Saccade Initiation Research Articles

The influence of motivational salience on saccade latencies

Eye movements provide a direct link to study the allocation of overt attention to stimuli in the visual field. The initiation of saccades towards visual stimuli is known to be influenced by the bottom-up salience of stimuli as well as the motivational context of the task. Here, we asked whether the initiation of saccades is also influenced by the intrinsic motivational salience of a stimulus. Face stimuli were first associated with positive or negative motivational salience through instrumental learning. The same faces served as target stimuli in a subsequent saccade task, in which their motivational salience was no longer task-relevant. Participants performed either voluntary saccades, which required the selection of the saccade target out of two simultaneously presented stimuli (experiment 1), or reactive saccades, where only the target stimulus was presented (experiment 2). We found a specific effect of learned positive stimulus value on the latencies of voluntary saccades: For faces with high versus low positive motivational salience, saccadic latencies were significantly reduced. No such difference was observed for previously punished faces. In contrast, reactive saccades to both previously rewarded and punished faces were unaffected by learned stimulus value. Our findings show for the first time that saccadic preparation is susceptible to the acquired intrinsic motivational salience of visual stimuli. Based on the observation that only voluntary saccades but not reactive saccades were modulated, we conclude that the recruitment of neural processes for target identification is required to allow for an influence of motivational stimulus salience on saccadic preparation.

A Role for the Parietal Cortex in Sensorimotor Adaptation of Saccades

Sensorimotor adaptation ensures movement accuracy despite continuously changing environment and body. Adaptation of saccadic eye movements is a classical model of sensorimotor adaptation. Beside the well-established role of the brainstem-cerebellum in the adaptation of reactive saccades (RSs), the cerebral cortex has been suggested to be involved in the adaptation of voluntary saccades (VSs). Here, we provide direct evidence for a causal involvement of the parietal cortex in saccadic adaptation. First, the posterior intraparietal sulcus (pIPS) was identified in each subject using functional magnetic resonance imaging (fMRI). Then, a saccadic adaptation paradigm was used to progressively reduce the amplitude of RSs and VSs, while single-pulse transcranial magnetic stimulation (spTMS) was applied over the right pIPS. The perturbations of pIPS resulted in impairment for the adaptation of VSs, selectively when spTMS was applied 60 ms after saccade onset. In contrast, the adaptation of RSs was facilitated by spTMS applied 90 ms after saccade initiation. The differential effect of spTMS relative to saccade types suggests a direct interference with pIPS activity for the VS adaptation and a remote interference with brainstem-cerebellum activity for the RS adaptation. These results support the hypothesis that the adaptation of VSs and RSs involves different neuronal substrates.

Effect of Aging on Coordinated Eye and Hand Movements With Two-Segment Sequence

This study examined how aging compromises coordinative eye-hand movements with multiple segments. Older adults and young controls performed two-segment movements with the eyes only or with the eyes and hand together. The results showed minimal age-related changes on the initiation and execution of primary saccade during the first segment. However, the older adults showed a scaling problem of saccade velocity when hand movements were included. They were also slow in stabilizing gaze fixation to the first target. Regarding hand movements, the older adults pronouncedly increased the deceleration phase compared with the controls while fixating their gazes to the target. They also increased the intersegment interval for both eye and hand movements. Taken together, aging differentially affects various components of movements, which contributes to the slowness of overall performance.

Response variability of frontal eye field neurons modulates with sensory input and saccade preparation but not visual search salience

Discharge rate modulation of frontal eye field (FEF) neurons has been identified with a representation of visual search salience (physical conspicuity and behavioral relevance) and saccade preparation. We tested whether salience or saccade preparation are evident in the trial-to-trial variability of discharge rate. We quantified response variability via the Fano factor in FEF neurons recorded in monkeys performing efficient and inefficient visual search tasks. Response variability declined following stimulus presentation in most neurons, but despite clear discharge rate modulation, variability did not change with target salience. Instead, we found that response variability was modulated by stimulus luminance and the number of items in the visual field independently of attentional demands. Response variability declined to a minimum before saccade initiation, and presaccadic response variability was directionally tuned. In addition, response variability was correlated with the response time of memory-guided saccades. These results indicate that the trial-by-trial response variability of FEF neurons reflects saccade preparation and the strength of sensory input, but not visual search salience or attentional allocation.

Deterioration of horizontal saccades in progressive supranuclear palsy

ObjectiveTo investigate horizontal saccade changes according to disease stage in patients with progressive supranuclear palsy (PSP). MethodsWe studied visually and memory guided saccades (VGS and MGS) in 36 PSP patients at various disease stages, and compared results with those in 66 Parkinson’s disease (PD) patients and 58 age-matched normal controls. ResultsBoth vertical and horizontal saccades were affected in PSP patients, usually manifesting as “slow saccades” but sometimes as a sequence of small amplitude saccades with relatively well preserved velocities. Disease progression caused saccade amplitude reduction in PSP but not PD patients. In contrast, VGS and MGS latencies were comparable between PSP and PD patients, as were the frequencies of saccades to cue, suggesting that voluntary initiation and inhibitory control of saccades are similar in both disorders. Hypermetria was rarely observed in PSP patients with cerebellar ataxia (PSPc patients). ConclusionsThe progressively reduced accuracy of horizontal saccades in PSP suggests a brainstem oculomotor pathology that includes the superior colliculus and/or paramedian pontine reticular formation. In contrast, the functioning of the oculomotor system above the brainstem was similar between PSP and PD patients. SignificanceThese findings may reflect a brainstem oculomotor pathology.

Alteration of the timing of self‐initiated but not reactive saccades by electrical stimulation in the supplementary eye field

Although we can generate movements whenever we feel like doing so, the way in which neuronal signals regulate the timing of self-initiated movements remains elusive. There is evidence that the dorsomedial frontal cortex, including the supplementary eye field (SEF), is involved in the self-triggering of movements. Because the gradual evolution of cortical activity over the dorsomedial frontal cortex is known to reflect the temporal prediction of an upcoming event, we postulated that the timing of self-initiated movements is regulated by the time course of neuronal activity in the SEF. To test the causal role, we applied electrical microstimulation to the SEF when monkeys prepared for memory-guided saccades. Stimulation delayed the initiation of saccades when animals were required to make saccades 1200 ± 300 ms following the cue (self-timed task), but not when they generated memory-guided saccades in response to the offset of the fixation point (conventional task). As well as the increment in median saccade latencies, stimulation at ∼24% of sites also increased the occurrence of early erroneous saccades. Saccades facilitated by stimulation were always directed toward the cue, even when the cue was located away from the movement field. In contrast, stimulation to the frontal eye fields during saccade preparation exerted no effects in either task. These results suggest that the preparatory signals in the SEF may play a causal role in regulating the timing rather than the direction of self-initiated saccades.

Saccadic inhibition is accompanied by large and complex amplitude modulations when induced by visual backward masking

Saccadic inhibition refers to the strong temporary decrease in saccadic initiation observed when a visual distractor appears shortly after the onset of a saccadic target. Here, to gain a better understanding of this phenomenon, we assessed whether saccade amplitude changes could accompany these modulations of latency distributions. As previous studies on the saccadic system using visual backward masking--a protocol in which the mask appears shortly after the target--showed latency increases and amplitude changes, we suspected that this could be a condition in which amplitude changes would accompany saccadic inhibition. We show here that visual backward masking produces a strong saccadic inhibition. In addition, this saccadic inhibition was accompanied by large and complex amplitude changes: a first phase of gain decrease occurred before the saccadic inhibition; when saccades reappeared after the inhibition, they were accurate before rapidly entering into a second phase of gain decrease. We observed changes in saccade kinematics that were consistent with the possibility of saccades being interrupted during these two phases of gain decrease. These results show that the onset of a large stimulus shortly after a first one induces the previously reported saccadic inhibition, but also induces a complex pattern of amplitude changes resulting from a dual amplitude perturbation mechanism with fast and slow components.

Action effects in saccade control

According to the ideomotor principle, action preparation involves the activation of associations between actions and their effects. However, there is only sparse research on the role of action effects in saccade control. Here, participants responded to lateralized auditory stimuli with spatially compatible saccades toward peripheral targets (e.g., a rhombus in the left hemifield and a square in the right hemifield). Prior to the imperative auditory stimulus (e.g., a left tone), an irrelevant central visual stimulus was presented that was congruent (e.g., a rhombus), incongruent (e.g., a square), or unrelated (e.g., a circle) to the peripheral saccade target (i.e., the visual effect of the saccade). Saccade targets were present throughout a trial (Experiment 1) or appeared after saccade initiation (Experiment 2). Results showed shorter response times and fewer errors in congruent (vs. incongruent) conditions, suggesting that associations between oculomotor actions and their visual effects play an important role in saccade control.

Electrophysiological recordings in humans reveal reduced location-specific attentional-shift activity prior to recentering saccades

Being able to effectively explore the visual world is of fundamental importance, and it has been suggested that the straight-ahead gaze position within the egocentric reference frame ("primary position") might play a special role in this context. In the present study we employed human electroencephalography (EEG) to examine neural activity related to the spatial guidance of saccadic eye movements. Moreover, we sought to investigate whether such activity would be modulated by the spatial relation of saccade direction to the primary gaze position (recentering saccades). Participants executed endogenously cued saccades between five equidistant locations along the horizontal meridian. This design allowed for the comparison of isoamplitude saccades from the same starting position that were oriented either toward the primary position (centripetal) or further away from it (centrifugal). By back-averaging time-locked to the saccade onset on each trial, we identified a parietally distributed, negative-polarity EEG deflection contralateral to the direction of the upcoming saccade. Importantly, this contralateral presaccadic negativity, which appeared to reflect the location-specific attentional guidance of the eye movement, was attenuated for recentering saccades relative to isoamplitude centrifugal saccades. This differential electrophysiological signature was paralleled by faster saccadic reaction times and was substantially more apparent when time-locking the data to the onset of the saccade rather than to the onset of the cue, suggesting a tight temporal association with saccade initiation. The diminished level of this presaccadic component for recentering saccades may reflect the preferential coding of the straight-ahead gaze position, in which both the eye-centered and head-centered reference frames are perfectly aligned and from which the visual world can be effectively explored.

Neuronal activity in the superior colliculus related to saccade initiation during coordinated gaze–reach movements

One must be quick and precise when foveating targets to be reached, because the eyes have to guide the hand trajectory by visual feedback, and we may miss a rapidly moving target if our grasping is not fast and accurate enough. To this end, our brains developed mechanisms coordinating gaze and hand movements to optimize the way in which we foveate and reach. One of these mechanisms is the facilitation of the primary saccade--proven in humans and confirmed here in monkeys--which allows the generation of short-latency gaze movements when reaching towards visual targets. Here we tested whether the neuronal activity in the superior colliculus (SC) accounts for this mechanism; alternatively, cortical saccade-related areas could play a major role in the fast initiation of saccades during such elaborated behaviours bypassing the SC. Upon presentation of a target, neurons located at the rostral pole of the SC started the saccade-related pause in their activity earlier in tasks involving coordinated gaze-reach movements than in tasks in which the saccades were made in isolation. In the same tasks neurons located at the caudal SC reached peak firing rates earlier in coordinated gaze-reach movements than with isolated saccades, confirming the tight coupling between their burst activity latencies and the saccadic reaction times. In sum, our results extend the role of the SC in saccade initiation to coordinated gaze-reach movements, identifying its activity as an important part of the distributed neural system for eye-hand coordination.

Frontal cortical regions controlling small and large amplitude saccades – A TMS study

Small and large amplitude saccades serve different functions in daily life, with the latter accompanied more frequently by head movements and blinks. They are presumably controlled differently by the frontal eye fields. To investigate the frontal cortical regions responsible for the initiation and inhibition of small and large amplitude saccades, we investigated the effects of transcranial magnetic stimulation (TMS) on antisaccades of different sizes (5° and 30°). While the subjects performed a specific task, we stimulated the bilateral frontal cortices at various locations overlying the frontal oculomotor regions, 100ms after the target presentation. A hemispheric asymmetry in TMS effect was noted, such that 5° saccades were delayed by TMS over both bilateral frontal cortices, whereas 30° saccades were delayed by TMS only over the left lateral frontal cortex. TMS also reduced the amplitude of 5° saccades over the bilateral frontal cortex, but 30° saccades were not significantly changed in amplitude. The frequency of erroneous prosaccades to targets was slightly decreased by TMS at 5°, but increased at 30°. The results suggest that 5° saccades are more susceptible to the effect of TMS than are 30° saccades. Furthermore, while bilateral frontal areas are involved in the initiation of antisaccades, especially of small amplitudes, the left lateral frontal cortex may subserve coordination of blinks and saccades, both of large and small amplitudes.

Effects of Anisometropic Amblyopia on Visuomotor Behavior, III: Temporal Eye-Hand Coordination during Reaching

To examine the effects of anisometropic amblyopia on the temporal pattern of eye-hand coordination during visually-guided reaching. Eighteen patients with anisometropic amblyopia and 18 control subjects were recruited. Participants executed reach-to-touch movements toward visual targets under three viewing conditions: binocular, monocular amblyopic eye, and monocular fellow eye viewing. Temporal coordination between eye and hand movements was examined during reach planning (interval between the initiation of saccade and reaching) and reach execution (interval between the initiation of saccade and reach peak velocity). The frequency and dynamics of secondary saccades were also examined. Patients with severe amblyopia spent a longer time planning the reaching response after fixating the target in comparison with control subjects and patients with mild amblyopia (P = 0.029). In comparison with control subjects, all patients extended the acceleration phase of the reach after target fixation (P = 0.018). Secondary (reach-related) saccades were initiated during the acceleration phase of the reach and patients executed these saccades with greater frequency than control subjects (P < 0.0001). The amplitude and peak velocity of reach-related saccades were higher when patients viewed with the amblyopic eye in comparison with the other viewing conditions (P < 0.001). This is the first study to show that patients with anisometropic amblyopia modified the temporal dynamics of eye-hand coordination during visually-guided reaching. They extended the planning and execution intervals after target fixation and increased the frequency of secondary, reach-related saccades. These may represent visuomotor strategies to compensate for the spatiotemporal visual deficits to achieve good reaching accuracy and precision.

Saccade Reaction Times Are Influenced by Caudate Microstimulation Following and Prior to Visual Stimulus Appearance

Several cognitive models suggest that saccade RTs are controlled flexibly not only by mechanisms that accumulate sensory evidence after the appearance of a sensory stimulus (poststimulus mechanisms) but also by mechanisms that preset the saccade control system before the sensory event (prestimulus mechanisms). Consistent with model predictions, neurons in structures tightly related to saccade initiation, such as the superior colliculus and FEF, have poststimulus and prestimulus activities correlated with RTs. It has been hypothesized that the BG influence the saccade initiation process by controlling both poststimulus and prestimulus activities of superior colliculus and FEF neurons. To examine this hypothesis directly, we delivered electrical microstimulation to the caudate nucleus, the input stage of the oculomotor BG, while monkeys performed a prosaccade (look toward a visual stimulus) and antisaccade (look away from the stimulus) paradigm. Microstimulation applied after stimulus appearance (poststimulus microstimulation) prolonged RTs regardless of saccade directions (contra/ipsi) or task instructions (pro/anti). In contrast, microstimulation applied before stimulus appearance (prestimulus microstimulation) shortened RTs, although the effects were limited to several task conditions. The analysis of RT distributions using the linear approach to threshold with ergodic rate model revealed that poststimulus microstimulation prolonged RTs by reducing the rate of rise to the threshold for saccade initiation, whereas fitting results for prestimulus microstimulation were inconsistent across different task conditions. We conclude that both poststimulus and prestimulus activities of caudate neurons are sufficient to control saccade RTs.

Investigating the role of the superior colliculus in active vision with the visual search paradigm

We review here both the evidence that the functional visuomotor organization of the optic tectum is conserved in the primate superior colliculus (SC) and the evidence for the linking proposition that SC discriminating activity instantiates saccade target selection. We also present new data in response to questions that arose from recent SC visual search studies. First, we observed that SC discriminating activity predicts saccade initiation when monkeys perform an unconstrained search for a target defined by either a single visual feature or a conjunction of two features. Quantitative differences between the results in these two search tasks suggest, however, that SC discriminating activity does not only reflect saccade programming. This finding concurs with visual search studies conducted in posterior parietal cortex and the idea that, during natural active vision, visual attention is shifted concomitantly with saccade programming. Second, the analysis of a large neuronal sample recorded during feature search revealed that visual neurons in the superficial layers do possess discriminating activity. In addition, the hypotheses that there are distinct types of SC neurons in the deeper layers and that they are differently involved in saccade target selection were not substantiated. Third, we found that the discriminating quality of single-neuron activity substantially surpasses the ability of the monkeys to discriminate the target from distracters, raising the possibility that saccade target selection is a noisy process. We discuss these new findings in light of the visual search literature and the view that the SC is a visual salience map for orienting eye movements.

A perceptual discrimination task abnormally facilitates reflexive saccades in Parkinson’s disease

Numerous studies have shown that Parkinson's disease (PD) affects the ability to generate voluntary saccades and the ability to suppress reflexive saccades. The effects of PD on the generation of reflexive saccades, however, are not clear. Some studies report impairments, but there are also reports of abnormal facilitation or hyper-reflexivity of the saccade system in PD. Meanwhile, it has been reported that the concurrent performance of a perceptual discrimination task facilitates saccade initiation and reduces saccade latencies in healthy subjects [A. Montagnini & L. Chelazzi (2005)Vis. Res., 45, 3391-3401; L. Trottier & J. Pratt (2005)Vis. Res., 45, 1349-1354]. To investigate the circumstances under which the saccade system may appear hyper-reflexive in PD, we compared reflexive saccades with and without a concurrent perceptual discrimination task in 20 PD patients and 20 controls. Without the discrimination task, the PD group produced reflexive saccades at normal latencies. The discrimination task reduced saccade latencies more in the PD group than in the control group, resulting in abnormally short mean reflexive saccade latencies in the PD group. The discrimination task increased saccade gain in both groups, but saccades in the PD group remained hypometric as compared with saccades in the control group. We conclude that the attentional demands of this paradigm revealed a hypersensitivity to visual inputs in the PD group.

Distinct Control of Initiation and Metrics of Memory-Guided Saccades and Vergence by the FEF: A TMS Study

BackgroundThe initiation of memory guided saccades is known to be controlled by the frontal eye field (FEF). Recent physiological studies showed the existence of an area close to FEF that controls also vergence initiation and execution. This study is to explore the effect of transcranial magnetic simulation (TMS) over FEF on the control of memory-guided saccade-vergence eye movements.Methodology/Principal FindingsSubjects had to make an eye movement in dark towards a target flashed 1 sec earlier (memory delay); the location of the target relative to fixation point was such as to require either a vergence along the median plane, or a saccade, or a saccade with vergence; trials were interleaved. Single pulse TMS was applied on the left or right FEF; it was delivered at 100 ms after the end of memory delay, i.e. extinction of fixation LED that was the “go” signal. Twelve healthy subjects participated in the study. TMS of left or right FEF prolonged the latency of all types of eye movements; the increase varied from 21 to 56 ms and was particularly strong for the divergence movements. This indicates that FEF is involved in the initiation of all types of memory guided movement in the 3D space. TMS of the FEF also altered the accuracy but only for leftward saccades combined with either convergence or divergence; intrasaccadic vergence also increased after TMS of the FEF.Conclusions/SignificanceThe results suggest anisotropy in the quality of space memory and are discussed in the context of other known perceptual motor anisotropies.

Attention to baseline: does orienting visuospatial attention really facilitate target detection?

Standard protocols testing the orientation of visuospatial attention usually present spatial cues before targets and compare valid-cue trials with invalid-cue trials. The valid/invalid contrast results in a relative behavioral or physiological difference that is generally interpreted as a benefit of attention orientation. However, growing evidence suggests that inhibitory control of response is closely involved in this kind of protocol that requires the subjects to withhold automatic responses to cues, probably biasing behavioral and physiological baselines. Here, we used two experiments to disentangle the inhibitory control of automatic responses from orienting of visuospatial attention in a saccadic reaction time task in humans, a variant of the classical cue-target detection task and a sustained visuospatial attentional task. Surprisingly, when referring to a simple target detection task in which there is no need to refrain from reacting to avoid inappropriate responses, we found no consistent evidence of facilitation of target detection at the attended location. Instead, we observed a cost at the unattended location. Departing from the classical view, our results suggest that reaction time measures of visuospatial attention probably relie on the attenuation of elementary processes involved in visual target detection and saccade initiation away from the attended location rather than on facilitation at the attended location. This highlights the need to use proper control conditions in experimental designs to disambiguate relative from absolute cueing benefits on target detection reaction times, both in psychophysical and neurophysiological studies.

Volitional saccades and attentional mechanisms in schizophrenia patients and healthy control subjects

Schizophrenia (SZ) patients showed increased volitional saccade latencies, suggesting deficient volitional initiation of action. Yet increased volitional saccade latencies may also result from deficits in attention shifts. To dissociate attention shifting and saccade initiation, we asked 25 SZ patients and 25 healthy subjects to make saccades toward newly appearing (onset) targets and toward the loci of disappearing (offset) targets. Similar onsets and offsets were also used as attention cues in a Posner-type manual task. As expected, onsets and offsets had similar effects on attention. In contrast, saccade latencies were considerably longer with offset compared to onset targets, reflecting additional time for volitional saccade initiation. Unexpectedly, SZ patients had normal saccade latencies. Presumably, the expected deficit was compensated by decreased fixation-related neural activity, which was induced by the disappearance of fixation stimuli.

Human Cerebral Cortex Initiation Potentials Preceding Memory-Guided Saccades

Differences in the parameters of memory-guided saccades and saccades to visual stimuli were demonstrated. Increases in the latent periods of memory-guided saccades as compared with saccades to visual stimuli provided evidence of slowing of saccade programming based on the extraction of information from working memory. Differently directed lateral differences were seen in the latent periods and durations of saccades to visual targets and memory-guided saccades, reflecting the leading role of the left hemisphere in the programming of saccades to visual stimuli and the right hemisphere in the programming of memory- guided saccades. Comparison of parameters of the temporospatial dynamics of initiation potentials P-1 and N-1, which develop in the last 100 msec of the latent periods of saccades, suggest that there are different mechanisms for the final step of programming saccades to visual stimuli and memory-guided saccades. Decreases in the latent period of the P-1 and N-1 peak potentials before memory-guided saccades may be evidence showing acceleration of the initiation processes for memory-guided saccades as compared with visually evoked saccades. This provides grounds for suggesting that the slowing of the programming of memory-guided saccades occurs at steps preceding saccade initiation.

Initiation and inhibitory control of saccades with the progression of Parkinson's disease – Changes in three major drives converging on the superior colliculus

The cardinal pathophysiology of Parkinson's disease (PD) is considered to be the increase in the activities of basal ganglia (BG) output nuclei, which excessively inhibits the thalamus and superior colliculus (SC) and causes preferential impairment of internal over external movements. Here we recorded saccade performance in 66 patients with PD and 87 age-matched controls, and studied how the abnormality changed with disease progression. PD patients were impaired not only in memory guided saccades, but also in visually guided saccades, beginning in the relatively early stages of the disease. On the other hand, they were impaired in suppressing reflexive saccades (saccades to cue). All these changes deteriorated with disease progression. The frequency of reflexive saccades showed a negative correlation with the latency of visually guided saccades and Unified Parkinson's Disease Rating Scale motor subscores reflecting dopaminergic function. We suggest that three major drives converging on SC determine the saccade abnormalities in PD. The impairment in visually and memory guided saccades may be caused by the excessive inhibition of the SC due to the increased BG output and the decreased activity of the frontal cortex-BG circuit. The impaired suppression of reflexive saccades may be explained if the excessive inhibition of SC is “leaky.” Changes in saccade parameters suggest that frontal cortex-BG circuit activity decreases with disease progression, whereas SC inhibition stays relatively mild in comparison throughout the course of the disease. Finally, SC disinhibition due to leaky suppression may represent functional compensation from neural structures outside BG, leading to hyper-reflexivity of saccades and milder clinical symptoms.