Head-free Pursuit Research Articles

Target position relative to the head is essential for predicting head movement during head-free gaze pursuit.

Gaze pursuit is the coordinated movement of the eyes and head that allows humans and other foveate animals to track moving objects. The control of smooth pursuit eye movements when the head is restrained is relatively well understood, but how the eyes coordinate with concurrent head movements when the head is free remains unresolved. In this study, we describe behavioral tasks that dissociate head and gaze velocity during head-free pursuit in monkeys. Existing models of gaze pursuit propose that both eye and head movements are driven only by the perceived velocity of the visual target and are therefore unable to account for these data. We show that in addition to target velocity, the positions of the eyes in the orbits and the retinal position of the target are important factors for predicting head movement during pursuit. When the eyes are already near their limits, further pursuit in that direction will be accompanied by more head movement than when the eyes are centered in the orbits, even when target velocity is the same. The step-ramp paradigm, often used in pursuit tasks, produces larger or smaller head movements, depending on the direction of the position step, while gaze pursuit velocity is insensitive to this manipulation. Using these tasks, we can reliably evoke head movements with peak velocities much faster than the target's velocity. Under these circumstances, the compensatory eye movements, which are often called counterproductive since they rotate the eyes in the opposite direction, are essential to maintaining accurate gaze velocity.

The interaction of visual, vestibular and extra‐retinal mechanisms in the control of head and gaze during head‐free pursuit

The ability to co-ordinate the eyes and head when tracking moving objects is important for survival. Tracking with eyes alone is controlled by both visually dependent and extra-retinal mechanisms, the latter sustaining eye movement during target extinction. We investigated how the extra-retinal component develops at the beginning of randomised responses during head-free pursuit and how it interacts with the vestibulo-ocular reflex (VOR). Subjects viewed horizontal step-ramp stimuli which occurred in pairs of identical velocity; velocity was randomised between pairs, ranging from ±5 to 40 deg s−1. In the first of each pair (short-ramp extinction) the target was visible for only 150 ms. In the second (initial extinction), after a randomised fixation period, the target was extinguished at motion onset, remaining invisible for 750 ms before reappearing for the last 200 ms of motion. Subjects used motion information acquired in the short-ramp extinction presentation to track the target from the start of unseen motion in the initial extinction presentation, using extra-retinal drive to generate smooth gaze and head movements scaled to target velocity. Gaze velocity rose more slowly than when visually driven, but had similar temporal development in head-free and head-fixed conditions. The difference in eye-in-head velocity between head-fixed and head-free conditions was closely related to head velocity throughout its trajectory, implying that extra-retinal drive was responsible for countermanding the VOR in the absence of vision. Thus, the VOR apparently remained active during head-free pursuit with near-unity gain. Evidence also emerged that head movements are not directly controlled by visual input, but by internal estimation mechanisms similar to those controlling gaze.

Extraction of visual motion information for the control of eye and head movement during head-free pursuit

We investigated how effectively briefly presented visual motion could be assimilated and used to track future target motion with head and eyes during target disappearance. Without vision, continuation of eye and head movement is controlled by internal (extra-retinal) mechanisms, but head movement stimulates compensatory vestibulo-ocular reflex (VOR) responses that must be countermanded for gaze to remain in the direction of target motion. We used target exposures of 50–200 ms at the start of randomised step-ramp stimuli, followed by >400 ms of target disappearance, to investigate the ability to sample target velocity and subsequently generate internally controlled responses. Subjects could appropriately grade gaze velocity to different target velocities without visual feedback, but responses were fully developed only when exposure was >100 ms. Gaze velocities were sustained or even increased during target disappearance, especially when there was expectation of target reappearance, but they were always less than for controls, where the target was continuously visible. Gaze velocity remained in the direction of target motion throughout target extinction, implying that compensatory (VOR) responses were suppressed by internal drive mechanisms. Regression analysis revealed that the underlying compensatory response remained active, but with gain slightly less than unity (0.85), resulting in head-free gaze responses that were very similar to, but slightly greater than, head-fixed. The sampled velocity information was also used to grade head velocity, but in contrast to gaze, head velocity was similar whether the target was briefly or continuously presented, suggesting that head motion was controlled by internal mechanisms alone, without direct influence of visual feedback.

Eye-Pursuit and Reafferent Head Movement Signals Carried by Pursuit Neurons in the Caudal Part of the Frontal Eye Fields during Head-Free Pursuit

Eye and head movements are coordinated during head-free pursuit. To examine whether pursuit neurons in frontal eye fields (FEF) carry gaze-pursuit commands that drive both eye-pursuit and head-pursuit, monkeys whose heads were free to rotate about a vertical axis were trained to pursue a juice feeder with their head and a target with their eyes. Initially the feeder and target moved synchronously with the same visual angle. FEF neurons responding to this gaze-pursuit were tested for eye-pursuit of target motion while the feeder was stationary and for head-pursuit while the target was stationary. The majority of pursuit neurons exhibited modulation during head-pursuit, but their preferred directions during eye-pursuit and head-pursuit were different. Although peak modulation occurred during head movements, the onset of discharge usually was not aligned with the head movement onset. The minority of neurons whose discharge onset was so aligned discharged after the head movement onset. These results do not support the idea that the head-pursuit–related modulation reflects head-pursuit commands. Furthermore, modulation similar to that during head-pursuit was obtained by passive head rotation on stationary trunk. Our results suggest that FEF pursuit neurons issue gaze or eye movement commands during gaze-pursuit and that the head-pursuit–related modulation primarily reflects reafferent signals resulting from head movements.

Further evidence for selective difficulty of upward eye pursuit in juvenile monkeys: effects of optokinetic stimulation, static roll tilt, and active head movements

The smooth-pursuit system moves the eyes in space accurately to track slowly moving objects of interest despite visual inputs from the moving background and/or vestibular inputs during head movements. Recently, our laboratory has shown that young primates exhibit asymmetric eye movements during vertical pursuit across a textured background; upward eye velocity gain is reduced. To further understand the nature of this asymmetry, we performed three series of experiments in young monkeys. In Experiment 1, we examined whether this asymmetry was due to an un-compensated downward optokinetic reflex induced by the textured background as it moves across the retina in the opposite direction of the pursuit eye movements. For this, we examined the monkeys' ability to fixate a stationary spot in space during movement of the textured background and compared it with vertical pursuit across the stationary textured background. We also examined gains of optokinetic eye movements induced by downward motion of the textured background during upward pursuit. In both task conditions, gains of downward eye velocity induced by the textured background were too small to explain reduced upward eye velocity gains. In Experiment 2, we examined whether the frame of reference for low-velocity, upward pursuit was orbital or earth vertical. To test this, we first applied static tilt in the roll plane until the animals were nearly positioned on their side in order to dissociate vertical or horizontal eye movements in the orbit from those in space. Deficits were observed for upward pursuit in the orbit but not in space. In Experiment 3, we tested whether asymmetry was observed during head-free pursuit that requires coordination between eye and head movements. Asymmetry in vertical eye velocity gains was still observed during head-free pursuit although it was not observed in vertical head velocity. These results, taken together, suggest that the asymmetric eye movements during vertical pursuit are specific for upward, primarily eye pursuit in the orbit.

Abnormalities of smooth eye and head movement control in parhson's disease

The control of horizontal head and eye movements was examined in 13 nondemented patients with Parkinson's disease (PD) of mild to moderate severity. During pursuit of single-frequency sine waves, smooth component eye velocity was lower in the PD group at frequencies of 1.2 Hz and above; but the differences in overall eye displacement were even greater, indicating an impaired ability to generate catch-up saccades at high frequencies. A corresponding deficit in saccadic performance was observed during a high-frequency saccadic tracking task where predictive saccades of reduced gain and variable timing were generated. During pursuit of pseudo-random target motion with varying degrees of predictability, small differences in smooth component eye velocity were observed, but prediction was otherwise well preserved in the patient group. Vestibulo-ocular reflex (VOR) suppression was also normal during head-free pursuit. No major improvement in smooth pursuit gain could be attributed to drug treatment, based on a comparison of patient results before and after administration of levodopa.

Predictive Mechanisms of Head-Eye Coordination and Vestibulo-Ocular Reflex Suppression in Humans

Head and eye movements of human subjects have been recorded during head-free pursuit in the horizontal plane of a target executing sinusoidal motion at a frequency of 0.26 to 0.78 Hz and a peak velocity of +/- 96 degrees/s. The target was not presented continuously but was exposed for brief durations of 120 to 320 ms as it passed through the centre of the visual field at peak velocity. This technique allowed the timing of each response to be assessed in relation to the onset of target appearance. During the first 3 to 4 target presentations, there was a progressive buildup of both head velocity and the smooth component of gaze velocity, while, simultaneously, the responses became more phase-advanced with respect to target onset. In the steady state, similar temporal response trajectories were observed for head and gaze velocity, which were initiated approximately 500 ms prior to target onset, rose to a peak that increased with the duration of target exposure, and then decayed with a time constant of 0.5 to 1 s. Whenever the target failed to appear as expected, the gaze and head velocity trajectories continued to be made, indicating that predictive suppression of the vestibulo-ocular reflex (VOR) was taking place in darkness. In a further experiment, subjects attempted to suppress the VOR during whole body oscillation at 0.2 or 0.4 Hz on a turntable by fixating a head-fixed target that appeared for 10 to 160 ms at the time of peak head velocity. Again, VOR suppression was initiated prior to target appearance in the same manner as for natural head movements, and when the target suddenly disappeared but rotation continued, predictive VOR suppression was observed in darkness. The similarity of these predictive effects to those obtained previously for head-fixed pursuit provides further support for the hypothesis that both pursuit and visual suppression of the VOR are controlled primarily by identical visual feedback mechanisms.

The role of prediction in head-free pursuit and vestibuloocular reflex suppression.

Annals of the New York Academy of SciencesVolume 656, Issue 1 p. 687-694 The Role of Prediction in Head-Free Pursuit and Vestibuloocular Reflex Suppression G. R. BARNES, G. R. BARNES MRC Human Movement & Balance Unit National Hospital Queen Square London WC1N 3BG, EnglandSearch for more papers by this authorM. A. GREALY, M. A. GREALY MRC Human Movement & Balance Unit National Hospital Queen Square London WC1N 3BG, EnglandSearch for more papers by this author G. R. BARNES, G. R. BARNES MRC Human Movement & Balance Unit National Hospital Queen Square London WC1N 3BG, EnglandSearch for more papers by this authorM. A. GREALY, M. A. GREALY MRC Human Movement & Balance Unit National Hospital Queen Square London WC1N 3BG, EnglandSearch for more papers by this author First published: May 1992 https://doi.org/10.1111/j.1749-6632.1992.tb25245.xCitations: 2AboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinked InRedditWechat Citing Literature Volume656, Issue1Sensing and Controlling Motion: Vestibular and Sensorimotor FunctionMay 1992Pages 687-694 RelatedInformation

Gaze control during head-free pursuit in patients with loss of vestibular function.

Studies of gaze control in labyrinthine-deficient (LD) patients have revealed a variety of adaptive mechanisms that may be used to compensate for loss of the vestibuloocular reflex (VOR), including central preprogramming of eye movements and the potentiation of the pursuit, optokinetic, and cervicoocular reflexes. To investigate the mechanisms that compensate for loss of the VOR during head-free pursuit we examined the responses to pursuit of pseudorandom target motion in LD patients under head-free and head-fixed conditions, using a stimulus that covers the frequency range of normal head-free pursuit movements.

Visual-Vestibular Interaction During Head-Free Pursuit of Pseudorandom Target Motion in Man1

Recordings of head and eye movement were made during pursuit of mixed-frequency, pseudorandom target motion to study the mechanism of vestibulo-ocular reflex (VOR) suppression during head-free pursuit. When high velocity stimuli were used, slow-phase gaze velocity gains decreased significantly with increases in both absolute target velocity and the velocity ratio between the frequency components. These changes occurred independently of changes in the head displacement gain, which remained relatively constant at the lower frequency and were directly attributable to impaired suppression of the VOR. Similar effects were seen when visual feedback was degraded by tachistoscopic illumination of the target. The results indicate that visual feedback, rather than an efference copy of the head velocity signal, is essential for suppression of slow-phase vestibular eye movement during head-free pursuit. When head-free and head-fixed pursuit were compared, striking similarities were seen for both slow phase gaze velocity gain and phase, indicating that gaze control during smooth pursuit is largely independent of the degree of associated head movement. This suggests that the VOR is not switched off during head-free pursuit. An estimate of the underlying VOR gain was obtained by recording the vestibular response produced by active head movements in darkness. The rather higher estimates of VOR gain obtained using an imaginary earth-fixed target paradigm were found to predict head-free gains more closely than the gains obtained during imaginary pursuit of a moving target, suggesting that such measures may be more representative of the underlying VOR gain.

Vestibulo-ocular Reflex Suppression during High Velocity Head-free Pursuit in Normal Subjects

Recordings of head and smooth pursuit eye movement were made during head-free pursuit of a pseudo-random target motion stimulus. The pseudo-random stimulus was composed of 2 high velocity sinusoids, of frequency 0.4 and 1.3 Hz, with the velocity of the higher frequency being varied as a ratio of the lower frequency velocity between 0 and 2. Slow-phase gaze velocity gain for the lower frequency component decreased significantly with an increase in velocity ratio, and with an increase in target velocity above 60 degrees/s. Gaze velocity gain was frequently less than head displacement gain which remained fairly constant, indicating that the eyes had been driven in the opposite direction to head movement as a result of inability of suppress the vestibulo-ocular reflex. Similar effects were seen when visual feedback was degraded by tachistoscopic illumination of a target composed of 2 low velocity sinusoids (0.11 and 0.13 Hz). These results indicate that visual feedback, rather than head displacement, is essential for suppression of slow-phase vestibular eye movement during head-free pursuit, even at high stimulus velocities.

Head-free pursuit in the human of a visual target moving in a pseudo-random manner.

1. Head and eye movements have been recorded in man during head-free pursuit of a target moving in a pseudo-random manner in the horizontal plane with a motion stimulus composed of the sum of four sinusoids. 2. In an initial experiment the three lowest frequencies remained constant at 0.11, 0.24 and 0.37 Hz, whilst the highest frequency (F4) took values of 0.39, 0.78, 1.56 and 2.08 Hz. Peak velocity of each component was 10 deg/s. When F4 was 0.39 Hz gaze displacement (i.e. the sum of head and eye displacement) was relatively smooth and had a mean velocity gain of 0.95. As F4 was increased gaze displacement contained more saccadic activity and gaze velocity gain for the three lower-frequency components was significantly (P less than 0.001) reduced to a minimum level of 0.66 when F4 was 1.56 Hz. 3. A similar reduction in gain of the lower-frequency components was obtained when the velocity of F4 was increased as a ratio of the velocity of the lower frequencies from 0 to 4. 4. When the frequency composition of the stimulus was varied so that the two highest frequencies were closely spaced, gaze velocity gain for the highest frequency was always significantly higher than that of the next lower frequency, indicating a true enhancement of the highest-frequency component. 5. Changing the lowest-frequency component of the stimulus resulted in a significant shift in the gaze velocity phase profile as a function of frequency, so that phase advance was always associated with the lowest frequency even when this was as high as 0.89 Hz. 6. These changes in gain and phase of gaze velocity with the frequency content of the stimulus were similar to those previously described for head-fixed pursuit and visual suppression of the vestibulo-ocular reflex (VOR) and implicate the frequency-dependent, non-linear visual feed-back mechanisms in gaze control. 7. A number of the non-linear characteristics of gaze velocity were also observed in a somewhat modified form in the head displacement gains and phases, implying that the drive to the neck muscles is also derived from the same non-linear visual feed-back source. 8. The role of the VOR in head-free pursuit was tested by exposing the subject to whole-body motion on a turntable which countered the volitional head movement generated by the subject.(ABSTRACT TRUNCATED AT 400 WORDS)

Head-free pursuit of pseudo-random target motion.

Experiments have been conducted in which subjects were required to pursue a target moving in the horizontal plane with co-ordinated movements of the head and eyes. Target motion was pseudo-random in form, composed of four sinusoids. The three lower frequencies of the stimulus were maintained at 0.11, 0.24 and 0.37 Hz with a peak velocity of 10 degrees/s, whilst the frequency and velocity of the highest frequency component (F4) were varied. When all frequencies were below 0.4 Hz, eye movements were smooth and gaze velocity gain was high (0.95), but when F4 was increased up to 1.56 Hz or when the velocity of F4 was increased up to 40 degrees/s, gaze velocity gain decreased significantly. When voluntary head movements were countered by whole-body rotation to eliminate the input to the semicircular canals, gaze velocity gain increased because there was no longer any requirement to suppress the vestibulo-ocular response to head rotation. The results are in accord with those of previous experiments involving head-fixed pursuit and vestibulo-ocular suppression.

Relationship between eye acceleration and retinal image velocity during foveal smooth pursuit in man and monkey.

Relationship between eye acceleration and retinal image velocity during foveal smooth pursuit in man and monkey.