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Contains fulltext : 69496.pdf (author's version ) (Open Access) Contains fulltext : 69496.pdf (Publisher’s version ) (Closed access) Recently, we proposed an ensemble-coding scheme of the midbrain superior colliculus (SC) in which, during a saccade, each spike emitted by each recruited SC neuron contributes a fixed minivector to the gaze-control motor output. The size and direction of this 'spike vector' depend exclusively on a cell's location within the SC motor map (Goossens and Van Opstal, in J Neurophysiol 95: 2326-2341, 2006). According to this simple scheme, the planned saccade trajectory results from instantaneous linear summation of all spike vectors across the motor map. In our simulations with this model, the brainstem saccade generator was simplified by a linear feedback system, rendering the total model (which has only three free parameters) essentially linear. Interestingly, when this scheme was applied to actually recorded spike trains from 139 saccade-related SC neurons, measured during thousands of eye movements to single visual targets, straight saccades resulted with the correct velocity profiles and nonlinear kinematic relations ('main sequence properties' and 'component stretching'). Hence, we concluded that the kinematic nonlinearity of saccades resides in the spatial-temporal distribution of SC activity, rather than in the brainstem burst generator. The latter is generally assumed in models of the saccadic system. Here we analyze how this behaviour might emerge from this simple scheme. In addition, we will show new experimental evidence in support of the proposed mechanism.

Saccadic eye movements are thought to be influenced by blinking through premotor interactions, but it is still unclear how. The present paper describes the properties of blink-associated eye movements and quantifies the effect of reflex blinks on the latencies, metrics, and kinematics of saccades in the monkey. In particular, it is examined to what extent the saccadic system accounts for blink-related perturbations of the saccade trajectory. Trigeminal reflex blinks were elicited near the onset of visually evoked saccades by means of air puffs directed on the eye. Reflex blinks were also evoked during a straight-ahead fixation task. Eye and eyelid movements were measured with the magnetic-induction technique. The data show that saccade latencies were reduced substantially when reflex blinks were evoked prior to the impending visual saccades as if these saccades were triggered by the blink. The evoked blinks also caused profound spatial-temporal perturbations of the saccades. Deflections of the saccade trajectory, usually upward, extended up to approximately 15 degrees. Saccade peak velocities were reduced, and a two- to threefold increase in saccade duration was typically observed. In general, these perturbations were largely compensated in saccade mid-flight, despite the absence of visual feedback, yielding near-normal endpoint accuracies. Further analysis revealed that blink-perturbed saccades could not be described as a linear superposition of a pure blink-associated eye movement and an unperturbed saccade. When evoked during straight-ahead fixation, blinks were accompanied by initially upward and slightly abducting eye rotations of approximately 2-15 degrees. Back and forth wiggles of the eye were frequently seen; but in many cases the return movement was incomplete. Rather than drifting back to its starting position, the eye then maintained its eccentric orbital position until a downward corrective saccade toward the fixation spot followed. Blink-associated eye movements were quite rapid, albeit slower than saccades, and the velocity-amplitude-duration characteristics of the initial excursions as well as the return movements were approximately linear. These data strongly support the idea that blinks interfere with the saccade premotor circuit, presumably upstream from the neural eye-position integrator. They also indicated that a neural mechanism, rather than passive elastic restoring forces within the oculomotor plant, underlies the compensatory behavior. The tight latency coupling between saccades and blinks is consistent with an inhibition of omnipause neurons by the blink system, suggesting that the observed changes in saccade kinematics arise elsewhere in the saccadic premotor system.

Influence of head position on the spatial representation of acoustic targets. Sound localization in humans relies on binaural differences (azimuth cues) and monaural spectral shape information (elevation cues) and is therefore the result of a neural computational process. Despite the fact that these acoustic cues are referenced with respect to the head, accurate eye movements can be generated to sounds in complete darkness. This ability necessitates the use of eye position information. So far, however, sound localization has been investigated mainly with a fixed head position, usually straight ahead. Yet the auditory system may rely on head motor information to maintain a stable and spatially accurate representation of acoustic targets in the presence of head movements. We therefore studied the influence of changes in eye-head position on auditory-guided orienting behavior of human subjects. In the first experiment, we used a visual-auditory double-step paradigm. Subjects made saccadic gaze shifts in total darkness toward brief broadband sounds presented before an intervening eye-head movement that was evoked by an earlier visual target. The data show that the preceding displacements of both eye and head are fully accounted for, resulting in spatially accurate responses. This suggests that auditory target information may be transformed into a spatial (or body-centered) frame of reference. To further investigate this possibility, we exploited the unique property of the auditory system that sound elevation is extracted independently from pinna-related spectral cues. In the absence of such cues, accurate elevation detection is not possible, even when head movements are made. This is shown in a second experiment where pure tones were localized at a fixed elevation that depended on the tone frequency rather than on the actual target elevation, both under head-fixed and -free conditions. To test, in a third experiment, whether the perceived elevation of tones relies on a head- or space-fixed target representation, eye movements were elicited toward pure tones while subjects kept their head in different vertical positions. It appeared that each tone was localized at a fixed, frequency-dependent elevation in space that shifted to a limited extent with changes in head elevation. Hence information about head position is used under static conditions too. Interestingly, the influence of head position also depended on the tone frequency. Thus tone-evoked ocular saccades typically showed a partial compensation for changes in static head position, whereas noise-evoked eye-head saccades fully compensated for intervening changes in eye-head position. We propose that the auditory localization system combines the acoustic input with head-position information to encode targets in a spatial (or body-centered) frame of reference. In this way, accurate orienting responses may be programmed despite intervening eye-head movements. A conceptual model, based on the tonotopic organization of the auditory system, is presented that may account for our findings.

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.

Goossens, H.H.L.M. and A. J. Van Opstal. Local feedback signals are not distorted by prior eye movements: evidence from visually evoked double saccades. J. Neurophysiol. 78: 533–538, 1997. Recent experiments have shown that the amplitude and direction of saccades evoked by microstimulation of the monkey superior colliculus depend systematically on the amplitude and direction of preceding visually guided saccades as well as on the postsaccade stimulation interval. The data are consistent with the hypothesis that an eye displacement integrator in the local feedback loop of the saccadic burst generator is gradually reset with a time constant of ∼45 ms. If this is true, similar effects should occur during naturally evoked saccade sequences, causing systematic interval-dependent errors. To test this prediction in humans, saccades toward visual single- and double-step stimuli were elicited, and the properties of the second saccades were investigated as a function of the intersaccadic interval (ISI). In 15–20% of the saccadic responses, ISIs fell well below 100 ms. The errors of the second saccades were not systematically affected by the preceding primary saccade, irrespective of the ISI. Only a slight increase in the endpoint variability of second saccades was observed for the shortest ISIs. These results are at odds with the hypothesis that the putative eye displacement integrator has a reset time constant >10 ms. Instead, it is concluded that the signals involved in the internal feedback control of the saccadic burst generator reflect eye position and/or eye displacement accurately, irrespective of preceding eye movements.