Mark Harwood

The Spectral Main Sequence of Human Saccades

Despite the many models of saccadic eye movements, little attention has been paid to the shape of saccade trajectories. Some investigators have argued that saccades are driven by a rectangular “bang-bang” neural control signal, whereas others have emphasized the similarity to fast arm movement trajectories, such as the “minimum jerk” profile. However, models have not been tested rigorously against empirical trajectories. We examined the Fourier transforms of saccades and compared them with theoretical models. Horizontal saccades were recorded from 10 healthy subjects. The Fourier transform of each saccade was accurately computed using a padded fast Fourier transform (FFT), and the frequencies of the first three minima (M1, M2, M3) in each energy spectrum were measured to a precision of 0.12 Hz. Each subject showed near-linear trends in the relationships among M1, M2, and M3 and the reciprocal of duration (1/T), which we call the “spectral main sequence.” Extrapolation of plots did not pass through the origin, indicating a subtle departure from self-similarity. Bivariate confidence regions were established to allow for slope-intercept variability. The nonharmonic relationships seen cannot arise from a rectangular saccadic pulse driving a linear ocular plant. The relationships are also incompatible with minimum acceleration, minimum jerk, or higher-order minimum square derivative trajectories. The best fits were made by trajectories that minimize postmovement variance with signal-dependent noise (Harris and Wolpert, 1998). It is concluded that the spectral main sequence is exquisitely sensitive to the saccade trajectory and should be used to test objectively all present and future models of saccades.

Comparison of the main sequence of reflexive saccades and the quick phases of optokinetic nystagmus

BACKGROUND/AIMS Abnormalities in the saccadic main sequence are an important finding and may indicate pathology of the ocular motor periphery or central neurological disorders. In young or uncooperative patients it can be difficult eliciting a sufficient number of saccades to measure the main sequence. It is often assumed that the quick phases of optokinetic nystagmus (OKN) are identical to saccades. If this were the case, it would be feasible to use OKN, an involuntary response that is easily evoked, as a simple way of eliciting many saccades. The aim of this study was to determine whether reflexive saccades and the quick phases of OKN are indeed identical, and whether OKN quick phases could have a clinical role in identifying patients with slow saccades. METHODS OKN and reflexive saccades were recorded from 10 healthy adults using an infrared limbus eye tracker and bitemporal DC electro-oculography simultaneously. OKN was stimulated by rotating a full field patterned curtain around the subject at 10–50°/s. Reflexive saccades were elicited to red LED targets at 5–20° eccentricity. RESULTS OKN quick phases tended to have a longer duration compared to saccades, but these differences were not significant. OKN quick phases had a slightly lower peak velocity compared to saccades, which was statistically significant (p<0.05). CONCLUSION The main sequence for duration is the same for reflexive saccades and OKN quick phases. The main sequence for peak velocity is slightly faster for reflexive saccades than OKN quick phases, but the difference is unlikely to be of clinical significance. As an illustration of the potential of this technique, the authors demonstrate that OKN quick phases show similar slowness to saccades in a child with brainstem pathology caused by Gaucher disease type III. It is concluded that recording OKN may be a simple clinical means for approximating the main sequence.

Abnormalities of optokinetic nystagmus in progressive supranuclear palsy

Objectives: To measure vertical and horizontal responses to optokinetic (OK) stimulation and investigate directional abnormalities of quick phases in progressive supranuclear palsy (PSP). Methods: Saccades and OK nystagmus were studied in six PSP patients, five with Parkinson’s disease (PD), and 10 controls. The OK stimulus subtended 72° horizontally, 60° vertically, consisted of black and white stripes, and moved at 10–50°/s. Results: All PSP patients showed slowed voluntary vertical saccades and nystagmus quick phases compared with PD or controls. Small, paired, horizontal saccadic intrusions (SWJ) were more frequent and larger in PSP during fixation. Vertical saccades were transiently faster at the time of SWJ and horizontal saccades in PSP. During vertical OK nystagmus, small quick phases were often combined with horizontal SWJ in all subjects; in PSP the vector was closer to horizontal. Vertical OK slow phase gain was reduced in PSP but, in most PD patients, was similar to normals. The average position of gaze shifted in the direction of vertical OK stimulus in PSP patients with preserved slow phase responses but impaired quick phases. Conclusions: Vertical OK responses in PSP show impaired slow phase responses, and quick phases that are slowed and combined with SWJ to produce an oblique vector. SWJ facilitate vertical saccades and quick phases in PSP, but it is unclear whether this is an adaptive process or a result of the disease. A large OK stimulus is useful to induce responses that can be quantitatively analysed in patients with limited voluntary range of vertical gaze.

Saccade adaptation specific to visual context.

When saccades consistently overshoot their targets, saccade amplitudes gradually decrease, thereby maintaining accuracy. This adaptive process has been seen as a form of motor learning that copes with changes in physical parameters of the eye and its muscles, brought about by aging or pathology. One would not expect such a motor-repair mechanism to be specific to the visual properties of the target stimulus. We had subjects make saccades to sudden movements of either of two targets-a steadily illuminated circle or a flickering circle-one of which stepped back during each saccade it elicited, simulating the effect of a hypermetric saccade. Saccade gain (saccade amplitude/target amplitude) decreased by 15% for the target that stepped back versus 6% for the target that did not step back. Most of the change in gain between successive blocks of trials of each type occurred on the first saccade of the block, decreasing by 0.12 on the first trial of a step-back block and increasing by 0.1 on the first trial of a no-step-back block. The differential adaptation of the two targets required postsaccadic feedback of both target types, as shown in a separate experiment, in which saccades to only one target received feedback, and the gain did not differ between the two target types. This demonstration that a context defined by a visual stimulus can serve as an effective cue for switching saccade gain between states suggests that saccade adaptation may have a heretofore unsuspected dimension of adaptability.

Evaluating small eye movements in patients with saccadic palsies.

Slow saccades are an important diagnostic feature of a range of degenerative, metabolic, and genetic diseases of the nervous system. Many affected patients have difficulty initiating saccades, and the movements themselves may be small, making it difficult to make comparisons with control subjects. A large‐field optokinetic stimulus may elicit quick phases of nystagmus in patients who cannot initiate voluntary saccades, but these movements may also be small. We show that it is still possible to compare amplitude‐duration and amplitude‐peak velocity relations with controls if data are fit with a power function (rather than an exponential equation). When analyzed this way, the dynamic properties of small saccades and quick phases from patients with progressive supranuclear palsy (PSP) could be differentiated from fast movements made by patients with idiopathic Parkinsons disease or controls. Normal saccades show a fairly constant ratio: peak velocity/mean velocity (Q ∼1.6 for vertical saccades). This ratio was abnormally high (Q >3) for some larger saccades made by patients with PSP, suggesting that either these movements were not entirely saccadic or that they were composed of a series of small saccades.

Oscillatory alpha-band suppression mechanisms during the rapid attentional shifts required to perform an anti-saccade task

Neuroimaging has demonstrated anatomical overlap between covert and overt attention systems, although behavioral and electrophysiological studies have suggested that the two systems do not rely on entirely identical circuits or mechanisms. In a parallel line of research, topographically-specific modulations of alpha-band power (~8-14 Hz) have been consistently correlated with anticipatory states during tasks requiring covert attention shifts. These tasks, however, typically employ cue-target-interval paradigms where attentional processes are examined across relatively protracted periods of time and not at the rapid timescales implicated during overt attention tasks. The anti-saccade task, where one must first covertly attend for a peripheral target, before executing a rapid overt attention shift (i.e. a saccade) to the opposite side of space, is particularly well-suited for examining the rapid dynamics of overt attentional deployments. Here, we asked whether alpha-band oscillatory mechanisms would also be associated with these very rapid overt shifts, potentially representing a common neural mechanism across overt and covert attention systems. High-density electroencephalography in conjunction with infra-red eye-tracking was recorded while participants engaged in both pro- and anti-saccade task blocks. Alpha power, time-locked to saccade onset, showed three distinct phases of significantly lateralized topographic shifts, all occurring within a period of less than 1s, closely reflecting the temporal dynamics of anti-saccade performance. Only two such phases were observed during the pro-saccade task. These data point to substantially more rapid temporal dynamics of alpha-band suppressive mechanisms than previously established, and implicate oscillatory alpha-band activity as a common mechanism across both overt and covert attentional deployments.

Saccade adaptation as a model of flexible and general motor learning.

The rapid point-to-point movements of the eyes called saccades are the most commonly made movement by humans, yet differ from nearly every other type of motor output in that they are completed too quickly to be adjusted during their execution by visual feedback. Saccadic accuracy remains quite high over a lifetime despite inevitable changes to the physical structures controlling the eyes, indicating that the oculomotor system actively monitors and adjusts motor commands to achieve consistent behavioral production. Indeed, it seems that beyond the ability to compensate for slow, age-related bodily changes, saccades can be modified following traumatic injury or pathology that affects their production, or in response to more short-term systematic alterations to post-saccadic visual feedback in a laboratory setting. These forms of plasticity rely on the visual detection of accuracy errors by a unified set of mechanisms that support the process known as saccade adaptation. Saccade adaptation has been mostly studied as a phenomenon in its own right, outside of motor learning in general. Here, we highlight the commonalities between eye and arm movement adaptation by reviewing the literature across these fields wherever there are compelling overlapping theories or data. Recent exciting findings are challenging previous interpretations of the underlying mechanisms of saccade adaptation with the incorporation of concepts including prediction, reinforcement and contextual learning. We review the emerging ideas and evidence with particular emphasis on the important contributions made by Josh Wallman in this sphere over the past 15 years.

Infant saccades are not slow

Saccadic eye movements are essential for redirecting the fovea at different visual targets. In adults and children saccades are remarkably stereotyped. Peak velocity and duration of saccades are a simple function of saccade amplitude called the ‘main sequence’. Saccades that are substantially slower than normal often reflect disease of the brain stem saccade generator but may also be associated with diseases of higher level structures including the cerebral hemispheres and superior colliculus. However, little is known about the speed of saccades in infancy. A single previous study reported that infant saccades may be similar to or slower than those of adults, but few saccades were recorded. The present study re‐examined this issue with the technique of measuring optokinetic (OKN) quick phases, which are readily elicited from healthy and sick infants, with a view to using saccade speed as a quantitative neurological measure. We measured the duration and peak velocity of saccades (main sequence) using direct‐current electro‐oculography from OKN quick phases in 18 infants (nine males, nine females) aged 2 to 18 months (mean age 8mo [SD 4]) and seven adult comparison participants (four males, three females; age range 21–32y, mean age 27y [SD 3]). All infant saccades showed typical relationships between duration, peak velocity, and amplitude. Overall, there was no statistically significant difference between adult and infant main sequences for duration or peak velocity. However, the differences in the main sequence for duration almost reached significance (p= 0.051) for infant saccades being faster than adults. Individual differences were also present, and some infants produced saccades faster than adults, but not slower. There was no significant age trend. We conclude that measuring saccade speed is practicable in the young infant. From the age of at least 2 months, infants generate saccades with speeds similar to or slightly higher than those of adults.

Saccade adaptation is unhampered by distractors.

Saccade adaptation has been extensively studied using a paradigm in which a target is displaced during the saccade, inducing an adjustment in saccade amplitude or direction. These changes in saccade amplitude are widely considered to be controlled by the post-saccadic position of the target relative to the fovea. However, because such experiments generally employ only a single target on an otherwise blank screen, the question remains whether the same adaptation could occur if both the target and a similar distractor were present when the saccade landed. To investigate this issue, three experiments were conducted, in which the post-saccadic locations of the target and distractor were varied. Results showed that decreased amplitude adaptation, increased amplitude adaptation, and recovery from adaptation were controlled by the post-saccadic position of the target rather than the distractor. These results imply that target selection is critical to saccade adaptation.

Saccade adaptation goes for the goal.

The oculomotor system maintains saccade accuracy by adjusting saccades that are consistently inaccurate. Four experiments were performed to determine the relative contribution of background and target postsaccadic displacement. Unlike typical saccade adaptation experiments, we used natural image scenes and masked target and background displacements during the saccade to exclude motion signals from allowing detection of the displacements. We found that the background had no effect on saccade gain while the target drove gain changes. Only when the target was blanked after the saccade did we observe some adaptation in the direction of the background displacement. We conclude that target selection is critical to saccade adaptation, and operates effectively against natural image backgrounds.