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The contribution of the human PPC to the orienting of visuospatial attention during smooth pursuit.

Smooth pursuit eye movements function to stabilize the retinal image of small moving targets. In order for those targets to be foveated, however, they must first be "captured" by an attentional mechanism which then interacts with the oculomotor system. Cortical sites involved with producing smooth pursuit overlap with areas known to be involved in directing visuospatial attention, particularly the posterior parietal cortex (PPC). The goal of the current study was to characterize the contributions made by the left and right posterior parietal cortices (lPPC and rPPC) to the interaction between visuospatial attention and the generation of smooth pursuit eye movements. Transcranial magnetic stimulation (TMS) was used to temporarily disrupt each area at different times around target motion onset in a pursuit task that explicitly manipulated the covert orienting of attention. TMS over the lPPC, rPPC and a control site (the vertex) evoked a similar pattern of results, in that the earlier TMS delivery times caused a reduced pursuit latency compared to baseline measures, while TMS immediately prior to target motion onset resulted in latencies slower than baseline. In addition, however, TMS over the lPPC and rPPC (but not the vertex) preferentially influenced the generation of contralateral pursuit, with the lPPC doing so in a relatively time-independent manner, and the rPPC doing so in a time-dependent manner. This pattern of results implies that both the left and right PPC are directly involved in the interaction between attention and smooth pursuit preparation.

Adult↗

The influence of structured visual backgrounds on smooth-pursuit initiation, steady-state pursuit and smooth-pursuit termination.

Smooth-pursuit eye movements were recorded in two rhesus monkeys in order to compare the influence of structured visual backgrounds on smooth-pursuit initiation, steady-state pursuit and pursuit termination. Different target trajectories were used in order to study smooth-pursuit initiation and termination. The influence of visual backgrounds on pursuit initiation was characterized by recording ocular responses elicited by step-ramp target displacements starting from straight ahead. Pursuit termination was characterized by analysing the transition from steady-state smooth-pursuit to fixation when a centripetally directed target ramp was terminated by a small target step in the direction of the ramp as soon as the target had come close to the straightahead position. The quantification of steady-state pursuit was based on ocular responses elicited by either paradigm. In accordance with previous work, we found that the onset of smooth-pursuit eye movements was delayed and initial eye acceleration reduced in the presence of a structured visual background. Likewise, mean eye velocity during steady-state pursuit was reduced by structured visual backgrounds. However, neither the latency nor the time course of smooth-pursuit termination was altered when the homogeneous background was replaced by a structured visual background. The lack of sensitivity of pursuit termination to the presence of visual structured backgrounds supports a previous contention that pursuit termination is mediated by a process which is different from the ones mediating smooth-pursuit initiation and steady-state pursuit. The absence of any noticeable effect of structured backgrounds on pursuit termination suggests that at least the fast component of the optokinetic reflex is suppressed during pursuit termination.

Algorithms↗

Extraretinal signals in MSTd neurons related to volitional smooth pursuit.

Smooth pursuit (SP)-related neurons in the dorsal-medial part of medial superior temporal cortex (MSTd) carry extraretinal signals that may play a role in maintenance of SP once eye velocity matches target velocity. For example, it has not been determined whether the extraretinal signals reflect volitional SP commands or proprioception. The aim of this study was to test some potential sources of extraretinal signals in MSTd pursuit neurons. We tested 40 MSTd neurons during step-ramp SP with target blink conditions to show that they carried an extraretinal signal. To examine potential contributions from eye movements that might reflect proprioceptive feedback from eye muscles, we tested MSTd neurons during rotational vestibular ocular reflex in complete darkness (VORd). Vestibular stimulation was delivered in the earth horizontal plane to elicit reflex driven smooth eye movements that matched the speed and frequency of volitional SP. We also tested VOR in the light (VOR x 1) and cancellation of the VOR (VOR x 0). Our neurons were modulated during both SP and cancellation of the VOR. In contrast, MSTd smooth pursuit neurons with extraretinal signals were not significantly modulated during VORd (sensitivity < or = 0.10 spike/s/ degrees /s). This combination of properties is compatible with classifying these neurons as gaze-velocity related. Absence of modulation during VORd testing could be caused by cancellation of head and eye movement sensitivity or dependence of neuronal firing on volitional SP commands. Our results support the suggestion that modulation of SP-related MSTd neurons reflects volitional SP commands rather then eye movements generated by reflex pathways.

Animals↗

The use of auto-correlation function to quantify periodicity in smooth pursuit.

Smooth pursuit eye movement was recorded with a DC amplifier during horizontal sinusoidal target movement at 0.3, 0.6, 0.8, 1.0 and 1.2 Hz. Eye movement was digitalized at 100 Hz and 12 bits accuracy. The digitalized eye movements were analyzed by the auto-correlation function, and the auto-correlation coefficient was used to quantify periodicity. In 13 healthy volunteers, the auto-correlation coefficient was nearly equal to 1.0 at 0.3 Hz but gradually decreased as the target frequency increased. In 8 patients with various neurological disorders, the auto-correlation coefficient was significantly smaller at all target frequencies than in the healthy volunteers. Less periodicity, as indicated by the decreased auto-correlation coefficient, suggests a disorder in the control visual feedback mechanism in smooth pursuit.

Adult↗

Non-target influences on the initiation of smooth pursuit.

Smooth pursuit is usually regarded as a relatively stereotyped oculomotor response in which the early part of the response reflects primarily the properties of the visual stimulus and cortical motion processing. We have investigated pursuit initiation in human subjects using the gap paradigm to alter fixation conditions, and single stationary distractors to alter visual context. The results suggest that a number of processes, distinct from motion processing, are involved in pursuit initiation. The processes which are modified by gaps and distractors are closely related and interact with each other. They may be shared with the saccade system.

Adult↗

Smooth pursuit disorders.

Smooth pursuit is a relatively recent eye movement which has developed in frontal-eyed species. The smooth pursuit system is involved during foveal smooth pursuit, the 'rapid' component of OKN slow phase and VOR suppression. The cortical areas controlling smooth pursuit (at the temporo-parieto-occipital junction and in the FEF) send ipsilateral projections onto the pontine nuclei, mainly the DLPN, passing through the anterior part of the midbrain. A midbrain or DLPN lesion results in ipsilateral smooth pursuit impairment (i.e. decreased gain) (Table 1). After the pontine nuclei, all smooth pursuit pathways pass through the cerebellum. They project onto the flocculus, mainly contralaterally (first decussation of the lateral smooth pursuit circuitry), and bilaterally onto the posterior vermis. Eye velocity is encoded in the activity of the floccular Purkinje cells, whereas target velocity is encoded in that of the vermal Purkinje cells. Unilateral floccular lesions and posterior vermal lesions (involving both sides of this structure) result in ipsilateral and bilateral smooth pursuit impairment, respectively. The flocculus sends an ipsilateral inhibitory projection onto the MVN, the y-group nucleus and the SVN, controlling contralateral, upward and perhaps downward smooth pursuit, respectively. Alternatively, the downward smooth pursuit pathway could pass through the dentate nuclei. The MVN sends a contralateral excitatory projection onto the abducens nucleus (second decussation of the lateral smooth pursuit circuitry). These anatomical and physiological characteristics of lateral smooth pursuit pathways, in addition to the results of lesion studies, suggest that, besides the floccular inhibitory Purkinje cell, there is another inhibitory neurone in the circuitry preceding this cell, perhaps within the flocculus itself. The posterior vermis projects onto the fastigial nuclei, which also control smooth pursuit. These nuclei could send efferents to those periabducens cells involved in ipsilateral smooth pursuit. The final part of the pathways involved in vertical smooth pursuit could pass mainly through the BC, originating in the y-group nucleus for upward movement and in the SVN or the dentate nuclei for downward movement. Alternatively, a ventral tegmental tract could transmit upward smooth pursuit signals between the y-group nucleus and the oculomotor nucleus. The MLF also belongs to this vestibulo-oculomotor circuitry, but does not appear to be crucial for vertical smooth pursuit since this eye movement is only partially impaired after MLF lesions. Lastly, parallel to the direct vestibulo-ocular motor nuclei pathways, there are other pathways passing through the brain stem integrators, converting eye velocity signals to eye position signals during all eye movements, including smooth pursuit.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals↗

Eye tracking in schizophrenia: does the antisaccade task measure anything that the smooth pursuit task does not?

Smooth pursuit and antisaccade eye-tracking abnormalities have been proposed as endophenotypes for schizophrenia. However, it is not clear whether these tasks measure the same underlying abnormality. We hypothesised that these measures would be correlated. The association between smooth pursuit and antisaccade task performance was assessed in 50 schizophrenic patients, 80 unaffected first-degree relatives and 40 unaffected controls. Smooth pursuit measures included gain, number of saccades and a qualitative measure of smooth pursuit. The antisaccade distractibility error (ADE) score was the only measure of the antisaccade task. A significant correlation was found between reduced gain and an increased ADE score for all the subjects in the three groups combined. The total number of saccades was negatively correlated with the ADE score in the schizophrenic group, but positively in the relative group. Qualitative ratings of smooth pursuit correlated with the ADE score. Our results suggest that the antisaccade distractibility error score is related to gain and qualitative measures of smooth pursuit, although the relationship with number of saccades did not conform to this pattern. The finding may reflect a shared genetic liability, that affects both eye-tracking phenotypes. It is likely that both measures reflect frontal cortical dysfunction.

Adult↗

Initiation of disjunctive smooth pursuit in monkeys: evidence that Hering's law of equal innervation is not obeyed by the smooth pursuit system.

Monkeys generated disjunctive smooth pursuit eye movements when they tracked visual targets that moved toward or away from them. Eye acceleration was computed during the initial 100 msec of pursuit (the open-loop interval) for various target trajectories. The initial acceleration of either eye was a function of the target's motion with respect to that eye, regardless of whether or not the pursuit was conjugate or disjunctive, or performed with one eye occluded. Eye movements produced by fusional vergence could be separated temporally from eye movements produced by smooth pursuit using step-ramp paradigms. The separation of the two responses demonstrates that the fusional vergence system operates in parallel with the smooth pursuit system, presumably to minimize disparity, but not to generate disjunctive components of smooth pursuit eye movements.

Animals↗

Predicting 2D target velocity cannot help 2D motion integration for smooth pursuit initiation.

Smooth pursuit eye movements reflect the temporal dynamics of bidimensional (2D) visual motion integration. When tracking a single, tilted line, initial pursuit direction is biased toward unidimensional (1D) edge motion signals, which are orthogonal to the line orientation. Over 200 ms, tracking direction is slowly corrected to finally match the 2D object motion during steady-state pursuit. We now show that repetition of line orientation and/or motion direction does not eliminate the transient tracking direction error nor change the time course of pursuit correction. Nonetheless, multiple successive presentations of a single orientation/direction condition elicit robust anticipatory pursuit eye movements that always go in the 2D object motion direction not the 1D edge motion direction. These results demonstrate that predictive signals about target motion cannot be used for an efficient integration of ambiguous velocity signals at pursuit initiation.

Eye Movements↗

The occluded onset pursuit paradigm: prolonging anticipatory smooth pursuit in the absence of visual feedback.

Humans can produce anticipatory smooth pursuit (ASP) for a few hundred ms prior to the appearance of a moving target. Once visual feedback is available, however, it is difficult to distinguish ASP from the visually-driven response with which it merges. Here we have developed a paradigm that extends the anticipatory period to show unequivocally how ASP can evolve over periods of up to 600 ms before being influenced by visual feedback. ASP was evoked by repeated presentation of constant velocity (ramp) stimuli preceded by auditory cues. The target was occluded during the initial part of the ramp, so that when it became visible it had already moved to an eccentric position. The occlusion period (T occ) varied from 0 to 500 ms in 100 ms increments; for each period ramps were presented in blocks of 8 with velocity held constant at 8, 16, 24 or 32 degrees/s. Eye displacement trajectories showed that subjects attempted to match the unseen target trajectory with a mixture of saccades and smooth pursuit. The smooth component was initiated progressively earlier in relation to target appearance as T occ increased, leading to progressively higher ASP gains by the time the target became visible. This prolongation of ASP throughout the occlusion period reveals the underlying internal drive that produces it, a drive that under normal circumstances quickly becomes masked by visual feedback.

Cues↗

Paresis of contralateral smooth pursuit and normal vestibular smooth eye movements after unilateral brainstem lesions.

Pursuit and vestibular smooth eye movements were measured in patients with lesions of the caudal brainstem tegmentum identified by magnetic resonance imaging (MRI) and computed tomography (CT), with neuropathological correlation in 1 patient. Contralateral smooth pursuit gain was significantly lower than ipsilateral gain in each patient. Ipsilateral smooth pursuit gain was also subnormal in patients with unilateral pontine damage that caused slowing of ipsilateral saccades. Horizontal vestibulo-ocular reflex gain and phase were normal. These quantitative correlations indicate that lesions of the pontine tegmentum that paralyze ipsilateral saccades can spare the vestibulo-ocular reflex, and that smooth pursuit movement and the vestibulo-ocular reflex can be impaired independently by pontine or medullary lesions. In contrast to lesions at other sites, unilateral lesions of the pontine or medullary tegmentum impair contralateral smooth pursuit more than ipsilateral pursuit movements. These findings provide evidence that a double decussating pathway mediates smooth pursuit; the first decussation is from the pons to the cerebellum, and the second decussation is from the vestibular nucleus to the contralateral abducens nucleus.

Brain Diseases↗

The use of non-motion-based cues to pre-programme the timing of predictive velocity reversal in human smooth pursuit.

Human smooth pursuit eye movements are principally driven by visual feedback and cannot normally be initiated at will. However, when tracking periodic motion, smooth eye movements reverse direction prior to target reversal, driven by anticipation, not visual feedback. Here, we investigate cognitive control over such eye reversals. Target stimuli were discrete double ramps-constant speed (30 degrees /s) rightwards followed by similar leftward movement, reversal time ranging from 420 ms to 840 ms. Three experimental conditions were examined. In the precued condition, double ramps of randomised reversal time were presented. Prior to ramp presentation audio precues were given with an interval indicating start and reversal time of the unseen, upcoming double ramp. Subjects were able to use these cues to voluntarily control timing of anticipatory eye reversal, so that when occasional false precues gave underestimates of target reversal time, eye reversal occurred before target reversal. Precued eye reversal times were comparable to those in a second, predictable condition, in which double ramps with identical reversal time were given repeatedly without precues. In contrast, reversal occurred much later in a third, reactive condition, also without precues, when unexpected early target reversals occurred sporadically within a series having identical, predictable reversal times. The findings provide evidence that timing of anticipatory smooth eye movement, both at the start of the double-ramp and at its reversal, can be independently controlled at will using non-motion-based timing cues.

Brain↗

Oculomotor function in Wernicke-Korsakoff's syndrome: II. Smooth pursuit eye movements.

Smooth pursuit eye movements were studied in three patients with alcoholic Korsakoff's syndrome, one with Wernicke's encephalopathy, and an age-matched control. Horizontal smooth pursuit eye movements were abnormal in all patients: peak eye velocity and the ability to sustain smooth eye velocity were reduced. Also, smooth pursuit gain began to decrease at relatively low target velocities (i.e., 8-10 degrees). These data demonstrate a severe disturbance in smooth pursuit function long after the clinically apparent oculomotor abnormalities have passed.

Aging↗

Frame of reference transformations in motion perception during smooth pursuit eye movements.

Smooth pursuit eye movements change the retinal image velocity of objects in the visual field. In order to change from a retinocentric frame of reference into a head-centric one, the visual system has to take the eye movements into account. Studies on motion perception during smooth pursuit eye movements have measured either perceived speed or perceived direction during smooth pursuit to investigate this frame of reference transformation, but never both at the same time. We devised a new velocity matching task, in which participants matched both perceived speed and direction during fixation to that during pursuit. In Experiment 1, the velocity matches were determined for a range of stimulus directions, with the head-centric stimulus speed kept constant. In Experiment 2, the retinal stimulus speed was kept approximately constant, with the same range of stimulus directions. In both experiments, the velocity matches for all directions were shifted against the pursuit direction, suggesting an incomplete transformation of the frame of reference. The degree of compensation was approximately constant across stimulus direction. We fitted the classical linear model, the model of Turano and Massof (2001) and that of Freeman (2001) to the velocity matches. The model of Turano and Massof fitted the velocity matches best, but the differences between de model fits were quite small. Evaluation of the models and comparison to a few alternatives suggests that further specification of the potential effect of retinal image characteristics on the eye movement signal is needed.

Adult↗

Effects of fixation target timing on smooth-pursuit initiation.

We measured smooth pursuit and anticipatory smooth eye movements in four normal subjects, using step-ramp stimuli. Between trials, subjects fixated a motionless central target which disappeared before, after, or at the same time as the ramp stimulus appeared. We found that gaps or overlaps in the relative timing of fixation target offset and ramp onset neither expedited nor delayed the initiation of smooth pursuit. In contrast, anticipatory and smooth pursuit eye accelerations were influenced by the presence of a stationary foveal target; both were significantly higher when the fixation stimulus disappeared before ramp onset than when it disappeared after ramp onset.

Adult↗

Experimental and computational analysis of monkey smooth pursuit eye movements.

Smooth pursuit eye movements are guided by visual feedback and are surprisingly accurate despite the time delay between visual input and motor output. Previous models have reproduced the accuracy of pursuit either by using elaborate visual signals or by adding sources of motor feedback. Our goal was to constrain what types of signals drive pursuit by obtaining data that would discriminate between these two modeling approaches, represented by the "image motion model" and the "tachometer feedback" model. Our first set of experiments probed the visual properties of pursuit with brief square-pulse and sine-wave perturbations of target velocity. Responses to pulse perturbations increased almost linearly with pulse amplitude, while responses to sine wave perturbations showed strong saturation with increasing stimulus amplitude. The response to sine wave perturbations was strongly dependent on the baseline image velocity at the time of the perturbation. Responses were much smaller if baseline image velocity was naturally large, or was artificially increased by superimposing sine waves on pulse perturbations. The image motion model, but not the tachometer feedback model, could reproduce these features of pursuit. We used a revision of the image motion model that was, like the original, sensitive to both image velocity and image acceleration. Due to a saturating nonlinearity, the sensitivity to image acceleration declined with increasing image velocity. Inclusion of this nonlinearity was motivated by our experimental results, was critical in accounting for the responses to perturbations, and provided an explanation for the unexpected stability of pursuit in the presence of perturbations near the resonant frequency. As an emergent property, the revised image motion model was able to reproduce the frequency and damping of oscillations recorded during artificial feedback delays. Our second set of experiments replicated prior recordings of pursuit responses to multiple-cycle sine wave perturbations, presented over a range of frequencies. The image motion model was able to reproduce the responses to sine wave perturbations across all frequencies, while the tachometer feedback model failed at high frequencies. These failures resulted from the absence of image acceleration signals in the tachometer model. We conclude that visual signals related to image acceleration are important in driving pursuit eye movements and that the nonlinearity of these signals provides stability. Smooth pursuit thus illustrates that a plausible neural strategy for combating natural delays in sensory feedback is to employ information about the derivative of the sensory input.

Animals↗

Quantitative measurement of smooth pursuit eye movements.

Smooth pursuit eye movements were quantitatively assessed in 25 normal subjects and 22 patients. A laboratory digital computer was used to compute 200 eye velocity samples per second and to statistically compare these eye velocity measurements for five different object velocities. Of six statistics evaluated, mode eye velocity showed the least variability in normal subjects and was most frequently abnormal in patients. Compared to normal subjects, patients with brain stem degeneration and cerebellar-pontine angle tumors with brain stem compression had significant impairment of smooth pursuit. Patients with peripheral vestibular lesions and C-P angle tumors without brain stem compression did not have impaired smooth pursuit. These preliminary findings suggest that quantitative measurement of pursuit eye velocity can be a sensitive test for brain stem dysfunction.

Adult↗

Coordination of smooth pursuit and saccades.

Smooth pursuit and saccades are two components of tracking eye movements. Their coordination has usually been studied by investigating latencies of pursuit onset in response to a moving target appearing simultaneously with the disappearance of the stationary fixation target. The general finding from such studies has been that latencies of saccades and pursuit are different and reflect independent processes. We discuss several limitations of the used targets. In this paper, we study latencies of saccades and smooth pursuit in response to a moving target that overlaps in time with a pursued moving target. We find that saccades and pursuit changes are synchronized. Furthermore, pursuit changes are made fast. Directional changes occur almost entirely within the accompanying saccade. To explain the results we hypothesize a two-stage mechanism for the coordinated generation of saccades and pursuit.

Adult↗