Not looking while leaping: the linkage of blinking and saccadic gaze shifts

Many vertebrates generate blinks as a component of saccadic gaze shifts. We investigated the nature of this linkage between saccades and blinking in normal humans. Activation of the orbicularis oculi, the lid closing muscle, EMG occurred with 97% of saccadic gaze shifts larger than 33°. The blinks typically began simultaneously with the initiation of head and/or eye movement. To minimize the possibility that the blinks accompanying saccadic gaze shifts were reflex blinks evoked by the wind rushing across the cornea and eyelashes as the head and eyes turned, the subjects made saccadic head turns with their eyes closed. In this condition, orbicularis oculi EMG activity occurred with all head turns greater than 17° in amplitude and the EMG activity began an average of 39.3 ms before the start of the head movement. Thus, one component of the command for large saccadic gaze shifts appears to be a blink. We call these blinks gaze-evoked blinks. The linkage between saccadic gaze shifts and blinking is reciprocal. Evoking a reflex blink prior to initiating a voluntary saccadic gaze shift dramatically reduces the latency of the initiation of the head movement.     

Head–eye interactions during vertical gaze shifts made by rhesus monkeys

Changing the direction of the line of sight (gaze) can involve coordinated movements of the eyes and head. During gaze shifts directed along the horizontal meridian, the contribution of the eyes and head depends upon the position of the eyes in the orbits; the contribution of the head to accomplishing the overall shift in gaze declines as the eyes increasingly are deviated away from the direction of the ensuing gaze shift. Also during horizontal gaze shifts, changes in the metrics and kinematics of the saccadic (eye movement) portion of coordinated movements, are correlated with the amplitude and velocity of the concurrent head movement. With increasing head contributions, saccade peak velocities decline, durations increase and velocity profiles develop two peaks. It remains unknown whether the interaction between head and eyes observed during horizontal gaze shifts also occurs during vertical gaze shifts. Yet, a full understanding of the neural control of eye–head coordination will depend upon the correlation of neural activity and features of vertical as well as horizontal movements. This report describes the metrics and kinematics of vertical gaze shifts made by head-unrestrained rhesus monkeys. Key observations include: (1) during vertical gaze shifts of a particular amplitude, relative eye and head contributions depend upon the initial vertical positions of the eyes in the orbits; (2) as head contribution increases, peak eye velocities decline, durations increase and vertical velocity profiles develop two peaks; (3) head movement metrics and kinematics are accurately predictable given knowledge only of head movement amplitude. In these ways, vertical gaze shifts were found to be qualitatively similar to horizontal gaze shifts. It seems probable that similar mechanisms mediate head–eye interactions during both horizontal and vertical movements. These observations are consistent with the hypothesis that a signal proportional to vertical head velocity reduces the gain of the vertical saccade burst generator.     

Saccade dysmetria in head-unrestrained gaze shifts after muscimol inactivation of the caudal fastigial nucleus in the monkey

Lesions in the caudal fastigial nucleus (cFN) severely impair the accuracy of visually guided saccades in the head-restrained monkey. Is the saccade dysmetria a central perturbation in issuing commands for orienting gaze (eye in space) or is it a more peripheral impairment in generating oculomotor commands? This question was investigated in two head-unrestrained monkeys by analyzing the effect of inactivating one cFN on horizontal gaze shifts generated from a straight ahead fixation light-emitting diode (LED) toward a 40 degrees eccentric target LED. After muscimol injections, when viewing the fixation LED, the starting position of the head was changed (ipsilesional and upward deviations). Ipsilesional gaze shifts were associated with a 24% increase in the eye saccade amplitude and a 58% reduction in the amplitude of the head contribution. Contralesional gaze shifts were associated with a decrease in the amplitude of both eye and head components (40 and 37% reduction, respectively). No correlation between the changes in the eye amplitude and in head contribution was observed. The amplitude of the complete head movement was decreased for ipsilesional movements (57% reduction) and unaffected for contralesional movements. For both ipsilesional and contralesional gaze shifts, the changes in eye saccade amplitude were strongly correlated with the changes in gaze amplitude and largely accounted for the gaze dysmetria. These results indicate a major role of cFN in the generation of appropriate saccadic oculomotor commands during head-unrestrained gaze shifts.     

Modulation of gaze-evoked blinks depends primarily on extraretinal factors

Gaze-evoked blinks are contractions of the orbicularis oculi (OO)-the lid closing muscle-occurring during rapid movements of the head and eyes and result from a common drive to the gaze and blink motor systems. However, blinks occurring during shifts of gaze are often suppressed when the gaze shift is made to an important visual stimulus, suggesting that the visual system can modulate the occurrence of these blinks. In head-stabilized, human subjects, we tested the hypothesis that the presence of a visual stimulus was sufficient, but not necessary, to modulate OO EMG (OOemg) activity during saccadic eye movements. Rapid, reorienting movements of the eyes (saccades) were made to visual targets that remained illuminated (visually guided trials) or were briefly flashed (memory-guided trials) at different amplitudes along the horizontal meridian. We measured OOemg activity and found that the magnitude and probability of OOemg activity occurrence was reduced when a saccade was made to the memory of the spatial location as well as to the actual visual stimulus. The reduced OOemg activity occurred only when the location of the target was previously cued. OOemg activity occurred reliably with spontaneous saccades that were made to locations with no explicit visual stimulus, generally, back to the fixation location. Thus the modulation of gaze-evoked OOemg activity does not depend on the presence of visual information per se, but rather, results from an extraretinal signal.     

Coordination of eye and head components of movements evoked by stimulation of the paramedian pontine reticular formation

Constant frequency microstimulation of the paramedian pontine reticular formation (PPRF) in head-restrained monkeys evokes a constant velocity eye movement. Since the PPRF receives significant projections from structures that control coordinated eye-head movements, we asked whether stimulation of the pontine reticular formation in the head-unrestrained animal generates a combined eye-head movement or only an eye movement. Microstimulation of most sites yielded a constant-velocity gaze shift executed as a coordinated eye-head movement, although eye-only movements were evoked from some sites. The eye and head contributions to the stimulation-evoked movements varied across stimulation sites and were drastically different from the lawful relationship observed for visually-guided gaze shifts. These results indicate that the microstimulation activated elements that issued movement commands to the extraocular and, for most sites, neck motoneurons. In addition, the stimulation-evoked changes in gaze were similar in the head-restrained and head-unrestrained conditions despite the assortment of eye and head contributions, suggesting that the vestibulo-ocular reflex (VOR) gain must be near unity during the coordinated eye-head movements evoked by stimulation of the PPRF. These findings contrast the attenuation of VOR gain associated with visually-guided gaze shifts and suggest that the vestibulo-ocular pathway processes volitional and PPRF stimulation-evoked gaze shifts differently.     

Contribution of the frontal eye field to gaze shifts in the head-unrestrained monkey: effects of microstimulation

The role of the primate frontal eye field (FEF) has been inferred primarily from experiments investigating saccadic eye movements with the head restrained. Three recent reports investigating head-unrestrained gaze shifts disagree on whether head movements are evoked with FEF stimulation and thus whether the FEF participates in gaze movement commands. We therefore examined the eye, head, and overall gaze movement evoked by low-intensity microstimulation of the low-threshold region of the FEF in two head-unrestrained monkeys. Microstimulation applied at 200 or 350 Hz for 200 ms evoked large gaze shifts with substantial head movement components from most sites in the dorsomedial FEF, but evoked small, predominantly eye-only gaze shifts from ventrolateral sites. The size and direction of gaze and eye movements were strongly affected by the eye position before stimulation. Head movements exhibited little position dependency, but at some sites and initial eye positions, head-only movements were evoked. Stimulus-evoked gaze shifts and their eye and head components resembled those elicited naturally by visual targets. With stimulus train durations >200 ms, the evoked gaze shifts were more likely to be accomplished with a substantial head movement, which often continued for the entire stimulus duration. The amplitude, duration and peak velocity of the evoked head movement were more strongly correlated with stimulus duration than were those of the gaze or eye movements. We conclude that the dorsomedial FEF generates a gaze command signal that can produce eye, head, or combined eye-head movement depending on the initial orbital position of the eye.     

Short- and long-term consequences of canal plugging on gaze shifts in the rhesus monkey. I. Effects on gaze stabilization.

Short- and long-term consequences of canal plugging on gaze shifts in the rhesus monkey. I. Effects on gaze stabilization. To study the contribution of the vestibular system to the coordinated eye and head movements of a gaze shift, we plugged the lumens of just the horizontal (n = 2) or all six semicircular canals (n = 1) in monkeys trained to make horizontal head-unrestrained gaze shifts to visual targets. After the initial eye saccade of a gaze shift, normal monkeys exhibit a compensatory eye counterrotation that stabilizes gaze as the head movement continues. This counterrotation, which has a gain (eye velocity/head velocity) near one has been attributed to the vestibuloocular reflex (VOR). One day after horizontal canal plugging, the gain of the passive horizontal VOR at frequencies between 0.1 and 1.0 Hz was <0.10 in the horizontal-canal-plugged animals and zero in the all-canal-plugged animal. One day after surgery, counterrotation gain was approximately 0.3 in the animals with horizontal canals plugged and absent in the animal with all canals plugged. As the time after plugging increased, so too did counterrotation gain. In all three animals, counterrotation gain recovered to between 0.56 and 0.75 within 80-100 days. The initial loss of compensatory counterrotation after plugging resulted in a gaze shift that ended long after the eye saccade and just before the end of the head movement. With recovery, the length of time between the end of the eye saccade and the end of the gaze movement decreased. This shortening of the duration of reduced gain counterrotation occurred both because head movements ended sooner and counterrotation gain returned to 1.0 more rapidly relative to the end of the eye saccade. Eye counterrotation was not due to activation of pursuit eye movements as it persisted when gaze shifts were executed to extinguished targets. Also counterrotation was not due simply to activation of neck receptors because counterrotation persisted after head movements were arrested in midflight. We suggest that the neural signal that is used to cause counterrotation in the absence of vestibular input is an internal copy of the intended head movement.     

Head movement evoked by electrical stimulation in the supplementary eye field of the rhesus monkey

Although the supplementary eye field (SEF) has been implicated in the control of head movements associated with gaze shifts, there is no direct evidence that SEF plays a role in the generation of head movements independent of gaze. If the SEF does, varying the duration of stimulation should selectively alter the head-movement kinematics during the postgaze-shift period. The duration of the stimulation was manipulated while head-unrestrained monkeys maintained stable head forward postures. The initial positions of the eyes in the orbits were systematically varied. Although combined movements of the eyes and head were produced in the majority of the trials, head movements were sometimes evoked in the absence of gaze shifts. These head-alone movements were most frequent when the initial eye position was contralateral to the stimulated side. When the stimulation produced eye and head movements, gaze onset was sometimes preceded by a relatively low-velocity phase of the head movement. Evoked head movements were primarily horizontal, unlike the gaze shifts, which typically had vertical components that varied according to the initial positions of the eyes in the orbits. The postgaze-shift head movements tended to be of low velocity and in many cases persisted until stimulation offset. In general, prolonging the stimulation resulted in improved centering of the eyes in the orbits. These findings suggest that, in addition to its previously described role in the generation of coordinated eye-head gaze shifts, the SEF is also involved in the control of head movements in the absence of a change of gaze.     

Effects of voluntary blinks on saccades,vergence eye movements,and saccade-vergence interactions in humans

Blinks are known to change the kinematic properties of horizontal saccades, probably by influencing the saccadic premotor circuit. The neuronal basis of this effect could be explained by changes in the activity of omnipause neurons in the nucleus raphe interpositus or in the saccade-related burst neurons of the superior colliculus. Omnipause neurons cease discharge during both saccades and vergence movements. Because eyelid blinks can influence both sets of neurons, we hypothesized that blinks would influence the kinematic parameters of saccades in all directions, vergence, and saccade-vergence interactions. To test this hypothesis, we investigated binocular eye and lid movements in five normal healthy subjects with the magnetic search coil technique. The subjects performed conjugate horizontal and vertical saccades from gaze straight ahead to targets at 20 degrees up, down, right, or left while either attempting not to blink or voluntarily blinking. While following the same blink instruction, subjects made horizontal vergence eye movements of 7 degrees and combined saccade-vergence movements with a version amplitude of 20 degrees. The movements were performed back and forth from two targets simultaneously presented nearby (38 cm) and more distant (145 cm). Small vertical saccades accompanied most vergence movements. These results show that blinks change the kinematics (saccade duration, peak velocity, peak acceleration, peak deceleration) of not only horizontal but also of vertical saccades, of horizontal vergence eye movements, and of combined saccade-vergence eye movements. Peak velocity, acceleration, and deceleration of eye movements were decreased on the average by 30%, and their duration increased by 43% on the average when they were accompanied by blinks. The blink effect was time dependent with respect to saccade and vergence onset: the greatest effect occurred 100 ms prior to saccade onset, whereas there was no effect when the blink started after saccade onset. The effects of blinks on saccades and vergence, which are tightly coupled to latency, support the hypothesis that blinks cause profound spatiotemporal perturbations of the eye movements by interfering with the normal saccade/vergence premotor circuits. However, the measured effect may to a certain degree but not exclusively be explained by mechanical interference.     

Eye, head, and body coordination during large gaze shifts in rhesus monkeys: movement kinematics and the influence of posture

Coordinated movements of the eye, head, and body are used to redirect the axis of gaze between objects of interest. However, previous studies of eye-head gaze shifts in head-unrestrained primates generally assumed the contribution of body movement to be negligible. Here we characterized eye-head-body coordination during horizontal gaze shifts made by trained rhesus monkeys to visual targets while they sat upright in a standard primate chair and assumed a more natural sitting posture in a custom-designed chair. In both postures, gaze shifts were characterized by the sequential onset of eye, head, and body movements, which could be described by predictable relationships. Body motion made a small but significant contribution to gaze shifts that were > or =40 degrees in amplitude. Furthermore, as gaze shift amplitude increased (40-120 degrees ), body contribution and velocity increased systematically. In contrast, peak eye and head velocities plateaued at velocities of approximately 250-300 degrees /s, and the rotation of the eye-in-orbit and head-on-body remained well within the physical limits of ocular and neck motility during large gaze shifts, saturating at approximately 35 and 60 degrees , respectively. Gaze shifts initiated with the eye more contralateral in the orbit were accompanied by smaller body as well as head movement amplitudes and velocities were greater when monkeys were seated in the more natural body posture. Taken together, our findings show that body movement makes a predictable contribution to gaze shifts that is systematically influenced by factors such as orbital position and posture. We conclude that body movements are part of a coordinated series of motor events that are used to voluntarily reorient gaze and that these movements can be significant even in a typical laboratory setting. Our results emphasize the need for caution in the interpretation of data from neurophysiological studies of the control of saccadic eye movements and/or eye-head gaze shifts because single neurons can code motor commands to move the body as well as the head and eyes.     

3-Dimensional eye-head coordination in gaze shifts evoked during stimulation of the lateral intraparietal cortex

Coordinated eye-head gaze shifts have been evoked during electrical stimulation of the frontal cortex (supplementary eye field (SEF) and frontal eye field (FEF)) and superior colliculus (SC), but less is known about the role of lateral intraparietal cortex (LIP) in head-unrestrained gaze shifts. To explore this, two monkeys (M1 and M2) were implanted with recording chambers and 3-D eye+ head search coils. Tungsten electrodes delivered trains of electrical pulses (usually 200 ms duration) to and around area LIP during head-unrestrained gaze fixations. A current of 200 μA consistently evoked small, short-latency contralateral gaze shifts from 152 sites in M1 and 243 sites in M2 (Constantin et al., 2007). Gaze kinematics were independent of stimulus amplitude and duration, except that subsequent saccades were suppressed. The average amplitude of the evoked gaze shifts was 8.46° for M1 and 8.25° for M2, with average head components of only 0.36 and 0.62° respectively. The head's amplitude contribution to these movements was significantly smaller than in normal gaze shifts, and did not increase with behavioral adaptation. Stimulation-evoked gaze, eye and head movements qualitatively obeyed normal 3-D constraints (Donders' law and Listing's law), but with less precision. As in normal behavior, when the head was restrained LIP stimulation evoked eye-only saccades in Listing's plane, whereas when the head was not restrained, stimulation evoked saccades with position-dependent torsional components (driving the eye out of Listing's plane). In behavioral gaze-shifts, the vestibuloocular reflex (VOR) then drives torsion back into Listing's plane, but in the absence of subsequent head movement the stimulation-induced torsion was “left hanging”. This suggests that the position-dependent torsional saccade components are preprogrammed, and that the oculomotor system was expecting a head movement command to follow the saccade. These data show that, unlike SEF, FEF, and SC stimulation in nearly identical conditions, LIP stimulation fails to produce normally-coordinated eye-head gaze shifts.     

Comparing extraocular motoneuron discharges during head-restrained saccades and head-unrestrained gaze shifts

Burst neurons (BNs) in the paramedian pontine reticular formation provide the primary input to the extraocular motoneurons (MNs) during head-restrained saccades and combined eye-head gaze shifts. Prior studies have shown that BNs carry eye movement-related signals during saccades and carry head as well as eye movement-related signals during gaze shifts. Therefore MNs receive signals related to head motion during gaze shifts, yet they solely drive eye motion. Here we addressed whether the relationship between MN firing rates and eye movements is influenced by the additional premotor signals present during gaze shifts. Neurons in the abducens nucleus of monkeys were first studied during saccades made with the head stationary. We then recorded from the same neurons during voluntary combined eye-head gaze shifts. We conclude that the activity of MNs, in contrast to that of BNs, is related to eye motion by the same dynamic relationship during head-restrained saccades and head-unrestrained gaze shifts. In addition, we show that a standard metric-based analysis [i.e., counting the number of spikes (NOS) in a burst] yields misleading results when applied to the same data set. We argue that this latter approach fails because it does not properly consider the system's dynamics or the strong interactions between eye and head motion.     

Eye movements and blinks: their relationship to higher cognitive processes

Information about the timing of spontaneous eye blinks was abstracted while subjects performed a detection and identification task. We found blinks to be time-locked to saccadic eye movements involved in the identification of peripherally presented stimuli. The larger the required eye movement, the greater the likelihood of blink occurrence. Blink latencies were found to be significantly shorter for centrally, as compared to peripherally presented stimuli, and blinks were more likely to be associated with eye movement returning gaze to a central location than with movements associated with the identification of peripherally presented information. Thus, we conclude that the spontaneous or endogenous eye blink is triggered by aspects of information processing, and that blink latencies can be used as one tool for evaluating the level of complexity of such processing under a wide variety of task demands.     

Kinematics and eye–head coordination of gaze shifts evoked from different sites in the superior colliculus of the cat

Shifting gaze requires precise coordination of eye and head movements. It is clear that the superior colliculus (SC) is involved with saccadic gaze shifts. Here we investigate its role in controlling both eye and head movements during gaze shifts. Gaze shifts of the same amplitude can be evoked from different SC sites by controlled electrical microstimulation. To describe how the SC coordinates the eye and the head, we compare the characteristics of these amplitude-matched gaze shifts evoked from different SC sites. We show that matched amplitude gaze shifts elicited from progressively more caudal sites are progressively slower and associated with a greater head contribution. Stimulation at more caudal SC sites decreased the peak velocity of the eye but not of the head, suggesting that the lower peak gaze velocity for the caudal sites is due to the increased contribution of the slower-moving head. Eye–head coordination across the SC motor map is also indicated by the relative latencies of the eye and head movements. For some amplitudes of gaze shift, rostral stimulation evoked eye movement before head movement, whereas this reversed with caudal stimulation, which caused the head to move before the eyes. These results show that gaze shifts of similar amplitude evoked from different SC sites are produced with different kinematics and coordination of eye and head movements. In other words, gaze shifts evoked from different SC sites follow different amplitude–velocity curves, with different eye–head contributions. These findings shed light on mechanisms used by the central nervous system to translate a high-level motor representation (a desired gaze displacement on the SC map) into motor commands appropriate for the involved body segments (the eye and the head).     

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.     

Head-unrestrained gaze shifts after muscimol injection in the caudal fastigial nucleus of the monkey

The effects of unilateral cFN inactivation on horizontal and vertical gaze shifts generated from a central target toward peripheral ones were tested in two head unrestrained monkeys. After muscimol injection, the eye component was hypermetric during ipsilesional gaze shifts, hypometric during contralesional ones and deviated toward the injected side during vertical gaze shifts. The ipsilesional gaze hypermetria increased with target eccentricity until approximately 24 degrees after which it diminished and became smaller than the hypermetria of the eye component. Contrary to eye saccades, the amplitude and peak velocity of which were enhanced, the amplitude and peak velocity of head movements were reduced during ipsilesional gaze shifts. These changes in head movement were not correlated with those affecting the eye saccades. Head movements were also delayed relative to the onset of eye saccades. The alterations in head movement and the faster eye saccades likely explained the reduced head contribution to the amplitude of ipsilesional gaze shifts. The contralesional gaze hypometria increased with target eccentricity and was associated with uncorrelated reductions in eye and head peak velocities. When compared with control movements of similar amplitude, contralesional eye saccades had lower peak velocity and longer duration. This slowing likely accounted for the increase in head contribution to the amplitude of contralesional gaze shifts. These data suggest different pathways for the fastigial control of eye and head components during gaze shifts. Saccade dysmetria was not compensated by appropriate changes in head contribution, raising the issue of the feedback control of movement accuracy during combined eye-head gaze shifts.     

Enhancement of the vestibulo-ocular reflex by prior eye movements.

We investigated the effect of visually mediated eye movements made before velocity-step horizontal head rotations in eleven normal human subjects. When subjects viewed a stationary target before and during head rotation, gaze velocity was initially perturbed by approximately 20% of head velocity; gaze velocity subsequently declined to zero within approximately 300 ms of the stimulus onset. We used a curve-fitting procedure to estimate the dynamic course of the gain throughout the compensatory response to head rotation. This analysis indicated that the median initial gain of compensatory eye movements (mainly because of the vestibulo-ocular reflex, VOR) was 0. 8 and subsequently increased to 1.0 after a median interval of 320 ms. When subjects attempted to fixate the remembered location of the target in darkness, the initial perturbation of gaze was similar to during fixation of a visible target (median initial VOR gain 0.8); however, the period during which the gain increased toward 1.0 was >10 times longer than that during visual fixation. When subjects performed horizontal smooth-pursuit eye movements that ended (i.e., 0 gaze velocity) just before the head rotation, the gaze velocity perturbation at the onset of head rotation was absent or small. The initial gain of the VOR had been significantly increased by the prior pursuit movements for all subjects (P < 0.05; mean increase of 11%). In four subjects, we determined that horizontal saccades and smooth tracking of a head-fixed target (VOR cancellation with eye stationary in the orbit) also increased the initial VOR gain (by a mean of 13%) during subsequent head rotations. However, after vertical saccades or smooth pursuit, the initial gaze perturbation caused by a horizontal head rotation was similar to that which occurred after fixation of a stationary target. We conclude that the initial gain of the VOR during a sudden horizontal head rotation is increased by prior horizontal, but not vertical, visually mediated gaze shifts. We postulate that this "priming" effect of a prior gaze shift on the gain of the VOR occurs at the level of the velocity inputs to the neural integrator subserving horizontal eye movements, where gaze-shifting commands and vestibular signals converge.     

Differential effects of blinks on horizontal saccade and smooth pursuit initiation in humans

Blinks executed during eye movements affect kinetic eye movement parameters, e.g., peak velocity of saccades is decreased, their duration is increased, but their amplitude is not altered. This effect is mainly explained by the decreased activity of premotor neurons in the brainstem: omni-pause neurons (OPN) in the nucleus raphe interpositus. Previous studies examined the immediate effect of blinks directly on eye movements but not their effect when they are elicited several hundred milliseconds before the eye movements. In order to address this question we tested blinks elicited before the target onset of saccades and pursuit and compared the results to the gap effect: if a fixation light is extinguished for several hundred milliseconds, the reaction time (latency) for subsequent saccades or smooth pursuit eye movements is decreased. Monocular eye and lid movements were recorded in nine healthy subjects using the scleral search-coil system. Laser stimuli were front-projected onto a tangent screen in front of the subjects. Horizontal step-ramp smooth pursuit of 20 deg/s was elicited in one session, or 5 deg horizontal visually guided saccades in another experimental session. In one-third of the trials (smooth pursuit or saccades) the fixation light was extinguished for 200 ms before stimulus onset (gap condition), and in another third of the trials reflexive blinks were elicited by a short airpuff before the stimulus onset (blink condition). The last third of the trials served as controls (control condition). Stimulus direction and the three conditions were randomized for saccades and smooth pursuit separately. The latency of the step-ramp smooth pursuit in the blink condition was found to be decreased by 10 ms, which was less than in the gap condition (38 ms). However, the initial acceleration and steady-state velocity of smooth pursuit did not differ in the three conditions. In contrast, the latency of the saccades in the gap condition was decreased by 39 ms, but not in the blink condition. Saccade amplitude, peak velocity, and duration were not different in the three conditions. There was also no difference in blink amplitude and duration of pupil occlusion in the blink condition, neither in saccades nor in smooth pursuit. The latency reduction of smooth pursuit, but not of saccades, may neither be explained by the brief pupil occlusion nor by visual suppression, warning signals, or the startle response. Whether the effects are caused by the influence of blinks on OPNs or other premotor structures remains to be tested.     

Coordination of the eyes and head: movement kinematics

When the head is restrained, saccades are characterized by lawful relationships between movement amplitude, peak velocity, and duration. In addition, the spatiotemporal progression of saccades (i.e., movement kinematics) is predictable if saccade amplitude and direction are known. However, when the head is free to move, changes in the direction of the line of sight (gaze shifts) often involve saccades associated with simultaneous head movements. The metrics (duration, amplitude, peak velocity) and kinematics of saccades occurring in conjunction with head movements cannot be predicted on the basis of saccade amplitude and direction alone. For example, when the head is unrestrained, velocity profiles of 35 degree eye movements can be symmetrical and might have peaks approximately 600 degrees/s. But, 35 degrees eye movements can also have peak velocities of approximately 300 degrees/s and have velocity profiles with two pronounced peaks: an initial peak followed by a reduction and subsequent increase in velocity. Saccade amplitude and direction are insufficient to predict the shape of the velocity profile. However, as illustrated in this report, if the amplitude of the concurrent head movement is taken into account, saccade kinematics are predictable even during gaze shifts with large head components. The data presented here are indicative of an interaction between eye and head motor systems in which head movement commands alter the execution of concurrent saccades.     

Head movements evoked by electrical stimulation in the frontal eye field of the monkey: evidence for independent eye and head control

When the head is free to move, electrical stimulation in the frontal eye field (FEF) evokes eye and head movements. However, it is unclear whether FEF stimulation-evoked head movements contribute to shifting the line of sight, like visually guided coordinated eye-head gaze shifts. Here we investigated this issue by systematically varying initial eye (IEP) and head (IHP) positions at stimulation onset. Despite the large variability of IEP and IHP and the extent of stimulation-evoked gaze amplitudes, gaze displacement was entirely accounted for by eye (re head) displacement. Overall, the majority (3/4) of stimulation-evoked gaze shifts consisted of eye-alone movements, in which head movements were below the detection threshold. When head movements did occur, they often started late (re gaze shift onset) and coincided with rapid eye deceleration, resulting in little change in the ensuing gaze amplitudes. These head movements often reached their peak velocities over 100 ms after the end of gaze shifts, indicating that the head velocity profile was temporally dissociated from the gaze drive. Interestingly, head movements were sometimes evoked by FEF stimulation in the absence of gaze shifts, particularly when IEP was deviated contralaterally (re the stimulated side) at stimulation onset. Furthermore, head movements evoked by FEF stimulation resembled a subset of head movements occurring during visually guided gaze shifts. These unique head movements minimized the eye deviation from the center of the orbit and contributed little to gaze shifts. The results suggest that head motor control may be independent from eye control in the FEF.