of the orbit. Under these conditions, it is difficult to identify the signals driving the two motor systems, because their initial motor errors are identical and equal to the coordinates of the sensory stimulus (i.e. retinal error). In this paper, we investigate head-free gaze saccades of human subjects towards visual as well as auditory stimuli presented in the two-dimensional frontal plane, under both aligned and unaligned initial fixation conditions. Although the basic patterns for eye and head movements were qualitatively comparable for both stimulus modalities, systematic differences were also obtained under aligned conditions, suggesting a task-dependent movement strategy. Auditory-evoked gaze shifts were endowed with smaller eye-head latency differences, consistently larger head movements and smaller concomitant ocular saccades than visually triggered movements. By testing gaze control for eccentric initial eye positions, we found that the head displacement vector was best related to the initial head motor-error (target-re-head), rather than to the initial gaze error (target-re-eye), regardless of target modality. These findings suggest an independent control of the eye and head motor systems by commands in different frames of reference. However, we also observed a systematic influence of the oculomotor response on the properties of the evoked head movements, indicating a subtle coupling between the two systems. The results are discussed in view of current eye-head coordination models.

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.

Scatter in the metrics of saccades and properties of the collicular motor map

Abstract Saccades, elicited by an identical visual stimulus in repeated trials, exhibit a certain amount of amplitude and direction scatter. The present paper illustrates how this scatter may be used to discern various properties of the subsystem that determines the metrics of a saccade. It is found in humans that scatter along the eccentricity axis is consistently more pronounced than along the direction axis. The ratio of amplitude scatter and direction scatter is approximately constant for all target positions tested. In addition, the absolute amount of scatter increases roughly linearly with target eccentricity but does not depend on target direction. We have explored whether these findings may reflect noisy variations in the neural representation of the saccade vector at the level of the collicular motor map. There are good reasons to assume that the motor map, at least in the monkey (1) is organized in polar coordinates (2) has a nonhomogeneous (roughly logarithmic) representation of saccade amplitude (3) is anisotropic in nature ( Robinson, 1972 ; Ottes, Van Gisbergen & Eggermont, 1986 ; Van Gisbergen, Van Opstal & Tax, 1987 ). To account for the intertrial variability in saccades, we have slightly extended an existing model for the collicular role in the coding of saccade metrics (Van Gisbergen et al., 1987) by allowing small variations in both the total amount and the location of the collicular population activity. We discuss how such noisy variations at the level of the motor map would be expressed in the metrics of saccadic responses and consider alternative models which could explain our data.

Skewness of saccadic velocity profiles: A unifying parameter for normal and slow saccades

It has become customary to make use of so-called main sequence plots to characterize the dynamic properties of saccades. However, such a description does not account for the fact that the ratio between the accelerating and the decelerating fraction of the eye movement is not constant for all saccades. In this paper we introduce a new parameter, skewness, that characterizes this much neglected aspect of the saccade velocity profile. Human saccade data in this report demonstrate a clear relation between saccade duration (D) and skewness (S). When saccadic eye movements become extremely slow, due to fatigue or diazepam, the main sequence relation breaks down, while the S-D relation still holds. Despite large differences in amplitude, saccades of a fixed duration appear to have the same shape of velocity profile. A unifying equation relating the saccade parameters amplitude, maximum velocity and skewness, which is valid for both normal and slow saccades, is proposed.

Calibration of three-dimensional eye position using search coil signals in the rhesus monkey

A procedure is described to calibrate three-dimensional eye position with a dual-search coil implant in rhesus monkeys using a two-field magnetic system. The method allows one to determine the sensitivity of the search coils taking into account the presence of d.c. offset voltages. The orientation of the implant on the eye relative to a space-fixed reference frame is computed using fixations of targets arranged vertically. The critical steps of the procedure are discussed and documented by experimental data.

Stimulus intensity modifies saccadic reaction time and visual response latency in the superior colliculus

Performance in a reaction time task can be strongly influenced by the physical properties of the stimuli used (e.g., position and intensity). The reduction in reaction time observed with higher-intensity visual stimuli has been suggested to arise from reduced processing time along the visual pathway. If this hypothesis is correct, activity should be registered in neurons sooner for higher-intensity stimuli. We evaluated this hypothesis by measuring the onset of neural activity in the intermediate layers of the superior colliculus while monkeys generated saccades to high or low-intensity visual stimuli. When stimulus intensity was high, the response onset latency was significantly reduced compared to low-intensity stimuli. As a result, the minimum time for visually triggered saccades was reduced, accounting for the shorter saccadic reaction times (SRTs) observed following high-intensity stimuli. Our results establish a link between changes in neural activity related to stimulus intensity and changes to SRTs, which supports the hypothesis that shorter SRTs with higher-intensity stimuli are due to reduced processing time.

Experimental test of two models for the generation of oblique saccades

SummaryIn this paper, we report a detailed study of the dynamic properties of horizontal, vertical and oblique saccades. These eye movements were measured with an improved version of the double-magnetic induction method in two rhesus monkeys. We found that onsets of orthogonal components of oblique saccades are so well synchronized in the monkey that a common initiation system seems likely. Saccade vectors obeyed a nonlinear peakvelocity/amplitude relationship in all directions. The peak-velocity/duration/amplitude relationship for components was not fixed, but depended on the relative size of the orthogonal component: for a component with a given size, its duration increased and its peak velocity decreased, as the saccade vector to which it contributed turned away from the component direction under consideration. This stretching effect, which reflects a nonlinearity in the system, was negligible for small saccade vectors but became very pronounced in large oblique saccades. These experimental data were confronted with quantitative predictions derived from two different models for the generation of saccades in two dimensions. It appears that a model which assumes the existence of synchronized, but otherwise independent, pulse generators for horizontal and vertical components must be rejected. An alternative model, featuring a nonlinear vectorial pulse generator followed by a decomposition stage which generates component velocity command signals from the vectorial eye velocity signal, provides good fit with the data. According to this common-source model, the two nonlinear phenomena observed, viz., the curvilinear peak-velocity/amplitude relationship of saccades in all directions and component stretching in large oblique saccades, are due to a single nonlinearity in the proposed vectorial pulse generator. A possible neural basis for the common-source model is discussed.

Role of monkey superior colliculus in saccade averaging.

SummaryWe have investigated the involvement of collicular movement cells in the monkey in the execution of averaging saccades, elicited by a visual double-step stimulus. We found that, qualitatively, most (12/14) movement cells were recruited during averaging saccades in roughly the same way as for comparable visually-elicited saccades to single targets (V-saccades). However, movement-cell responses during averaging saccades in trials where the target suddenly changed direction were often less intense than for a comparable V-saccade. In these cases, the averaging responses were observed to be also slower than V-saccades of the same amplitude. Firing rate and double-step saccade dynamics were found to be significantly correlated in 9/14 cells tested. Several hypotheses for the collicular role in the generation of averaging saccades are discussed.