Graham R. Barnes

The mechanism of prediction in human smooth pursuit eye movements

1. Experiments have been conducted on human subjects to determine the role of prediction in smooth eye movement control. Subjects were required to actively pursue a small target or stare passively at a larger display as it moved in the horizontal plane. 2. Target motion was basically periodic, but, after a random number of cycles an unexpected change was made in the amplitude, direction or frequency of target motion. Initially, the periodic stimulus took the form of a square waveform. In subsequent experiments, a triangular or sawtooth waveform was used, but in order to examine the timing of the response in relation to stimulus appearance, the target was tachistoscopically illuminated for 40‐320 ms at the time that it passed through the mid‐line position. 3. When subjects either actively pursued the target or stared passively at the larger display a characteristic pattern of steady‐state eye movement was evoked composed of two phases, an initial build‐up of eye velocity that reached a peak after 200 ms, followed by a decay phase with a time constant of 0.5‐2 s. The build‐up phase was initiated prior to target displacement for square‐wave motion and before onset of target illumination for other waveforms. 4. The peak eye velocity evoked gradually increased over the first two to four cycles of repeated stimulation. Simultaneously, the response became more phase advanced, the reaction time between stimulus onset and the time at which peak velocity occurred decreasing from an average of 300 to 200 ms for triangular waveform stimuli. 5. When there was a sudden and unexpected change in amplitude and direction of the stimulus waveform, the eye movement induced had a peak velocity and direction that was inappropriate for the current visual stimulus, but which was highly correlated with the features of the preceding sequence in the stimulus. 6. When there was a sudden change in the frequency of the stimulus waveform the predictive eye movement was induced with a timing appropriate to the periodicity of the previous sequence but inappropriate to the new sequence. 7. The results indicate that prediction is carried out through the storage of information about both the magnitude and timing of eye velocity. The trajectory of the averaged eye velocity response was similar in form irrespective of the duration of target exposure or basic stimulus frequency, suggesting that the predictive estimate is released as a stereotyped volley of constant duration but varying magnitude under the control of a periodicity estimator.(ABSTRACT TRUNCATED AT 400 WORDS)

Cognitive processes involved in smooth pursuit eye movements

Ocular pursuit movements allow moving objects to be tracked with a combination of smooth movements and saccades. The principal objective is to maintain smooth eye velocity close to object velocity, thus minimising retinal image motion and maintaining acuity. Saccadic movements serve to realign the image if it falls outside the fovea, the area of highest acuity. Pursuit movements are often portrayed as voluntary but their basis lies in processes that sense retinal motion and can induce eye movements without active participation. The factor distinguishing pursuit from such reflexive movements is the ability to select and track a single object when presented with multiple stimuli. The selective process requires attention, which appears to raise the gain for the selected object and/or suppress that associated with other stimuli, the resulting competition often reducing pursuit velocity. Although pursuit is essentially a feedback process, delays in motion processing create problems of stability and speed of response. This is countered by predictive processes, probably operating through internal efference copy (extra-retinal) mechanisms using short-term memory to store velocity and timing information from prior stimulation. In response to constant velocity motion, the initial response is visually driven, but extra-retinal mechanisms rapidly take over and sustain pursuit. The same extra-retinal mechanisms may also be responsible for generating anticipatory smooth pursuit movements when past experience creates expectancy of impending object motion. Similar, but more complex, processes appear to operate during periodic pursuit, where partial trajectory information is stored and released in anticipation of expected future motion, thus minimising phase errors associated with motion processing delays.

Fast, anticipatory smooth-pursuit eye movements appear to depend on a short-term store.

Abstract Anticipatory smooth pursuit before the expected appearance of a moving target can reduce the initial retinal blur caused by the 100-ms delay of visual feedback. Humans, though, can only voluntarily generate smooth velocities up to about 5°/s without a moving target. However, previous experiments have shown that repetitive brief presentations of a moving target every few seconds appear to charge an internal store, the contents of which can later be released to generate higher velocity anticipatory movements. This store’s longevity was assessed here by repetitively presenting a moving target for 500 ms at different known intervals up to 7.2 s. Target motion at 25°/s or 50°/s was tested, with presentations in alternate directions or the same direction. Anticipatory velocity, measured 100 ms after target onset, decreased with increasing interval for all target motion conditions. A decrease was still seen when accurate timing cues were given before each presentation, suggesting that the drive for anticipatory pursuit is held in a short-term store lasting a few seconds which can enhance the low velocities produced by volition alone. The results also demonstrate that high-velocity anticipatory pursuit helps to overcome the temporal delays in the system and allows target velocity to be matched at an earlier time.

Volitional control of anticipatory ocular pursuit responses under stabilised image conditions in humans.

Ocular pursuit responses have been examined in humans in three experiments in which the pursuit target image has been fully or partially stabilised on the fovea by feeding a recorded eye movement signal back to drive the target motion. The objective was to establish whether subjects could volitionally control smooth eye movement to reproduce trajectories of target motion in the absence of a concurrent target motion stimulus. In experiment 1 subjects were presented with a target moving with a triangular waveform in the horizontal axis with a frequency of 0.325 Hz and velocities of ± 10–50°/s. The target was illuminated twice per cycle for pulse durations (PD) of 160–640 ms as it passed through the centre position; otherwise subjects were in darkness. Subjects initially tracked the target motion in a conventional closed-loop mode for four cycles. Prior to the next target presentation the target image was stabilised on the fovea, so that any target motion generated resulted solely from volitional eye movement. Subjects continued to make anticipatory smooth eye movements both to the left and the right with a velocity trajectory similar to that observed in the closed-loop phase. Peak velocity in the stabilised-image mode was highly correlated with that in the prior closed-loop phase, but was slightly less (84% on average). In experiment 2 subjects were presented with a continuously illuminated target that was oscillated sinusoidally at frequencies of 0.2–1.34 Hz and amplitudes of ± 5–20°. After four cycles of closed-loop stimulation the image was stabilised on the fovea at the time of peak target displacement. Subjects continued to generate an oscillatory smooth eye velocity pattern that mimicked the sinusoidal motion of the previous closed-loop phase for at least three further cycles. The peak eye velocity generated ranged from 57–95% of that in the closed-loop phase at frequencies up to 0.8 Hz but decreased significantly at 1.34 Hz. In experiment 3 subjects were presented with a stabilised display throughout and generated smooth eye movements with peak velocity up to 84°/s in the complete absence of any prior external target motion stimulus, by transferring their attention alternately to left and right of the centre of the display. Eye velocity was found to be dependent on the eccentricity of the centre of attention and the frequency of alternation. When the target was partially stabilised on the retina by feeding back only a proportion (Kf = 0.6–0.9) of the eye movement signal to drive the target, subjects were still able to generate smooth movements at will, even though the display did not move as far or as fast as the eye. Peak eye velocity decreased as Kf decreased, suggesting that there was a continuous competitive interaction between the volitional drive and the visual feedback provided by the relative motion of the display with respect to the retina. These results support the evidence for two separate mechanisms of smooth eye movement control in ocular pursuit: reflex control from retinal velocity error feedback and volitional control from an internal source. Arguments are presented to indicate how smooth pursuit may be controlled by matching a voluntarily initiated estimate of the required smooth movement, normally derived from storage of past re-afferent information, against current visual feedback information. Such a mechanism allows preemptive smooth eye movements to be made that can overcome the inherent delays in the visual feedback pathway.

Interaction of active and passive slow eye movement systems

SummaryIndependent target and background motions have been used to generate conflicting activity within the pursuit and optokinetic systems. Subjects were required to pursue a small target against a structured background which moved independently. Selective enhancement of the response to the target generated high-gain active pursuit which dominated the eye movements. Passive eye movements induced during relative target and background motion are not normally directly quantifiable due to their low gain. By reducing the gain of the active pursuit optokinetically induced eye movements were enhanced and quantified. Three techniques are described for degrading active pursuit: tachistoscopic, eccentric and pseudorandom methods of target presentation. Our results demonstrate the synchronous input of active and passive eye movement drives to the oculomotor system and illustrate their interaction.

Cognitive processes involved in smooth pursuit eye movements: behavioral evidence, neural substrate and clinical correlation.

Smooth-pursuit eye movements allow primates to track moving objects. Efficient pursuit requires appropriate target selection and predictive compensation for inherent processing delays. Prediction depends on expectation of future object motion, storage of motion information and use of extra-retinal mechanisms in addition to visual feedback. We present behavioral evidence of how cognitive processes are involved in predictive pursuit in normal humans and then describe neuronal responses in monkeys and behavioral responses in patients using a new technique to test these cognitive controls. The new technique examines the neural substrate of working memory and movement preparation for predictive pursuit by using a memory-based task in macaque monkeys trained to pursue (go) or not pursue (no-go) according to a go/no-go cue, in a direction based on memory of a previously presented visual motion display. Single-unit task-related neuronal activity was examined in medial superior temporal cortex (MST), supplementary eye fields (SEF), caudal frontal eye fields (FEF), cerebellar dorsal vermis lobules VI–VII, caudal fastigial nuclei (cFN), and floccular region. Neuronal activity reflecting working memory of visual motion direction and go/no-go selection was found predominantly in SEF, cerebellar dorsal vermis and cFN, whereas movement preparation related signals were found predominantly in caudal FEF and the same cerebellar areas. Chemical inactivation produced effects consistent with differences in signals represented in each area. When applied to patients with Parkinsons disease (PD), the task revealed deficits in movement preparation but not working memory. In contrast, patients with frontal cortical or cerebellar dysfunction had high error rates, suggesting impaired working memory. We show how neuronal activity may be explained by models of retinal and extra-retinal interaction in target selection and predictive control and thus aid understanding of underlying pathophysiology.

Progressive bradykinesia and hypokinesia of ocular pursuit in Parkinson’s disease

OBJECTIVES Patients with Parkinson’s disease characteristically have difficulty in sustaining repetitive motor actions. The purpose of this study was to establish if parkinsonian difficulty with sustaining repetitive limb movements also applies to smooth ocular pursuit and to identify any pursuit abnormalities characteristic of Parkinson’s disease. METHODS Ocular pursuit in seven patients with moderate to severe bradykinesia predominant Parkinson’s disease was compared with seven age matched controls. Predictive and non-predictive pursuit of constant velocity target ramps were examined. Subjects pursued intermittently illuminated 400/s ramps sweeping to the left or right with an exposure duration of 480 ms and average interval of 1.728 s between presentations. To examine for any temporal changes in peak eye velocity, eye displacement or anticipatory smooth pursuit the 124 s duration of each record was divided into four epochs (E1, E2, E3, E4), each lasting 31 s and containing 18 ramp stimuli. Three test conditions were examined in each subject: predictive (PRD1), non-predictive (NPD), and predictive (PRD2) in that order. RESULTS Both patients and controls initiated appropriate anticipatory pursuit before target onset in the PRD1 and PRD2 conditions that enhanced the response compared with the NPD condition. The distinctive findings in patients with Parkinson’s disease were a reduction in response magnitude compared with controls and a progressive decline of response with stimulus repetition. The deficits were explained on the basis of easy fatiguability in Parkinson’s disease. CONCLUSIONS Ocular pursuit shows distinct anticipatory movements in Parkinson’s disease but peak velocity and displacement are reduced and progressively decline with repetition as found with limb movements.

Smooth ocular pursuit during the transient disappearance of an accelerating visual target: the role of reflexive and voluntary control

This study examined the extent to which human subjects predict future target motion for the control of smooth ocular pursuit. Subjects were required to pursue an accelerating target (0, 4 or 8°/s2) that underwent a transient occlusion, and consequently reappeared with the same or increased velocity. Presentations were received in a random or blocked order. Subjects exhibited anticipatory smooth pursuit prior to target motion onset, which in blocked presentations was scaled to the velocity generated by the target acceleration. In random presentations subjects also exhibited anticipatory smooth pursuit, but this was reflected in a more generalized response. During the transient occlusion all subjects exhibited a reduction in eye velocity, which was followed in the majority by a recovery prior to target reappearance. In random presentations, eye velocity decayed and recovered to a level that followed on from the response to the initial ramp. In blocked presentations, there was evidence of improved scaling throughout, which culminated in a significant increase in eye velocity between the start and end of the transient occlusion (8°/s2 only). These findings are difficult to reconcile with reflexive accounts of oculomotor control that perpetuate current eye motion, and hence generate a simple form of prediction using a direct efference copy (“eye-velocity memory”). Rather, they are more consistent with the scaling of smooth pursuit eye movements by means of a more-persistent velocity-based representation, which plays a significant role in both random and blocked stimulus presentations.

Anticipatory control of hand and eye movements in humans during oculo-manual tracking

Anticipatory activity of hand and eye has been examined during oculo‐manual tracking of a constant velocity visual target with a hand cursor. Both target and cursor were presented briefly (< 480 ms), but repeatedly, at regular inter‐stimulus intervals (ISI). In Expt 1, the build‐up of hand and eye responses was examined for target velocities varying from 10–40 deg s−1 with an ISI of 2.4 s. The velocity 100 ms after target onset (i.e. prior to visual feedback) for both hand and eye (V100) progressively increased over the first four presentations but then attained a steady state (SS). SS V100 values for eye and hand increased in proportion to target velocity and were thus predictive of forthcoming movement. Hand velocity exceeded eye velocity but both exhibited similar anticipatory trajectories. In Expt 2, target velocity was constant (40 deg s−1) but ISI varied from 0.48–3.74 s. Subjects made anticipatory eye movements for all ISIs but hand movements were often reactive at the longest ISI. If the target failed to appear as expected, subjects initiated predictive hand and eye responses with timing appropriate for the prevailing ISI. In Expt 3, predictive responses were compared with responses to randomised presentation. Peak hand velocity was greater in the randomised mode than in the predictive condition, whereas the converse was true for peak eye velocity. This difference is discussed in terms of the mechanisms of positional error correction in hand and eye. Results provide evidence of similar anticipatory mechanisms in hand and eye, using storage of velocity and timing to achieve rapid prediction of target motion.

Oculomotor prediction of accelerative target motion during occlusion: long-term and short-term effects.

The present study examined the influence of long-term (i.e., between-trial) and short-term (i.e., within-trial) predictive mechanisms on ocular pursuit during transient occlusion. To this end, we compared ocular pursuit of accelerative and decelerative target motion in trials that were presented in random or blocked-order. Catch trials in which target acceleration was unexpectedly modified were randomly interleaved in blocked-order trials. Irrespective of trial order, eye velocity decayed following target occlusion and then recovered towards the different levels of target velocity at reappearance. However, the recovery was better scaled in blocked-order trials than random-order trials. In blocked-order trials only, the reduced gain of smooth pursuit during occlusion was compensated by a change in saccade amplitude and resulted in total eye displacement (TED) that was well matched to target displacement. Subsidiary analysis indicated that three repeats of blocked-order trials was sufficient for participants to modify eye displacement compared to that exhibited in random-order trials, although more trials were required before end-occlusion eye velocity was better scaled. Finally, we found that participants exhibited evidence of a scaled response to an unexpected change in target acceleration (i.e., catch trials), although there were also transfer effects from the preceding blocked-order trials. These findings are consistent with the suggestion that on-the-fly prediction (short-term effect) is combined with memorised information from previous trials (long-term effect) to generate a persistent and veridical prediction of occluded target motion.