Saccadic Suppression Research Articles

Inhibition of saccades elicits attentional suppression

Visuospatial attention has been shown to have a central role in planning and generation of saccades but what role, if any, it plays in inhibition of saccades remains unclear. In this study, we used an oculomotor delayed match- or nonmatch-to-sample task in which a cued location has to be encoded and memorized for one of two very different goals-to plan a saccade to it or to avoid making a saccade to it. We measured the spatial allocation of attention during the delay and found that while marking a location as a future saccade target resulted in an attentional benefit at that location, marking it as forbidden to saccades led to an attentional cost. Additionally, saccade trajectories were found to deviate away more from the "don't look" location than from a saccade-irrelevant distractor confirming greater inhibition of an actively forbidden location in oculomotor programming. Our finding that attention is suppressed at locations forbidden to saccades confirms and complements the claim of a selective and obligatory coupling between saccades and attention-saccades at the memorized location could neither be planned nor suppressed independent of a corresponding effect on attentional performance.

Fixational saccades reflect volitional action preparation

Human volitional actions are preceded by preparatory processes, a critical mental process of cognitive control for future behavior. Volitional action preparation is regulated by large-scale neural circuits including the cerebral cortex and the basal ganglia. Because volitional action preparation is a covert process, the network dynamics of such neural circuits have been examined by neuroimaging and recording event-related potentials. Here, we examined whether such covert processes can be measured by the overt responses of fixational saccades (including microsaccades), the largest miniature eye movements that occur during eye fixation. We analyzed fixational saccades while adult humans maintained fixation on a central visual stimulus as they prepared to generate a volitional saccade in response to peripheral stimulus appearance. We used the antisaccade paradigm, in which subjects generate a saccade toward the opposite direction of a peripheral stimulus. Appropriate antisaccade performance requires the following two aspects of volitional control: 1) facilitation of saccades away from the stimulus and 2) suppression of inappropriate saccades toward the stimulus. We found that fixational saccades that occurred before stimulus appearance reflected the dual preparatory states of saccade facilitation and suppression and correlated with behavioral outcome (i.e., whether subjects succeeded or failed to cancel inappropriate saccades toward the stimulus). Moreover, fixational saccades explained a large proportion of individual differences in behavioral performance (poor/excellent) across subjects. These results suggest that fixational saccades predict the outcome of future volitional actions and may be used as a potential biomarker to detect people with difficulties in volitional action preparation.

Spatio-temporal topography of saccadic overestimation of time

Rapid eye movements (saccades) induce visual misperceptions. A number of studies in recent years have investigated the spatio-temporal profiles of effects like saccadic suppression or perisaccadic mislocalization and revealed substantial functional similarities. Saccade induced chronostasis describes the subjective overestimation of stimulus duration when the stimulus onset falls within a saccade. In this study we aimed to functionally characterize saccade induced chronostasis in greater detail. Specifically we tested if chronostasis is influenced by or functionally related to saccadic suppression. In a first set of experiments, we measured the perceived duration of visual stimuli presented at different spatial positions as a function of presentation time relative to the saccade. We further compared perceived duration during saccades for isoluminant and luminant stimuli. Finally, we investigated whether or not saccade induced chronostasis is dependent on the execution of a saccade itself. We show that chronostasis occurs across the visual field with a clear spatio-temporal tuning. Furthermore, we report chronostasis during simulated saccades, indicating that spurious retinal motion induced by the saccade is a prime origin of the phenomenon.

Brain Processing of Visual Information during Fast Eye Movements Maintains Motor Performance

Movement accuracy depends crucially on the ability to detect errors while actions are being performed. When inaccuracies occur repeatedly, both an immediate motor correction and a progressive adaptation of the motor command can unfold. Of all the movements in the motor repertoire of humans, saccadic eye movements are the fastest. Due to the high speed of saccades, and to the impairment of visual perception during saccades, a phenomenon called “saccadic suppression”, it is widely believed that the adaptive mechanisms maintaining saccadic performance depend critically on visual error signals acquired after saccade completion. Here, we demonstrate that, contrary to this widespread view, saccadic adaptation can be based entirely on visual information presented during saccades. Our results show that visual error signals introduced during saccade execution–by shifting a visual target at saccade onset and blanking it at saccade offset–induce the same level of adaptation as error signals, presented for the same duration, but after saccade completion. In addition, they reveal that this processing of intra-saccadic visual information for adaptation depends critically on visual information presented during the deceleration phase, but not the acceleration phase, of the saccade. These findings demonstrate that the human central nervous system can use short intra-saccadic glimpses of visual information for motor adaptation, and they call for a reappraisal of current models of saccadic adaptation.

Saccadic Momentum and Facilitation of Return Saccades Contribute to an Optimal Foraging Strategy

The interest in saccadic IOR is funneled by the hypothesis that it serves a clear functional purpose in the selection of fixation points: the facilitation of foraging. In this study, we arrive at a different interpretation of saccadic IOR. First, we find that return saccades are performed much more often than expected from the statistical properties of saccades and saccade pairs. Second, we find that fixation durations before a saccade are modulated by the relative angle of the saccade, but return saccades show no sign of an additional temporal inhibition. Thus, we do not find temporal saccadic inhibition of return. Interestingly, we find that return locations are more salient, according to empirically measured saliency (locations that are fixated by many observers) as well as stimulus dependent saliency (defined by image features), than regular fixation locations. These results and the finding that return saccades increase the match of individual trajectories with a grand total priority map evidences the return saccades being part of a fixation selection strategy that trades off exploration and exploitation.

Macaque Dorsolateral Prefrontal Cortex Does not Suppress Saccade-Related Activity in the Superior Colliculus

Of the many functions ascribed to the dorsolateral prefrontal cortex (DLPFC), the ability to override automatic stimulus-driven behavior is one of the most prominent. This ability has been investigated extensively with the antisaccade task, which requires suppression of saccades toward suddenly appearing visual stimuli. Convergent lines of evidence have supported a model in which the DLPFC suppresses unwanted saccades by inhibiting saccade-related activity in the ipsilateral superior colliculus (SC), a midbrain oculomotor structure. Here, we carried out a direct test of this inhibitory model using unilateral cryogenic deactivation of the DLPFC within the caudal principal sulcus (cPS) and simultaneous single-neuron recording of SC saccade-related neurons in monkeys performing saccades and antisaccades. Contrary to the inhibition model, which predicts that attenuation of inhibition effected by unilateral cPS deactivation should result in activity increases in ipsilateral and decreases in contralateral SC, we observed a delayed onset of saccade-related activity in the ipsilateral SC, and activity increases in the contralateral SC. These effects were mirrored by increased error rates of ipsiversive antisaccades, and reaction times of contraversive saccades. These data challenge the inhibitory model and suggest instead that the primary influence of the DLPFC on the SC is excitatory.

Neural correlates of saccadic inhibition in healthy elderly and patients with amnestic mild cognitive impairment

Performance on tasks that require saccadic inhibition declines with age and altered inhibitory functioning has also been reported in patients with Alzheimer's disease. Although mild cognitive impairment (MCI) is assumed to be a high-risk factor for conversion to AD, little is known about changes in saccadic inhibition and its neural correlates in this condition. Our study determined whether the neural activation associated with saccadic inhibition is altered in persons with amnestic mild cognitive impairment (aMCI). Functional magnetic resonance imaging (fMRI) revealed decreased activation in parietal lobe in healthy elderly persons compared to young persons and decreased activation in frontal eye fields in aMCI patients compared to healthy elderly persons during the execution of anti-saccades. These results illustrate that the decline in inhibitory functions is associated with impaired frontal activation in aMCI. This alteration in function might reflect early manifestations of AD and provide new insights in the neural activation changes that occur in pathological ageing.

Intrasaccadic suppression is dominated by reduced detector gain

Human vision requires fast eye movements (saccades). Each saccade causes a self-induced motion signal, but we are not aware of this potentially jarring visual input. Among the theorized causes of this phenomenon is a decrease in visual sensitivity before (presaccadic suppression) and during (intrasaccadic suppression) saccades. We investigated intrasaccadic suppression using a perceptual template model (PTM) relating visual detection to different signal-processing stages. One stage changes the gain on the detector's input; another increases uncertainty about the stimulus, allowing more noise into the detector; and other stages inject noise into the detector in a stimulus-dependent or -independent manner. By quantifying intrasaccadic suppression of flashed horizontal gratings at varying external noise levels, we obtained threshold-versus-noise (TVN) data, allowing us to fit the PTM. We tested if any of the PTM parameters changed significantly between the fixation and saccade models and could therefore account for intrasaccadic suppression. We found that the dominant contribution to intrasaccadic suppression was a reduction in the gain of the visual detector. We discuss how our study differs from previous ones that have pointed to uncertainty as an underlying cause of intrasaccadic suppression and how the equivalent noise approach provides a framework for comparing the disparate neural correlates of saccadic suppression.

Deficits of cortical oculomotor mechanisms in cerebellar atrophy patients

Commonly, the cerebellum is not associated with cortical components of saccadic eye movement programming. The present study investigates cerebellar effects on visually guided saccades in reflexive tasks (step, gap, overlap) and on internally driven saccades in intentional tasks (anti, memory, short memory sequences of four targets) in five patients with isolated cerebellar atrophy. The cerebellar dysfunction led to impairments in both reflexive and intentional saccades. Cerebellar atrophy patients showed an increase in the gain variability and an increase in the saccade latency. Furthermore, in the memory and anti task, suppression and pro-saccade errors were more frequent in the atrophy group compared to the control group. In the sequence task, patients had difficulties reproducing all four target locations in the order of the displayed sequence. The high variability of the saccade gain is a common observation in cerebellar atrophy patients and can be explained by the general variability present in the saccadic system. The increase in the saccade latency could be due to a cerebellar contribution to cortical processes related to fixation and target selection preceding the initiation of a saccade. Furthermore, the frequent occurrence of saccade errors in the memory and anti task suggests a cerebellar involvement in frontal inhibition of unwanted reflexive saccades. The impaired reproduction of saccade sequences in atrophy patients points to a deficit in short-term memory processes. Thus, this study provides further evidence that the cerebellum is involved in different cortical mechanisms related to the control of saccadic eye movements.

Saccadic inhibition of return can arise from late-stage execution processes

Inhibition of return (IOR) is thought to improve the efficiency of visual search behaviour by biasing attention, eye movements, or both, toward novel stimuli. Previous research suggests that IOR might arise from early sensory, attentional or motor programming processes. In the present study, we were interested in determining if IOR could instead arise from processes operating at or during response execution, independent from effects on earlier processes. Participants made consecutive saccades (from a common starting location) to central arrowhead stimuli. We removed the possible contribution of early sensory/attentional and motor preparation effects in IOR by allowing participants to fully prepare their responses in advance of an execution signal. When responses were prepared in advance, we continued to observe IOR. Our data therefore provide clear evidence that saccadic IOR can result from an execution bias that might arise from inhibitory effects on motor output neurons, or alternatively from late attentional engagement processes.

Neuro-ophthalmology of movement disorders

Movement disorders commonly present with ocular features. The purpose of this review is to outline neuro-ophthalmologic findings that can help in diagnosis, treatment and determining prognosis in patients with movement disorders. Common movement disorders with ophthalmic symptoms include extrapyramidal disorders such as Parkinson disease-associated dry eye, decreased blink rate, and vergence dysfunction, and progressive supranuclear palsy-related lid retraction, frequent square-wave jerks and supranuclear gaze palsy. Multisystem atrophy can present with gaze-evoked horizontal or positional downbeat nystagmus and impaired vestibulo-ocular reflex suppression. Genetic disorders such as Huntington disease produce increased saccadic latencies and impaired suppression of saccades to presented stimulus, whereas Wilson disease is associated with saccadic pursuits, increased antisaccade latencies and decreased pursuit gain. Whipple's disease can present with supranuclear gaze palsy and characteristic oculomasticatory myorrhythmia. Movement disorders commonly present with ocular features. Knowledge of these ocular symptoms can assist the ophthalmologist in diagnosis and treatment of movement disorders.

Spatiotemporal structure of visual receptive fields in macaque superior colliculus

Saccades are useful for directing the high-acuity fovea to visual targets that are of behavioral relevance. The selection of visual targets for eye movements involves the superior colliculus (SC), where many neurons respond to visual stimuli. Many of these neurons are also activated before and during saccades of specific directions and amplitudes. Although the role of the SC in controlling eye movements has been thoroughly examined, far less is known about the nature of the visual responses in this area. We have, therefore, recorded from neurons in the intermediate layers of the macaque SC, while using a sparse-noise mapping procedure to obtain a detailed characterization of the spatiotemporal structure of visual receptive fields. We find that SC responses to flashed visual stimuli start roughly 50 ms after the onset of the stimulus and last for on average ~70 ms. About 50% of these neurons are strongly suppressed by visual stimuli flashed at certain locations flanking the excitatory center, and the spatiotemporal pattern of suppression exerts a predictable influence on the timing of saccades. This suppression may, therefore, contribute to the filtering of distractor stimuli during target selection. We also find that saccades affect the processing of visual stimuli by SC neurons in a manner that is quite similar to the saccadic suppression and postsaccadic enhancement that has been observed in the cortex and in perception. However, in contrast to what has been observed in the cortex, decreased visual sensitivity was generally associated with increased firing rates, while increased sensitivity was associated with decreased firing rates. Overall, these results suggest that the processing of visual stimuli by SC receptive fields can influence oculomotor behavior and that oculomotor signals originating in the SC can shape perisaccadic visual perception.

Synchrony and firing rate modulation in area MT at the time of saccades

Humans perform about three eye movements per second. The detection of briefly flashed targets around such saccades is more difficult compared to fixation. This loss in sensitivity is typically referred to as saccadic suppression. Because a clear neurophysiologic correlate has not yet been identified, we continue the quest to identify possible neural mechanisms of saccadic suppression. We recorded electrophysiological data in area MT of two macaques while they observed randomly positioned flickering bars and performed optokinetic nystagmus (OKN), a sequence of slow phases interspersed with fast backward eye movements. The OKN was induced by a random dot pattern that moved to the left or to the right and filled the entire screen. We analyzed the firing rate, local field potential (LFP), the power of the LFP, as well as the correlations between the stimulus and the spikes and the correlations between the stimulus and the LFP, all around the time of saccades. The power of the LFP in a frequency band matched to the stimulus frequency showed a large drop around saccade onset, even when the firing rate of individual cells was increased or not modulated. This suggests that a lack of population synchrony may contribute to the reduced detectability of a visual stimulus around the time of a saccade. We also used the polarity of the LFP modulation around saccade onset to putatively assign neurons and LFP recordings to specific layers (supra or infragranular; Murthy and Fetz, JNeurophys 1996). This assignment revealed a layer-specific modulation of firing rate immediately after the saccade. One group of neurons (e.g. in the putative infragranular layers) showed an increase of firing after the saccade, while the other group showed a decrease. We speculate that this may be a signature of feedback modulation enhancing the representation of afferent input. Meeting abstract presented at VSS 2012

Attentional modulation of saccadic inhibition during scene viewing

Attentional modulation of saccadic inhibition during scene viewing

Modulation of saccadic inhibition by distractor size and location

Distractors presented contralateral to a visual target inhibit the generation of saccades within a precise temporal window (Buonocore & McIntosh, 2008; Reingold & Stampe, 2002; Walker, Kentridge, & Findlay, 1995). The greatest ‘dip’ of saccadic inhibition typically occurs at about 90ms after distractor onset, with a subsequent recovery period showing an elevated frequency of saccades. It is not yet known how the spatial properties of the distractor stimulus influence the saccadic inhibition signature. To study this, we manipulated the size and the field of presentation of the distractor in four experiments. Experiment 1 demonstrated that the size of a distractor in the contralateral field is logarithmically related to the magnitude of the saccadic inhibition dip. This implies that the probability of a planned saccade being inhibited increases logarithmically with the size of the distractor. Experiment 2 showed a qualitatively similar but more pronounced effect of size for distractors in the ipsilateral field. Experiment 3 compared the effects of contralateral and ipsilateral distractors directly using a within-subjects design, confirming the more pronounced impact of ipsilateral distractors. Experiment 4 replicated the more pronounced effect of ipsilateral distractors in a task in which target side was unpredictable, confirming that the effect does not result merely from participants preparing in advance to ignore events on one side. We suggest that participants are more able to resist contralateral distraction during target selection, as they can more effectively withdraw attention from locations remote from the target than from locations close to it.

Neural networks related to pro-saccades and anti-saccades revealed by independent component analysis

The saccadic eye movement system provides an excellent model for investigating basic cognitive processes and flexible control over behaviour. While the mechanism of pro-saccades (PS) is well known, in the case of the anti-saccade task (AS) it is still not clear which brain regions play a role in the inhibition of reflexive saccade to the target, nor what is the exact mechanism of vector inversion (i.e. orienting in the opposite direction). Independent component analysis (ICA) is one of the methods being used to establish temporally coherent brain regions, i.e. neural networks related to the task. In the present study ICA was applied to fMRI data from PS and AS experiments. The study revealed separate networks responsible for saccade generation into the desired direction, the inhibition of automatic responses, as well as vector inversion. The first function is accomplished by the eye fields network. The inhibition of automatic responses is associated with the executive control network. Vector inversion seems to be accomplished by the network comprising a large set of areas, including intraparietal sulcus, precuneus/posterior cingulate cortices, retrosplenial and parahippocampal. Those regions are associated with the parieto-medial temporal pathway, so far linked only to navigation. These results provide a new insight into understanding of the processes of the inhibition and vector inversion.

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.

It's all about the transient: Intra-saccadic onset stimuli do not capture attention

An abrupt onset stimulus was presented while the participants' eyes were in motion. Because of saccadic suppression, participants did not perceive the visual transient that normally accompanies the sudden appearance of a stimulus. In contrast to the typical finding that the presentation of an abrupt onset captures attention and interferes with the participants' responses, we found that an intra-saccadic abrupt onset does not capture attention: It has no effect beyond that of increasing the set-size of the search array by one item. This finding favours the local transient account of attentional capture over the novel object hypothesis.

Saccade-Related beta-Band Desynchronization in the Subthalamic Nucleus of Parkinson Disease Patients during Successful Antisaccades and Error Trials (P01.196)

Objective: To investigate the saccade-related beta-band desynchronization (beta-SRD) recorded from deep brain stimulation (DBS) electrodes implanted in the subthalamic nucleus (STN) of Parkinson disease (PD) patients during successful antisaccades and error trials. Background The basal ganglia including the STN are involved in response selection by exerting or removing tonic inhibition in the thalamocortical loops and in the brainstem motor circuits. Beta-SRDs are thought to play a role in inhibition of unwanted movements and in execution of movements. Antisaccades require a strong inhibition of reflexive saccades towards the visual cue and a strong driving signal for voluntary saccades away from the visual cue. Whether beta-SRDs in the STN during successful antisaccades are different from those during error trials has not been studied. Design/Methods: Eighteen PD patients performed an antisaccade task 1 to 3 days after DBS surgery when the leads were externalized. Local field potentials were recorded from DBS electrodes implanted in the STN and electrooculography was used to measure saccades. We analyzed the power spectrum in each DBS contact pair using Morlet wavelets averaged on saccade onset. The incidence, latency, and duration of beta-SRDs during successful antisaccades were compared with those during errors trials. Results: The averaged incidence of errors was 36.3%. Mean latencies of saccades were longer during antisaccades (432.6 ± 170.6 ms (mean ± SD)) than during errors (309.5 ± 146.1 ms). Beta-SRDs were observed more often during antisaccades (24 of 31 STN) than during errors (7 of 31 STN; p Conclusions: Beta-SRDs were observed more frequently and were sustained for longer during successful antisaccades than during error trials. Those results suggest that beta-SRDs played a role in the suppression of unwanted saccades and in the successful execution of antisaccades. Disclosure: Dr. Yugeta has nothing to disclose. Dr. Hutchison has received personal compensation for activities with Medtronic Inc. as a speaker. Dr. Hutchison has received research support from Medtronic Inc. Dr. Chen has received personal compensation for activities with Allergan, Inc., Medtronic, Inc., Biovail, EMD Serono, Merz Pharma, the American Academy of Neurology, the Douglas Mental Health University Institute, Movement Disorders Society, the University of Pittsburg, Merz, CHIR, the Michael J. Fox Foundation for Parkinson9s Research, the Dystonia Medical Research Foundation, and has provided expert testimony and affidavit in welding related litigations. Dr. Chen has received research support from Medtronic, Inc.

Saccadic Abnormalities in Familial Parkinson's Disease Associated with -Synuclein (SNCA) Gene Mutation (PARK1) (P02.258)

Objective: To investigate saccadic characteristics of PARK1 and to compare them with those of other parkinsonian syndromes. Background Typical patterns of eye movement abnormalities have been described in both idiopathic (PD, CDB, LBD and MSA) and familial (PARK2 and PARK6) parkinsonian syndromes, providing not only useful diagnostic markers, but also insights in to the functions of the basal ganglia. Mutations in the SNCA gene are a rare cause of autosomal dominant early-onset Parkinson9s Diseases (PARK1); its gene product is the main component of Lewy bodies, the hallmark of parkinsonian neuronal degeneration. Design/Methods: Two symptomatic PARK1 patients were recorded during various saccadic paradigms: horizontal visually-guided saccades (VGS), anti-saccades, overlap, and memory-guided saccades (MGS) (10° and 18°). Data were statistically compared with those of 19 healthy controls. Results were related to findings reported in other parkinsonian syndromes. Results: Both patients showed saccadic abnormalities. VGS amplitude (10° p1:9.6±0.8°, p2:8.4±0.5° normal values (n.v.) 10.3±1.0° p Conclusions: PARK1 patients present peculiar abnormalities in both voluntary and reflexive saccades. Hypometric VGS, abnormal inhibition of reflexive saccades and staircase saccades have been described in other parkinsonian syndromes. The observation of slow VGS has never been reported in parkinsonian syndromes and may indicate the extension of the neuronal degeneration to other structures controlling saccade dynamics. The characteristic patterns of saccade abnormalities may help diagnosis as well as pointing to an understanding of the functions of the basal ganglia and how they become impaired in parkinsonian syndromes. Disclosure: Dr. Pretegiani has nothing to disclose. Dr. Leigh has nothing to disclose. Dr. Zee has received royalty payments from Oxford University Press. Dr. Federico has nothing to disclose. Dr. Piu has nothing to disclose. Dr. Rufa has nothing to disclose.