Saccadic Performance Research Articles

Subthalamic deep brain stimulation improves smooth pursuit and saccade performance in patients with Parkinson’s disease

BackgroundDeep brain stimulation (DBS) in the subthalamic nucleus (STN) significantly reduces symptoms of Parkinson’s disease (PD) such as bradykinesia, tremor and rigidity. It also reduces the need for anti-PD medication, and thereby potential side-effects of L-Dopa. Although DBS in the STN is a highly effective therapeutic intervention in PD, its mechanism and effects on oculomotor eye movement control and particularly smooth pursuit eye movements have to date rarely been investigated. Furthermore, previous reports provide conflicting information. The aim was to investigate how DBS in STN affected oculomotor performance in persons with PD using novel analysis techniques.MethodsTwenty-five patients were eligible (22 males, 3 females) according to the clinical inclusion criteria: idiopathic PD responsive to L-Dopa and having had bilateral STN stimulation for at least one year to ensure stable DBS treatment. Fifteen patients were excluded due to the strict inclusion criteria applied to avoid interacting and confounding factors when determining the effects of DBS applied alone without PD medication. One patient declined participation. Nine PD patients (median age 63, range 59–69 years) were assessed after having their PD medications withdrawn overnight. They were examined with DBS ON and OFF, with the ON/OFF order individually randomized.ResultsDBS ON increased smooth pursuit velocity accuracy (p < 0.001) and smooth pursuit gain (p = 0.005), especially for faster smooth pursuits (p = 0.034). DBS ON generally increased saccade amplitude accuracy (p = 0.007) and tended to increase peak saccade velocity also (p = 0.087), specifically both saccade velocity and amplitude accuracy for the 20 and 40 degree saccades (p < 0.05). Smooth pursuit latency tended to be longer (p = 0.090) approaching normal with DBS ON. Saccade latency was unaffected.ConclusionsSTN stimulation from DBS alone significantly improved both smooth pursuit and saccade performance in patients with PD. The STN stimulation enhancement found for oculomotor performance suggests clear positive implications for patients’ ability to perform tasks that rely on visual motor control and visual feedback. The new oculomotor analysis methods provide a sensitive vehicle to detect subtle pathological modifications from PD and the functional enhancements produced by STN stimulation from DBS alone.

Saccadic eye movements and face recognition performance in patients with central glaucomatous visual field defects

Patients with more advanced glaucoma are likely to experience problems with everyday visual tasks such as face recognition. However, some patients still perform well at face recognition despite their visual field (VF) defects. This study investigated whether certain eye movement patterns are associated with better performance in the Cambridge Face Memory Test. For patients with bilateral VF defects in their central 10° of VF, making larger saccades appeared to be associated with better face recognition performance (rho=0.60, p=0.001). Associations were less apparent for the patients without significant 10° defects. There were no significant associations between saccade amplitude and task performance in people with healthy vision (rho=−0.24; p=0.13). These findings suggest that some patients with likely symptomatic glaucomatous damage manifest eye movements to adapt to VF loss during certain visual activities.

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.

Eye movements in patients with neurodegenerative disorders

The neural pathways and brain regions involved in eye movements during ocular fixation and gaze control include the cerebrum, brainstem and cerebellum, and abnormal eye movements can indicate the presence of neurodegeneration. In some patients, oculomotor signs are key to making a diagnosis. Careful clinical examination of eye movements in patients with neurodegenerative disorders is, therefore, an invaluable adjunct to neurological and cognitive assessments. Eye movement recordings in the laboratory are generally not necessary for diagnostic purposes, but can be a useful addition to the clinical examination. Laboratory recordings of eye movements can provide valuable information about disease severity, progression or regression in neurodegenerative disease, and hold particular promise for objective evaluation of the efficacy of putative neuroprotective and neurorestorative therapies. For example, aspects of saccade performance can be tested to probe both motor and cognitive aspects of oculomotor behaviour. This Review describes the oculomotor features of the major age-related movement disorders, including Parkinson disease, Huntington disease, dementia and other neurodegenerative disorders. Findings in presymptomatic individuals and changes associated with disease progression are discussed.

Age-related change of the mean level and intraindividual variability of saccadic reaction time performance in persons with intellectual disabilities

The current study examined age-related change of saccadic reaction time (SRT) in persons with intellectual disabilities (ID). Participants were 29 persons with intellectual disabilities aged between 14 and 34 years whose IQs were between 14 and 70. Participants were divided into Group I (IQ≧35) and Group II (IQ≦34). The mean and the standard deviation of SRT (SRTM and SRTSD, respectively) reduced through adolescence in both groups. This result suggests that the speed and stability of information processing develops during adolescence irrespective of the level of ID. Although SRTM and SRTSD of Group I stabilized after adolescence, those of Group II increased after their thirties. This outcome indicates that persons with severe ID may show signs of the aging process. The results of multiple regression analyses and path analyses indicated that SRTM was influenced by both the speed of information processing and the variability of the response. However, given that the extent of increase of SRTSD in Group II was smaller as compared with that of SRTM, this increase of SRTM after the thirties in Group II appears to be mainly affected by the slowness of information processing.

Saccadic Performance and Cortical Excitability as Trait-Markers and State-Markers in Rapid Cycling Bipolar Disorder: A Two-Case Follow-Up Study

Background: The understanding of physiopathology and cognitive impairments in mood disorders requires finding objective markers. Mood disorders have often been linked to hypometabolism in the prefrontal dorsolateral cortex, and to GABAergic and glutamatergic neurotransmission dysfunction. The present study aimed to discover whether saccadic tasks (involving DPLFC activity), and cortical excitability (involving GABA/Glutamate neurotransmission) could provide neuropsychophysical markers for mood disorders, and/or of its phases, in patients with rapid cycling bipolar disorders (rcBD). Methods: Two rcBD patients were followed for a cycle, and were compared to nine healthy controls. A saccade task, mixing prosaccades, antisaccades, and nosaccades, and an evaluation of cortical excitability using transcranial magnetic stimulation were performed. Results: We observed a deficit in antisaccade in patients independently of thymic phase, and in nosaccade in the manic phase only. Cortical excitability data revealed global intracortical deficits in all phases, switching according to cerebral hemisphere and thymic phase. Conclusion: Specific patterns of performance in saccade tasks and cortical excitability could characterize mood disorders (trait-markers) and its phases (state-markers). Moreover, a functional relationship between oculometric performance and cortical excitability is discussed.

The Relationship between Abnormalities of Saccadic and Manual Response Times in Parkinson's Disease

Clinicians normally use subjective rating scales to estimate the impairment of patients with Parkinson's disease (PD). More objective and quantitative methods of assessment would greatly aid our understanding of the disease. One promising approach is to measure reaction time: the large amount of data recorded in a short period provides precise, reproducible evaluation of the underlying neural decision processes. Manual evoked reaction times and repetitive tapping speed are often used, but differences of experimental design and analysis tend to obscure their interpretation. Saccadic latency, in many ways a simpler and more standardised task, is also normally affected in PD, but its relation to the kind of movement impairment that affects patients' quality of life is less obvious. OBJESTIVE: The aim of this study was to evaluate these tasks in detail and also see whether their use in combination could provide a better measure than each in isolation. We compared three reaction time tasks: saccadometry, and evoked and spontaneous tapping, using protocols as similar as possible, correlating the measurements within a group of PD patients and of age-matched controls. Surprisingly, manual and saccadic performance is uncorrelated in the normal population; but both are similarly affected by PD. The differences between groups are strengthened when the three measures are combined. Saccadic latency can be regarded as an appropriate surrogate for more general kinds of motor impairment. The combination of saccadic and manual parameters enhances their potential use in quantifying disease status and evaluating treatments.

Changes to Saccade Behaviors in Parkinson’s Disease Following Dancing and Observation of Dancing

Background: The traditional view of Parkinson’s disease (PD) as a motor disorder only treated by dopaminergic medications is now shifting to include non-pharmacologic interventions. We have noticed that patients with PD obtain an immediate, short-lasting benefit to mobility by the end of a dance class, suggesting some mechanism by which dancing reduces bradykinetic symptoms. We have also found that patients with PD are unimpaired at initiating highly automatic eye movements to visual stimuli (pro-saccades) but are impaired at generating willful eye movements away from visual stimuli (anti-saccades). We hypothesized that the mechanisms by which a dance class improves movement initiation may generalize to the brain networks impacted in PD (frontal lobe and basal ganglia, BG), and thus could be assessed objectively by measuring eye movements, which rely on the same neural circuitry.Methods: Participants with PD performed pro- and anti-saccades before, and after, a dance class. “Before” and “after” saccade performance measurements were compared. These measurements were then contrasted with a control condition (observing a dance class in a video), and with older and younger adult populations, who rested for an hour between measurements.Results: We found an improvement in anti-saccade performance following the observation of dance (but not following dancing), but we found a detriment in pro-saccade performance following dancing.Conclusion: We suggest that observation of dance induced plasticity changes in frontal-BG networks that are important for executive control. Dancing, in contrast, increased voluntary movement signals that benefited mobility, but interfered with the automaticity of efficient pro-saccade execution.

Neural Activity in the Macaque Putamen Associated with Saccades and Behavioral Outcome

It is now widely accepted that the basal ganglia nuclei form segregated, parallel loops with neocortical areas. The prevalent view is that the putamen is part of the motor loop, which receives inputs from sensorimotor areas, whereas the caudate, which receives inputs from frontal cortical eye fields and projects via the substantia nigra pars reticulata to the superior colliculus, belongs to the oculomotor loop. Tracer studies in monkeys and functional neuroimaging studies in human subjects, however, also suggest a potential role for the putamen in oculomotor control. To investigate the role of the putamen in saccadic eye movements, we recorded single neuron activity in the caudal putamen of two rhesus monkeys while they alternated between short blocks of pro- and anti-saccades. In each trial, the instruction cue was provided after the onset of the peripheral stimulus, thus the monkeys could either generate an immediate response to the stimulus based on the internal representation of the rule from the previous trial, or alternatively, could await the visual rule-instruction cue to guide their saccadic response. We found that a subset of putamen neurons showed saccade-related activity, that the preparatory mode (internally- versus externally-cued) influenced the expression of task-selectivity in roughly one third of the task-modulated neurons, and further that a large proportion of neurons encoded the outcome of the saccade. These results suggest that the caudal putamen may be part of the neural network for goal-directed saccades, wherein the monitoring of saccadic eye movements, context and performance feedback may be processed together to ensure optimal behavioural performance and outcomes are achieved during ongoing behaviour.

Effects of Strabismic Amblyopia and Strabismus without Amblyopia on Visuomotor Behavior, I: Saccadic Eye Movements

It has previously been shown that anisometropic amblyopia affects the programming and execution of saccades. The aim of the current study was to investigate the impact of strabismic amblyopia on saccade performance. Fourteen adults with strabismic amblyopia, 13 adults with strabismus without amblyopia, and 14 visually normal adults performed saccades and reach-to-touch movements to targets presented at ± 5° and ± 10° eccentricity during binocular and monocular viewing. Latency, amplitude, and peak velocity of primary and secondary saccades were measured. In contrast to visually normal participants who had shorter primary saccade latency during binocular viewing, no binocular advantage was found in patients with strabismus with or without amblyopia. Patients with amblyopia had longer saccade latency during amblyopic eye viewing (P < 0.0001); however, there were no significant differences in saccade amplitude precision among the three groups across viewing conditions. Further analysis showed that only patients with severe amblyopia and no stereopsis (n = 4) exhibited longer latency (which was more pronounced for more central targets; P < 0.0001), and they also had reduced amplitude precision during amblyopic eye viewing. In contrast, patients with mild amblyopia (n = 5) and no stereopsis had normal latency and reduced precision during amblyopic eye viewing (P < 0.001), whereas those with gross stereopsis (n = 5) had normal latency and precision. There were no differences in peak velocity among the groups. Distinct patterns of saccade performance according to different levels of visual acuity and stereoscopic losses in strabismic amblyopia were found. These findings were in contrast to those in anisometropic amblyopia in which the altered saccade performance was independent of the extent of visual acuity or stereoscopic deficits. These results were most likely due to different long-term sensory suppression mechanisms in strabismic versus anisometropic amblyopia.

The Primate Ventral Pallidum Encodes Expected Reward Value and Regulates Motor Action

Motor actions are facilitated when expected reward value is high. It is hypothesized that there are neurons that encode expected reward values to modulate impending actions and potentially represent motivation signals. Here, we present evidence suggesting that the ventral pallidum (VP) may participate in this process. We recorded single neuronal activity in the monkey VP using a saccade task with a direction-dependent reward bias. Depending on the amount of the expected reward, VP neurons increased or decreased their activity tonically until the reward was delivered, for both ipsiversive andcontraversive saccades. Changes in expected reward values were also associated with changes in saccade performance (latency and velocity). Furthermore, bilateral muscimol-induced inactivation of the VP abolished the reward-dependent changes in saccade latencies. These data suggest that the VP provides expected reward value signals that are used to facilitate or inhibit motor actions.

Saccadic eye movements in children: a developmental study

To our knowledge, there are no studies exploring the development of voluntary and reflexive saccades in children using different types of paradigms to investigate horizontal saccades. In the present study, we examined the development of horizontal saccades in children aged 6-15 years. Binocular eye movements were recorded using an infrared video-oculography system (mobileEBT(®), e(ye)BRAIN) in seventy-two children (aged 6-15). Several paradigms were used to stimulate reflexive and voluntary horizontal saccades: gap, step and overlap paradigms. Horizontal anti-saccades were also examined. In all paradigms, the latency of saccades decreased with the age of children and it did not depend on the direction of the saccades (left/right); the error rate in the anti-saccade task decreased with age; the gain of horizontal saccades improved with age; the peak velocity of horizontal saccades was stable throughout childhood. We conclude that saccadic performances are influenced by age and cortical circuits responsible for the preparation of reflexive or voluntary saccades are completed at 12 years old. These data could be used as reference values for further studies dealing with pathologic development.

Unique saccadic abilities associated with tourette syndrome: Pure and comorbid groups a controlled study

Tourette Syndrome (TS) is a childhood onset disorder characterized by motor and vocal tics. TS often co-occurs with Attention Deficit Hyperactivity Disorder (ADHD) and Obsessive-Compulsive Disorder (OCD). Since neural networks associated with TS overlap with that of saccadic eye movements, saccadic performance may reflect psychopathology underlying TS+comorbidity. The aims of the present study were to determine whether heterogeneity in TS samples and use of various saccadic conditions are responsible for inconsistent findings. We examined: (1) saccadic behaviour in children groups: TS-only, TS+ADHD, TS+ADHD+OCD and healthy Controls; (2) the effect of different saccadic conditions. Participants (8–16 years) either looked towards (prosaccade) or in the opposite direction (antisaccade) of a peripheral visual stimulus in three conditions: fixation dot disappeared simultaneously (standard), 200ms prior to (Gap200) and 800ms following (Overlap800) stimulus onset. The findings demonstrated that sample heterogeneity and use of various saccadic conditions contribute to inconsistent findings. The TS+ADHD+OCD group displayed an enhanced saccadic ability substantiating the hypothesis of an enhanced adaptive cognitive control in certain groups of children with TS. The TS+ADHD group displayed significantly higher rates of antisaccade errors and unable to reduce their error rates. These findings lend further support to the nosological hypothesis.

Impairment of voluntary saccades and facilitation of reflexive saccades do not co-occur in Parkinson’s disease

Reflexive saccades (fast eye movements) and voluntary saccades activate overlapping parts of the oculomotor system. It is assumed that striatal dopamine depletion in Parkinson’s disease (PD) only affects the voluntary saccadic system and that the often-reported facilitation of the reflexive saccadic system in PD is secondary to impairment of the voluntary saccadic system. If this assumption is correct, facilitation of reflexive saccades should co-occur with impaired performance of voluntary saccades in patients with PD. We measured reflexive and voluntary saccades in a group of patients with PD (both “on” and “off” medication) and a matching group of control subjects. Interestingly, performance measures showed strong positive correlations across reflexive and voluntary saccades in the PD group. Our results suggest that facilitation of reflexive saccades does not co-occur with impairment of voluntary saccades and that PD may affect the parts of the oculomotor system which are common to reflexive and voluntary saccade generation.

Evidence from cluster analysis for differentiation of antisaccade performance groups based on speed/accuracy trade-offs

Anti and pro-saccade performance in single or mixed contexts was explored in a large sample of young adults (n=281). ANOVAs were first conducted to evaluate trial type, context and gender effects. A cluster analysis was then used to determine whether subgroups could be identified based on saccadic performance variables. Increased antisaccade errors were observed among females and during mixed-saccade runs. Cluster analysis identified two groups: 1) increased errors clustered with faster latencies and 2) decreased errors clustered with slower latencies. These data offer justification for examining subgroups based on saccadic performance and may help elucidate mechanisms underlying response variability within and between different populations.

Saccade performance in the nasal and temporal hemifields

There are numerous asymmetries in anatomy between the nasal and temporal hemiretinae, which have been connected to various asymmetries in behavioral performance. These include asymmetries in Vernier acuity, saccade selection, and attentional function, in addition to some evidence for latency differences for saccadic eye movements. There is also evidence for stronger retinotectal neural projection from the nasal than the temporal hemiretina. There is, accordingly, good reason to predict asymmetries in saccadic performance depending on which hemifield the saccade trigger stimuli are presented in, but the evidence on this is mixed. We tested for asymmetries in both saccade latency and landing point accuracy in a variety of different saccade tasks. We found no evidence for any asymmetries in saccade latency and only modest evidence for asymmetries in landing point accuracy. While this lack of asymmetry is surprising in light of previous findings of attentional asymmetries, it may reflect that cortical input to midbrain eye control centers mitigates any retinal and retinotectal asymmetry.

What can fMRI tell us about functional variability in the oculomotor system and saccade performance?

Eye movement behavior is variable, and the brain's oculomotor circuitry may not always function consistently. In a recent fMRI study, Ozyurt and Greenlee (2011) correlated the activation strength of cortical and striatal brain regions with inter- and intraindividual variability in saccade performance. We discuss the design and implications of this study with regard to the differences between inter- and intraindividual variability, and the link between the BOLD signal and oculomotor activity.

Covert attention regulates saccadic reaction time by routing between different visual-oculomotor pathways

Covert attention modulates saccadic performance, e.g., the abrupt onset of a task-irrelevant visual stimulus grabs attention as measured by a decrease in saccadic reaction time (SRT). The attentional advantage bestowed by the task-irrelevant stimulus is short-lived: SRT is actually longer ~200 ms after the onset of a stimulus than it is when no stimulus appears, known as inhibition of return. The mechanism by which attention modulates saccadic reaction is not well-understood. Here, we propose two possible mechanisms: by selective routing of the visuomotor signal through different pathways (routing hypothesis) or by general modulation of the speed of visuomotor transformation (shifting hypothesis). To test them, we designed a cue gap paradigm in which a 100-ms gap was introduced between the fixation point disappearance and the target appearance to the conventional cued visual reaction time paradigm. The cue manipulated the location of covert attention, and the gap interval resulted in a bimodal distribution of SRT, with an early mode (express saccade) and a late mode (regular saccade). The routing hypothesis predicts changes in the proportion of express saccades vs. regular saccades, whereas the shifting hypothesis predicts a shift of SRT distribution. The addition of the cue had no effect on mean reaction time of express and regular saccades, but it changed the relative proportion of two modes. These results demonstrate that the covert attention modification of the mean SRT is largely attributed to selective routing between visuomotor pathways rather than general modulation of the speed of visuomotor transformation.

Comparison of vertical and horizontal saccade measures and their relation to gray matter changes in premanifest and manifest Huntington disease

Saccades are a potentially important biomarker of Huntington disease (HD) progression, as saccadic abnormalities can be detected both cross-sectionally and longitudinally. Although vertical saccadic impairment was reported decades ago, recent studies have focused on horizontal saccades. This study investigated antisaccade (AS) and memory guided saccade (MG) impairment in both the horizontal and vertical directions in individuals with the disease-causing CAG expansion (CAG+; n = 74), using those without the expansion (CAG-; n = 47) as controls. Percentage of errors, latency, and variability of latency were used to measure saccadic performance. We evaluated the benefits of measuring saccades in both directions by comparing effect sizes of horizontal and vertical measures, and by investigating the correlation of saccadic measures with underlying gray matter loss. Consistent with previous studies, AS and MG impairments were detected prior to the onset of manifest disease. Furthermore, the largest effect sizes were found for vertical saccades. A subset of participants (12 CAG-, 12 premanifest CAG+, 7 manifest HD) underwent magnetic resonance imaging, and an automated parcellation and segmentation procedure was used to extract thickness and volume measures in saccade-generating and inhibiting regions. These measures were then tested for associations with saccadic impairment. Latency of vertical AS was significantly associated with atrophy in the left superior frontal gyrus, left inferior parietal lobule, and bilateral caudate nuclei. This study suggests an important role for measuring vertical saccades. Vertical saccades may possess more statistical power than horizontal saccades, and the latency of vertical AS is associated with gray matter loss in both cortical and subcortical regions important in saccade function.

Saccades and Vergence Performance in a Population of Children with Vertigo and Clinically Assessed Abnormal Vergence Capabilities

PurposeEarly studies reported some abnormalities in saccade and vergence eye movements in children with vertigo and vergence deficiencies. The purpose of this study was to further examine saccade and vergence performance in a population of 44 children (mean age: 12.3±1.6 years) with vertigo symptoms and with different levels of vergence abnormalities, as assessed by static orthoptic examination (near point of convergence, prism bar and cover-uncover test).MethodsThree groups were identified on the basis of the orthoptic tests: group 1 (n = 13) with vergence spasms and mildly perturbed orthoptic scores, group 2 (n = 14) with moderately perturbed orthoptic scores, and group 3 (n = 17) with severely perturbed orthoptic scores. Data were compared to those recorded from 28 healthy children of similar ages. Latency, accuracy and peak velocity of saccades and vergence movements were measured in two different conditions: gap (fixation offset 200 ms prior to target onset) and simultaneous paradigms. Binocular horizontal movements were recorded by a photoelectric device.ResultsGroup 2 of children with vergence abnormalities showed significantly longer latency than normal children in several types of eye movements recorded. For all three groups of children with vergence abnormalities, the gain was poor, particularly for vergence movement. The peak velocity values did not differ between the different groups of children examined.InterpretationEye movement measures together with static orthoptic evaluation allowed us to better identify children with vergence abnormalities based on their slow initiation of eye movements. Overall, these findings support the hypothesis of a central deficit in the programming and triggering of saccades and vergence in these children.