Saccade Planning Research Articles

Pupil size and social vigilance in rhesus macaques.

Complex natural environments favor the dynamic alignment of neural processing between goal-relevant stimuli and conflicting but biologically salient stimuli like social competitors or predators. The biological mechanisms that regulate dynamic changes in vigilance have not been fully elucidated. Arousal systems that ready the body to respond adaptively to threat may contribute to dynamic regulation of vigilance. Under conditions of constant luminance, pupil diameter provides a peripheral index of arousal state. Although pupil size varies with the processing of goal-relevant stimuli, it remains unclear whether pupil size also predicts attention to biologically salient objects and events like social competitors, whose presence interferes with current goals. Here we show that pupil size in rhesus macaques both reflects the biological salience of task-irrelevant social distractors and predicts vigilance for these stimuli. We measured pupil size in monkeys performing a visual orienting task in which distractors—monkey faces and phase-scrambled versions of the same images—could appear in a congruent, incongruent, or neutral position relative to a rewarded target. Baseline pupil size under constant illumination predicted distractor interference, consistent with the hypothesis that pupil-linked arousal mechanisms regulate task engagement and distractibility. Notably, pupil size also predicted enhanced vigilance for social distractors, suggesting that pupil-linked arousal may adjust the balance of processing resources between goal-relevant and biologically important stimuli. The magnitude of pupil constriction in response to distractors closely tracked distractor interference, saccade planning and the social relevance of distractors, endorsing the idea that the pupillary light response is modulated by attention. These findings indicate that pupil size indexes dynamic changes in attention evoked by both the social environment and arousal.

Adaptation of scanning saccades co-occurs in different coordinate systems

Plastic changes of saccades (i.e., following saccadic adaptation) do not transfer between oppositely directed saccades, except when multiple directions are trained simultaneously, suggesting a saccadic planning in retinotopic coordinates. Interestingly, a recent study in human healthy subjects revealed that after an adaptive increase of rightward-scanning saccades, both leftward and rightward double-step, memory-guided saccades, triggered toward the adapted endpoint, were modified, revealing that target location was coded in spatial coordinates (Zimmermann et al. 2011). However, as the computer screen provided a visual frame, one alternative hypothesis could be a coding in allocentric coordinates. Here, we questioned whether adaptive modifications of saccadic planning occur in multiple coordinate systems. We reproduced the paradigm of Zimmermann et al. (2011) using target light-emitting diodes in the dark, with and without a visual frame, and tested different saccades before and after adaptation. With double-step, memory-guided saccades, we reproduced the transfer of adaptation to leftward saccades with the visual frame but not without, suggesting that the coordinate system used for saccade planning, when the frame is visible, is allocentric rather than spatiotopic. With single-step, memory-guided saccades, adaptation transferred to leftward saccades, both with and without the visual frame, revealing a target localization in a coordinate system that is neither retinotopic nor allocentric. Finally, with single-step, visually guided saccades, the classical, unidirectional pattern of amplitude change was reproduced, revealing retinotopic coordinate coding. These experiments indicate that the same procedure of adaptation modifies saccadic planning in multiple coordinate systems in parallel-each of them revealed by the use of different saccade tasks in postadaptation.

The enigma of Bálint's syndrome: neural substrates and cognitive deficits

The enigma of Bálint's syndrome: neural substrates and cognitive deficits

Response Suppression Delays the Planning of Subsequent Stimulus-Driven Saccades

The completion of an antisaccade selectively increases the reaction time (RT) of a subsequent prosaccade: a result that has been interpreted to reflect the residual inhibition of stimulus-driven saccade networks [1], [2]. In the present investigation we sought to determine whether the increase in prosaccade RT is contingent on the constituent antisaccade planning processes of response suppression and vector inversion or is limited to response suppression. To that end, in one block participants alternated between pro- and antisaccades after every second trial (task-switching block), and in another block participants completed a series of prosaccades that were randomly (and infrequently) interspersed with no-go catch-trials (go/no-go block). Notably, such a design provides a framework for disentangling whether response suppression and/or vector inversion delays the planning of subsequent prosaccades. As expected, results for the task-switching block showed that antisaccades selectively increased the RTs of subsequent prosaccades. In turn, results for the go/no-go block showed that prosaccade RTs were increased when preceded by a no-go catch-trial. Moreover, the magnitude of the RT ‘cost’ was equivalent across the task-switching and go/no-go blocks. That prosaccades preceded by an antisaccade or a no-go catch-trial produced equivalent RT costs indicates that the conjoint processes of response suppression and vector inversion do not drive the inhibition of saccade planning mechanisms. Rather, the present findings indicate that a general consequence of response suppression is a residual inhibition of stimulus-driven saccade networks.

Saccade-like behavior in the fast-phases of optokinetic nystagmus: an illustration of the emergence of volitional actions from automatic reflexes.

As a potential exemplar for understanding how volitional actions emerged from reflexes, we studied the relationship between an ancient reflexive gaze stabilization mechanism (optokinetic nystagmus [OKN]) and purposeful eye movements (saccades) that target an object. Traditionally, these have been considered distinct (except in the kinematics of their execution) and have been studied independently. We find that the fast-phases of OKN clearly show properties associated with saccade planning: (a) They are characteristically delayed by irrelevant distractors in an indistinguishable way to saccades (the saccadic inhibition effect), and (b) horizontal OKN fast-phases produce curvature in vertical targeting saccades, just like a competing saccade plan. Thus, we argue that the saccade planning network plays a role in the production of OKN fast-phases, and we question the need for a strict distinction between eye movements that appear to be automatic or volitional. We discuss whether our understanding might benefit from shifting perspective and considering the entire "saccade" system to have developed from an increasingly sophisticated OKN system.

Linking cortical visual processing to viewing behaviour using fMRI

One characteristic of natural visual behavior in humans is the frequent shifting of eye position. It has been argued that the characteristics of these eye movements can be used to distinguish between distinct modes of visual processing (Unema et al., 2005). These viewing modes would be distinguishable on the basis of the eye-movement parameters fixation duration and saccade amplitude and have been hypothesized to reflect the differential involvement of dorsal and ventral systems in saccade planning and information processing. According to this hypothesis, on the one hand, while in a “pre-attentive” or ambient mode, primarily scanning eye movements are made; in this mode fixation are relatively brief and saccades tends to be relatively large. On the other hand, in “attentive” focal mode, fixations last longer and saccades are relatively small, and result in viewing behavior which could be described as detailed inspection. Thus far, no neuroscientific basis exists to support the idea that such distinct viewing modes are indeed linked to processing in distinct cortical regions. Here, we used fixation-based event-related (FIBER) fMRI in combination with independent component analysis (ICA) to investigate the neural correlates of these viewing modes. While we find robust eye-movement-related activations, our results do not support the theory that the above mentioned viewing modes modulate dorsal and ventral processing. Instead, further analyses revealed that eye-movement characteristics such as saccade amplitude and fixation duration did differentially modulate activity in three clusters in early, ventromedial and ventrolateral visual cortex. In summary, we conclude that evaluating viewing behavior is crucial for unraveling cortical processing in natural vision.

Parallel programming of saccades during natural scene viewing: Evidence from eye movement positions

Previous studies have shown that saccade plans during natural scene viewing can be programmed in parallel. This evidence comes mainly from temporal indicators, i.e., fixation durations and latencies. In the current study, we asked whether eye movement positions recorded during scene viewing also reflect parallel programming of saccades. As participants viewed scenes in preparation for a memory task, their inspection of the scene was suddenly disrupted by a transition to another scene. We examined whether saccades after the transition were invariably directed immediately toward the center or were contingent on saccade onset times relative to the transition. The results, which showed a dissociation in eye movement behavior between two groups of saccades after the scene transition, supported the parallel programming account. Saccades with relatively long onset times (>100 ms) after the transition were directed immediately toward the center of the scene, probably to restart scene exploration. Saccades with short onset times (<100 ms) moved to the center only one saccade later. Our data on eye movement positions provide novel evidence of parallel programming of saccades during scene viewing. Additionally, results from the analyses of intersaccadic intervals were also consistent with the parallel programming hypothesis.

Social Information Signaling by Neurons in Primate Striatum

Social decisions depend on reliable information about others. Consequently, social primates are motivated to acquire information about the identity, social status, and reproductive quality of others. Neurophysiological and neuroimaging studies implicate the striatum in the motivational control of behavior. Neuroimaging studies specifically implicate the ventromedial striatum in signaling motivational aspects of social interaction. Despite this evidence, precisely how striatal neurons encode social information remains unknown. Therefore, we probed the activity of single striatal neurons in monkeys choosing between visual social information at the potential expense of fluid reward. We show for the first time that a population of neurons located primarily in medial striatum selectively signals social information. Surprisingly, representation of social information was unrelated to simultaneously expressed social preferences. A largely nonoverlapping population of neurons that was not restricted to the medial striatum signaled information about fluid reward. Our findings demonstrate that information about social context and nutritive reward are maintained largely independently in striatum, even when both influence decisions to execute a single action.

Eye movement control during scene viewing: Immediate effects of scene luminance on fixation durations.

Recent research on eye movements during scene viewing has primarily focused on where the eyes fixate. But eye fixations also differ in their durations. Here we investigated whether fixation durations in scene viewing are under the direct and immediate control of the current visual input. Subjects freely viewed photographs of scenes in preparation for a later memory test while their eye movements were recorded. Using a novel scene degradation paradigm based on a saccade-contingent display change method, scenes were reduced in luminance during saccades ending in critical fixations. Results from two experiments showed that the durations of the critical fixations were immediately affected by scene luminance, with a monotonic relationship between luminance reduction and fixation duration. The results are the first to demonstrate that fixation durations in scene viewing are immediately influenced by the ease of processing of the image currently in view. These results are consistent with the CRISP (a timer-Controlled Random-Walk with Inhibition for Saccade Planning) computational model of saccade generation in scenes, proposing that difficulty in moment-by-moment visual and cognitive processing of the scene modulates fixation durations.

Proactive control of sequential saccades in the human supplementary eye field

Our ability to regulate behavior based on past experience has thus far been examined using single movements. However, natural behavior typically involves a sequence of movements. Here, we examined the effect of previous trial type on the concurrent planning of sequential saccades using a unique paradigm. The task consisted of two trial types: no-shift trials, which implicitly encouraged the concurrent preparation of the second saccade in a subsequent trial; and target-shift trials, which implicitly discouraged the same in the next trial. Using the intersaccadic interval as an index of concurrent planning, we found evidence for context-based preparation of sequential saccades. We also used functional MRI-guided, single-pulse, transcranial magnetic stimulation on human subjects to test the role of the supplementary eye field (SEF) in the proactive control of sequential eye movements. Results showed that (i) stimulating the SEF in the previous trial disrupted the previous trial type-based preparation of the second saccade in the nonstimulated current trial, (ii) stimulating the SEF in the current trial rectified the disruptive effect caused by stimulation in the previous trial, and (iii) stimulating the SEF facilitated the preparation of second saccades based on previous trial type even when the previous trial was not stimulated. Taken together, we show how the human SEF is causally involved in proactive preparation of sequential saccades.

Eye movement control in scene viewing and reading: Evidence from the stimulus onset delay paradigm.

The present study used the stimulus onset delay paradigm to investigate eye movement control in reading and in scene viewing in a within-participants design. Short onset delays (0, 25, 50, 200, and 350 ms) were chosen to simulate the type of natural processing difficulty encountered in reading and scene viewing. Fixation duration increased linearly with delay duration, and the effect was equivalent for both tasks. Although fixations were longer in scene viewing, the effects of onset delay were highly consistent across tasks. These results suggest that reading and scene viewing share a common mechanism for saccade planning and control.

Changes in Timing and kinematics of goal directed eye-hand movements in early-stage Parkinson’s disease

ObjectiveMany daily activities involve intrinsic or extrinsic goal-directed eye and hand movements. An extensive visuomotor coordination network including nigro-striatal pathways is required for efficient timing and positioning of eyes and hands. The aim of this study was to investigate how Parkinson’s disease (PD) affects eye-hand coordination in tasks with different cognitive complexity.MethodsWe used a touch screen, an eye-tracking device and a motion capturing system to quantify changes in eye-hand coordination in early-stage PD patients (H&Y < 2.5) and age-matched controls. Timing and kinematics of eye and hand were quantified in four eye-hand coordination tasks (pro-tapping, dual planning, anti-tapping and spatial memory task).ResultsIn the pro-tapping task, saccade initiation towards extrinsic goals was not impaired. However, in the dual planning and anti-tapping task initiation of saccades towards intrinsic goals was faster in PD patients. Hand movements were differently affected: initiation of the hand movement was only delayed in the pro-tapping and dual planning task. Overall, hand movements in PD patients were slower executed compared to controls.InterpretationWhereas initiation of saccades in an extrinsic goal-directed task (pro-tapping task) is not affected, early stage PD patients have difficulty in suppressing reflexive saccades towards extrinsic goals in tasks where the endpoint is an intrinsic goal (e.g. dual planning and anti-tapping task). This is specific for eye movements, as hand movements have delayed responses in the pro-tapping and dual planning task. This suggests that reported impairment of the dorsolateral prefrontal cortex in early-stage PD patients affects only inhibition of eye movements. We conclude that timing and kinematics of eye and hand movements in visuomotor tasks are affected in PD patients. This result may have clinical significance by providing a behavioral marker for the early diagnosis of PD.

The parietal cortex and saccade planning: lessons from human lesion studies.

The parietal cortex is a critical interface for attention and integration of multiple sensory signals that can be used for the implementation of motor plans. Many neurons in this region exhibit strong attention-, reach-, grasp- or saccade-related activity. Here, we review human lesion studies supporting the critical role of the parietal cortex in saccade planning. Studies of patients with unilateral parietal damage and spatial neglect reveal characteristic spatially lateralized deficits of saccade programming when multiple stimuli compete for attention. However, these patients also show bilateral impairments of saccade initiation and control that are difficult to explain in the context of their lateralized deficits of visual attention. These findings are reminiscent of the deficits of oculomotor control observed in patients with Bálint's syndrome consecutive to bilateral parietal damage. We propose that some oculomotor deficits following parietal damage are compatible with a decisive role of the parietal cortex in saccade planning under conditions of sensory competition, while other deficits reflect disinhibition of low-level structures of the oculomotor network in the absence of top-down parietal modulation.

Mapping Face Recognition Information Use across Cultures

Face recognition is not rooted in a universal eye movement information-gathering strategy. Western observers favor a local facial feature sampling strategy, whereas Eastern observers prefer sampling face information from a global, central fixation strategy. Yet, the precise qualitative (the diagnostic) and quantitative (the amount) information underlying these cultural perceptual biases in face recognition remains undetermined. To this end, we monitored the eye movements of Western and Eastern observers during a face recognition task, with a novel gaze-contingent technique: the Expanding Spotlight. We used 2° Gaussian apertures centered on the observers’ fixations expanding dynamically at a rate of 1° every 25 ms at each fixation – the longer the fixation duration, the larger the aperture size. Identity-specific face information was only displayed within the Gaussian aperture; outside the aperture, an average face template was displayed to facilitate saccade planning. Thus, the Expanding Spotlight simultaneously maps out the facial information span at each fixation location. Data obtained with the Expanding Spotlight technique confirmed that Westerners extract more information from the eye region, whereas Easterners extract more information from the nose region. Interestingly, this quantitative difference was paired with a qualitative disparity. Retinal filters based on spatial-frequency decomposition built from the fixations maps revealed that Westerners used local high-spatial-frequency information sampling, covering all the features critical for effective face recognition (the eyes and the mouth). In contrast, Easterners achieved a similar result by using global low-spatial-frequency information from those facial features. Our data show that the face system flexibly engages into local or global eye movement strategies across cultures, by relying on distinct facial information span and culturally tuned spatially filtered information. Overall, our findings challenge the view of a unique putative process for face recognition.

Inactivation of the Parietal Reach Region Causes Optic Ataxia, Impairing Reaches but Not Saccades

Lesions in human posterior parietal cortex can cause optic ataxia (OA), in which reaches but not saccades to visual objects are impaired, suggesting separate visuomotor pathways for the two effectors. In monkeys, one potentially crucial area for reach control is the parietal reach region (PRR), in which neurons respond preferentially during reach planning as compared to saccade planning. However, direct causal evidence linking the monkey PRR to the deficits observed in OA is missing. We thus inactivated part of the macaque PRR, in the medial wall of the intraparietal sulcus, and produced the hallmarks of OA, misreaching for peripheral targets but unimpaired saccades. Furthermore, reach errors were larger for the targets preferred by the neural population local to the injection site. These results demonstrate that PRR is causally involved in reach-specific visuomotor pathways, and reach goal disruption in PRR can be a neural basis of OA.

Prioritized Maps of Space in Human Frontoparietal Cortex

Priority maps are theorized to be composed of large populations of neurons organized topographically into a map of gaze-centered space whose activity spatially tags salient and behaviorally relevant information. Here, we identified four priority map candidates along human posterior intraparietal sulcus (IPS0-IPS3) and two along the precentral sulcus (PCS) that contained reliable retinotopically organized maps of contralateral visual space. Persistent activity increased from posterior-to-anterior IPS areas and from inferior-to-superior PCS areas during the maintenance of a working memory representation, the maintenance of covert attention, and the maintenance of a saccade plan. Moreover, decoders trained to predict the locations on one task (e.g., working memory) cross-predicted the locations on other tasks (e.g., attention) in superior PCS and IPS2, suggesting that these patterns of maintenance activity may be interchangeable across the tasks. Such properties make these two areas in frontal and parietal cortex viable priority map candidates.

A perceptual discrimination task results in greater facilitation of voluntary saccades in Parkinson's disease patients

Many studies have shown that Parkinson's disease (PD) affects not only the ability to generate voluntary saccades but also the ability to suppress reflexive saccades (hyper-reflexivity). To further investigate these apparently contradictory effects of PD on the saccade system we adapted a well-known dual-task paradigm (Deubel, 2008) to measure saccades with and without a peripheral discrimination task. Previously we reported that the concurrent performance of a perceptual discrimination task abnormally reduced the latencies of reflexive saccades in PD. Here we report the effects of the concurrent discrimination task on the generation of voluntary saccades in a PD and a control group. As expected, when saccades were performed without the discrimination task the PD group made voluntary saccades with longer latencies and smaller gain than the control group. The concurrent performance of the perceptual discrimination task facilitated the initiation of voluntary saccades in both groups, but, surprisingly, this facilitatory effect was stronger in the PD group than in the control group. In addition, in the PD group voluntary saccades were abnormally facilitated by the peripheral symbol-changes that occur during saccade planning in this paradigm. The results of this study may help to clarify apparently contradictory oculomotor abnormalities observed in PD.

Fixation positions after skipping saccades: A single space makes a large difference

During reading, saccadic eye movements are generated to shift words into the center of the visual field for lexical processing. Recently, Krügel and Engbert (Vision Research 50:1532–1539, 2010) demonstrated that within-word fixation positions are largely shifted to the left after skipped words. However, explanations of the origin of this effect cannot be drawn from normal reading data alone. Here we show that the large effect of skipped words on the distribution of within-word fixation positions is primarily based on rather subtle differences in the low-level visual information acquired before saccades. Using arrangements of “x” letter strings, we reproduced the effect of skipped character strings in a highly controlled single-saccade task. Our results demonstrate that the effect of skipped words in reading is the signature of a general visuomotor phenomenon. Moreover, our findings extend beyond the scope of the widely accepted range-error model, which posits that within-word fixation positions in reading depend solely on the distances of target words. We expect that our results will provide critical boundary conditions for the development of visuomotor models of saccade planning during reading.Electronic supplementary materialThe online version of this article (doi:10.3758/s13414-012-0365-1) contains supplementary material, which is available to authorized users.

Eye movements and attention: The role of pre-saccadic shifts of attention in perception, memory and the control of saccades

Saccadic eye movements and perceptual attention work in a coordinated fashion to allow selection of the objects, features or regions with the greatest momentary need for limited visual processing resources. This study investigates perceptual characteristics of pre-saccadic shifts of attention during a sequence of saccades using the visual manipulations employed to study mechanisms of attention during maintained fixation. The first part of this paper reviews studies of the connections between saccades and attention, and their significance for both saccadic control and perception. The second part presents three experiments that examine the effects of pre-saccadic shifts of attention on vision during sequences of saccades. Perceptual enhancements at the saccadic goal location relative to non-goal locations were found across a range of stimulus contrasts, with either perceptual discrimination or detection tasks, with either single or multiple perceptual targets, and regardless of the presence of external noise. The results show that the preparation of saccades can evoke a variety of attentional effects, including attentionally-mediated changes in the strength of perceptual representations, selection of targets for encoding in visual memory, exclusion of external noise, or changes in the levels of internal visual noise. The visual changes evoked by saccadic planning make it possible for the visual system to effectively use saccadic eye movements to explore the visual environment.

Paying Attention through Eye Movements: A Computational Investigation of the Premotor Theory of Spatial Attention

Growing evidence indicates that planning eye movements and orienting visuospatial attention share overlapping brain mechanisms. A tight link between endogenous attention and eye movements is maintained by the premotor theory, in contrast to other accounts that postulate the existence of specific attention mechanisms that modulate the activity of information processing systems. The strong assumption of equivalence between attention and eye movements, however, is challenged by demonstrations that human observers are able to keep attention on a specific location while moving the eyes elsewhere. Here we investigate whether a recurrent model of saccadic planning can account for attentional effects without requiring additional or specific mechanisms separate from the circuits that perform sensorimotor transformations for eye movements. The model builds on the basis function approach and includes a circuit that performs spatial remapping using an "internal forward model" of how visual inputs are modified as a result of saccadic movements. Simulations show that the latter circuit is crucial to account for dissociations between attention and eye movements that may be invoked to disprove the premotor theory. The model provides new insights into how spatial remapping may be implemented in parietal cortex and offers a computational framework for recent proposals that link visual stability with remapping of attention pointers.