Oculomotor Phenomena Research Articles

Visual feature tuning properties of stimulus-driven saccadic inhibition in macaque monkeys.

Saccadic inhibition refers to a short-latency transient cessation of saccade generation after visual sensory transients. This oculomotor phenomenon occurs with a latency that is consistent with a rapid influence of sensory responses, such as stimulus-induced visual bursts, on oculomotor control circuitry. However, the neural mechanisms underlying saccadic inhibition are not well understood. Here, we exploited the fact that macaque monkeys experience robust saccadic inhibition to test the hypothesis that inhibition time and strength exhibit systematic visual feature tuning properties to a multitude of visual feature dimensions commonly used in vision science. We measured saccades in three monkeys actively controlling their gaze on a target, and we presented visual onset events at random times. Across seven experiments, the visual onsets tested size, spatial frequency, contrast, orientation, motion direction, and motion speed dependencies of saccadic inhibition. We also investigated how inhibition might depend on the behavioral relevance of the appearing stimuli. We found that saccadic inhibition starts earlier, and is stronger, for large stimuli of low spatial frequencies and high contrasts. Moreover, saccadic inhibition timing depends on motion direction and orientation, with earlier inhibition systematically occurring for horizontally drifting vertical gratings. On the other hand, saccadic inhibition is stronger for faster motions and when the appearing stimuli are subsequently foveated. Besides documenting a range of feature tuning dimensions of saccadic inhibition to the properties of exogenous visual stimuli, our results establish macaque monkeys as an ideal model system for unraveling the neural mechanisms underlying a ubiquitous oculomotor phenomenon in visual neuroscience.NEW & NOTEWORTHY Visual onsets dramatically reduce saccade generation likelihood with very short latencies. Such latencies suggest that stimulus-induced visual responses, normally jump-starting perceptual and scene analysis processes, can also directly impact the decision of whether to generate saccades or not, causing saccadic inhibition. Consistent with this, we found that changing the appearance of the visual onsets systematically alters the properties of saccadic inhibition. These results constrain neurally inspired models of coordination between saccade generation and exogenous sensory stimulation.

Urgency forces stimulus-driven action by overcoming cognitive control.

Intelligent behavior requires to act directed by goals despite competing action tendencies triggered by stimuli in the environment. For eye movements, it has recently been discovered that this ability is briefly reduced in urgent situations (Salinas et al., 2019). In a time-window before an urgent response, participants could not help but look at a suddenly appearing visual stimulus, even though their goal was to look away from it. Urgency seemed to provoke a new visual-oculomotor phenomenon: A period in which saccadic eye movements are dominated by external stimuli, and uncontrollable by current goals. This period was assumed to arise from brain mechanisms controlling eye movements and spatial attention, such as those of the frontal eye field. Here, we show that the phenomenon is more general than previously thought. We found that also in well-investigated manual tasks, urgency made goal-conflicting stimulus features dominate behavioral responses. This dominance of behavior followed established trial-to-trial signatures of cognitive control mechanisms that replicate across a variety of tasks. Thus together, these findings reveal that urgency temporarily forces stimulus-driven action by overcoming cognitive control in general, not only at brain mechanisms controlling eye movements.

Under time pressure, the exogenous modulation of saccade plans is ubiquitous, intricate, and lawful.

The choice of where to look next is determined by both exogenous (bottom-up) and endogenous (top-down) factors, but details of their interaction and distinct contributions to target selection have remained elusive. Recent experiments with urgent choice tasks, in which stimuli are evaluated while motor plans are already advancing, have greatly clarified these contributions. Specifically, exogenous modulations associated with stimulus detection act rapidly and briefly (∼25ms) to automatically halt and/or boost ongoing motor plans as per spatial congruence rules. These stereotypical modulations explain, in quantitative detail, characteristic features of many saccadic tasks (e.g. antisaccade, countermanding, saccadic-inhibition, gap, and double-step). Thus, the same low-level visuomotor interactions contribute to diverse oculomotor phenomena traditionally attributed to different neural mechanisms.

Auditory stimuli degrade visual performance in virtual reality

We report an auditory effect of visual performance degradation in a virtual reality (VR) setting, where the viewing conditions are significantly different from previous studies. With the presentation of temporally congruent but spatially incongruent sound, we can degrade visual performance significantly at detection and recognition levels. We further show that this effect is robust to different types and locations of both auditory and visual stimuli. We also analyze participants behavior with an eye tracker to study the underlying cause of the degradation effect. We find that the performance degradation occurs even in the absence of saccades towards the sound source, during normal gaze behavior. This suggests that this effect is not caused by oculomotor phenomena, but rather by neural interactions or attentional shifts.

Effects of reward on oculomotor control.

The present study examines the extent to which distractors that signal the availability of monetary reward on a given trial affect eye movements. We used a novel eye movement task in which observers had to follow a target around the screen while ignoring distractors presented at varying locations. We examined the effects of reward magnitude and distractor location on a host of oculomotor properties, including saccade latency, amplitude, landing position, curvature, and erroneous saccades toward the distractor. We found consistent effects of reward magnitude on classic oculomotor phenomena such as the remote distractor effect, the global effect, and oculomotor capture by the distractor. We also show that a distractor in the visual hemifield opposite to the target had a larger effect on oculomotor control than an equidistant distractor in the same hemifield as the target. Bayesian hierarchical drift diffusion modeling revealed large differences in drift rate depending on the reward value, location, and visual hemifield of the distractor stimulus. Our findings suggest that high reward distractors not only capture the eyes but also affect a multitude of oculomotor properties associated with oculomotor inhibition and control.

Descriptions of vestibular migraine and Menière's disease in Greek and Chinese antiquity.

Background Vestibular migraine and Menière's disease are two types of episodic vertigo syndromes that were already observed in Greek and Chinese antiquity. Descriptions first appeared in the work of the classical Greek physician Aretaeus of Cappadocia, who lived in the 2nd century AD, and in Huangdi Neijing, a seminal medical source in the Chinese Medical Classics, written between the 2nd century BC and the 2nd century AD. Aim The aim of this paper is to search in Aretaeus' book De causis et signis acutorum et chronicorum morborum and in Huangdi Neijing for descriptions of vertigo co-occurring with headache or ear symptoms that resemble current classifications of vestibular migraine or Menière's disease. Results Aretaeus describes a syndrome combining headache, vertigo, visual disturbance, oculomotor phenomena, and nausea that resembles the symptoms of vestibular migraine. In the Chinese book Huangdi Neijing the Yellow Thearch mentions the co-occurrence of episodic dizziness and a ringing noise of the ears that recalls an attack of Menière's disease. Conclusions The descriptions of these two conditions in Greek and Chinese antiquity are similar to the vertigo syndromes currently classified as vestibular migraine and Menière's disease. In clinical practice it may be difficult to clearly differentiate between them, and they may also co-occur.

Saccadic inhibition and the remote distractor effect: One mechanism or two?

It has been hotly debated whether a single mechanism underlies two established and highly robust oculomotor phenomena thought to index the competitive nature of eye movement plans: the remote distractor effect and saccadic inhibition (SI). It has been suggested that a transient mechanism underlying SI would not be able to account for the shift in the saccade latency distribution produced by early distractors (e.g., those appearing 60 ms before target onset) without additional assumptions or a more sustained source of inhibition. Here we tested this prediction with a model previously optimized to capture SI for late distractors. Where behavioral studies have intermingled stimulus onset asynchronies (SOAs) within the same block, the model captures the pattern of RDEs and SI effects with no parameter changes. Where SOAs have been blocked behaviorally, the pattern of RDEs can also be captured by the same model architecture, but requires changes to the inputs of the model between SOAs. Such changes plausibly reflect likely changes in participants' expectations and attentional strategy across block types.

Fixed and dilated: the history of a classic pupil abnormality.

The aim of this study was to investigate the development of ideas about the nature and mechanism of the fixed dilated pupil, paying particular attention to experimental conditions and clinical observations in the 19th century. Starting from Kocher's standard review in 1901, the authors studied German, English, and French texts for historical information. Medical and neurological textbooks from the 19th and 20th centuries were reviewed to investigate when and how this information percolated through neurological and neurosurgical practices. Cooper experimented with intracranial pressure (ICP) in a dog in the 1830s, but did not mention the pupils. He described dilated pupils in clinical cases without referring to the effect of light. Bright demonstrated to have some knowledge of the pupil sign (clinical observations). Realizing the unreliability of the pupil sign, Hutchinson in 1867-1868 tried to reason in which cases trepanation would be advisable. Von Leyden's 1866 animal experiments, in which he increased CSF volume by injecting protein solutions intracranially, was the first observation in which the association between fixed dilated pupils and increased ICP was established. Along with bradycardia and motor and respiratory effects, he noticed wide pupils were usually present in a comatose state. Asymmetrical dilation could not always be attributed to increased ICP, but to an oculomotor nerve lesion. Pagenstecher in 1871 extended knowledge by meticulously studying consecutive pupil phenomena with increasing pressure. In 1880, von Bergmann emphasized the significance of the ipsilateral dilation in experiments as well as in clinical cases. He distinguished the extent of pressure increase and its duration. Probably confusing irritation (epileptic head turning to the other side with pupil dilation) and lesion effects, he suggested a cortical area responsible for oculomotor phenomena, indicating what is now known as the frontal eye field. Naunyn and Schreiber (1881) understood the relationship between increased ICP with pupil dilation and decreased pulse frequency and blood pressure, warning not to decrease the latter. Concentrating on experimental traumatic effects, Duret (1878) investigated compression and commotion, in which he distinguished two phases, notably pupil constriction by bulbar lesions, due to CSF shock, followed by dilation from congestion and inflammation, due to blood around the oculomotor nerve. The key observation of a fixed dilated pupil as a sign of acute mass effect came gradually and after some localization stumbles. Following the period of extensive experimental research in ICP, the results of which were translated to clinical observations, the prognostic significance was gradually acknowledged by authors of neurological textbooks. It is well known that Cushing did similar experiments in Berne (1900-1901), and later suggested he would not have done so if he had studied the literature.

Temporal Oculomotor Inhibition of Return and Spatial Facilitation of Return in a Visual Encoding Task

*Correspondence: John M. Henderson, Visual Cognition Laboratory, Institute for Mind and Brain and Department of Psychology, University of South Carolina, 1800 Gervais Street, Columbia, SC 29208, USA e-mail: john.henderson@sc.edu Oculomotor inhibition of return (O-IOR) is an increase in saccade latency prior to an eye movement to a recently fixated location compared to other locations. It has been proposed that this temporal O-IOR may have spatial consequences, facilitating foraging by inhibiting return to previously attended regions. In order to test this possibility, participants viewed arrays of objects and of words while their eye movements were recorded.Temporal O-IOR was observed, with equivalent effects for object and word arrays, indicating that temporal O-IOR is an oculomotor phenomenon independent of array content.There was no evidence for spatial inhibition of return (IOR). Instead, spatial facilitation of return was observed: participants were significantly more likely than chance to make return saccades and to refixate just-visited locations. Further, the likelihood of making a return saccade to an object or word was contingent on the amount of time spent viewing that object or word before leaving it. This suggests that, unlike temporal O-IOR, return probability is influenced by cognitive processing. Taken together, these results are inconsistent with the hypothesis that IOR functions as a foraging facilitator. The results also provide strong evidence for a different oculomotor bias that could serve as a foraging facilitator: saccadic momentum, a tendency to repeat the most recently executed saccade program.We suggest that models of visual attention could incorporate saccadic momentum in place of IOR.

Temporal oculomotor inhibition of return and spatial facilitation of return in a visual encoding task

Oculomotor inhibition of return (O-IOR) is an increase in saccade latency prior to an eye movement to a recently fixated location compared to other locations. It has been proposed that this temporal O-IOR may have spatial consequences, facilitating foraging by inhibiting return to previously attended regions. In order to test this possibility, participants viewed arrays of objects and of words while their eye movements were recorded. Temporal O-IOR was observed, with equivalent effects for object and word arrays, indicating that temporal O-IOR is an oculomotor phenomenon independent of array content. There was no evidence for spatial inhibition of return (IOR). Instead, spatial facilitation of return was observed: participants were significantly more likely than chance to make return saccades and to re-fixate just-visited locations. Further, the likelihood of making a return saccade to an object or word was contingent on the amount of time spent viewing that object or word before leaving it. This suggests that, unlike temporal O-IOR, return probability is influenced by cognitive processing. Taken together, these results are inconsistent with the hypothesis that IOR functions as a foraging facilitator. The results also provide strong evidence for a different oculomotor bias that could serve as a foraging facilitator: saccadic momentum, a tendency to repeat the most recently executed saccade program. We suggest that models of visual attention could incorporate saccadic momentum in place of IOR.

Oculomotor inhibition of return in normal and mindless reading

Oculomotor inhibition of return (O-IOR) is an increase in saccade latency prior to an eye movement to a recently fixated location, as compared with other locations. To investigate O-IOR in reading, subjects participated in two conditions while their eye movements were recorded: normal reading and mindless reading with words replaced by geometric shapes. We investigated the manifestation of O-IOR in reading and whether it is related to extracting meaning from the text or is an oculomotor phenomenon. The results indicated that fixation durations prior to a saccade returning to the immediately preceding fixated word were longer than those to other words, consistent with O-IOR. Furthermore, fixation durations were longest prior to a saccade that returned the eyes to the specific character position in the word that had previously been fixated and dropped off as the distance between the previously fixated character and landing position increased. This result is consistent with the hypothesis that O-IOR is relatively precise in its application during reading and drops off as a gradient. Both of these results were found for text reading and for mindless reading, suggesting that they are consequences of oculomotor control, and not of language processing. Finally, although these temporal IOR effects were robust, no spatial consequences of IOR were observed: Previously fixated words and characters were as likely to be refixated as new words and characters.

Oculomotor Inhibition of Return in Normal and Mindless Reading

Oculomotor inhibition of return (O-IOR) is an increase in saccade latency prior to an eye movement to a recently fixated location compared to other locations. To investigate O-IOR in reading, subjects participated in two conditions while their eye movements were recorded: normal reading, and mindless reading in which words were replaced by equivalent geometric shapes. We investigated the manifestation of O-IOR in reading, and whether it is related to extracting meaning from the text or is a purely oculomotor phenomenon. The results indicated that fixation durations prior to a saccade returning to the last fixated word were longer than to other words, consistent with O-IOR. Furthermore, this effect was spatially specific: Fixation durations were longest prior to a saccade that returned the eyes to the character in the word that had previously been fixated, and dropped off as the distance between the previously fixated character and landing position increased. This result is consistent with the hypothesis that IOR is applied to the fixated character location during reading and drops off as a spatial gradient. Both of these results were found for text reading and for mindless reading, suggesting that they are consequences of oculomotor control and not of language processing. Finally, although the temporal IOR effects were robust, no spatial consequences of IOR were observed: Previously fixated words and characters were as likely to be re-fixated as new words and characters. Meeting abstract presented at VSS 2012

What Sherrington missed: the ubiquity of the neural integrator

Despite its numerous illustrations unequivocally demonstrating the phenomenon, in Sherrington's Integrative Action of the Nervous System, he considered "integration" only in its spatial and coordinative aspects, and failed to notice time integration as an equally pervasive feature of all motor systems. First demonstrated in the oculomotor system by Robinson and others, in the vestibulo-ocular reflex, and then as a necessary component of the oculomotor "final common path" (another Sherringtonian concept), integration is manifested at two further levels: in generating optokinetic responses and in the mechanism of saccadic decision. But integration is not a purely oculomotor phenomenon: behind it lie two fundamental motor principles. First, that the brain operates in terms of change, implying differentiation in sensory systems and integration in motor ones. Second, that the molecular physiology of muscle contraction means that remaining still requires not only continual expenditure of energy but also continual computational effort--a firm and precise integrator.

Eye Movements and Abducens Motoneuron Behavior after Cholinergic Activation of the Nucleus Reticularis Pontis Caudalis

the aim of this work was to characterize eye movements and abducens (ABD) motoneuron behavior after cholinergic activation of the nucleus reticularis pontis caudalis (NRPC). six female adult cats were prepared for chronic recording of eye movements (using the scleral search-coil technique), electroencephalography, electromyography, ponto-geniculo-occipital (PGO) waves in the lateral geniculate nucleus, and ABD motoneuron activities after microinjections of the cholinergic agonist carbachol into the NRPC. unilateral microinjections of carbachol in the NRPC induced tonic and phasic phenomena in the oculomotor system. Tonic effects consisted of ipsiversive rotation to the injected side, convergence, and downward rotation of the eyes. Phasic effects consisted of bursts of rhythmic rapid eye movements directed contralaterally to the injected side along with PGO-like waves in the lateral geniculate and ABD nuclei. Although tonic effects were dependent on the level of drowsiness, phasic effects were always present and appeared along with normal saccades when the animal was vigilant. ABD motoneurons showed phasic activities associated with ABD PGO-like waves during bursts of rapid eye movements, and tonic and phasic activities related to eye position and velocity during alertness. the cholinergic activation of the NRPC induces oculomotor phenomena that are somewhat similar to those described during REM sleep. A precise comparison of the dynamics and timing of the eye movements further suggests that a temporal organization of both NRPCs is needed to reproduce the complexity of the oculomotor behavior during REM sleep.

On the launch-site effect for skipped words during reading

The launch-site effect, a systematic variation of within-word landing position as a function of launch-site distance, is among the most important oculomotor phenomena in reading. Here we show that the launch-site effect is strongly modulated in word skipping, a finding which is inconsistent with the view that the launch-site effect is caused by a saccadic-range error. We observe that distributions of landing positions in skipping saccades show an increased leftward shift compared to non-skipping saccades at equal launch-site distances. Using an improved algorithm for the estimation of mislocated fixations, we demonstrate the reliability of our results.

Anticompensatory eye position ("contraversion") in optokinetic nystagmus.

The quick phases of full-field optokinetic nystagmus (OKN) not only reset the eyes, but also move them in an anticompensatory direction (that is, in the opposite direction to stimulus movement, “contraversion”).1–7 Although recognized as an oculomotor phenomenon, contraversion is poorly understood, and it has been suggested as a strategy for directing the line of sight into the visual field from which motion is originating.5–7 We have previously observed extreme contraversion in patients with absent smooth pursuit and a leaky eye position integrator.8 In this study we examined contraversion in healthy adults and propose a model for this behaviour based on observation from a clinical group.

Oculomotor phenomena in petit-mal

Objective: To determine the temporal relationship among behavior, eye movements and respiration during absence seizures.Method: This included simultaneous videorecording of a patient's face, EEG and respirogram, in 5 patients with absence seizures. Absence seizures were defined as a sudden lapse of consciousness with impairment of mental functions. Oculomotor phenomena consisted of: eye fluttering, eye deviation (conjugate lateral or upward deflection), and eye-opening.Results: Oculomotor phenomena began 1 2/3–3 s after the onset of the electrographic discharge and ended before the discharge. The most frequent events were eye-opening, stare with or without palpebral myoclonias, and tonic or clonic upward movements. Downward movement or convergence was not observed as well as head version. Respiratory changes (apnea) are the last events to occur.Conclusions: absence seizures were characterized by the onset of a 3/s spike-slow wave discharge followed by oculomotor phenomena and respiratory changes. The time course suggests that epileptic discharges precede and then involve oculomotor and respiratory brainstem centers.

Spatial attention and latencies of saccadic eye movements

Recent theories of visual attention, such as the oculomotor readiness theory of Klein (1980) (Does oculomotor readiness mediate cognitive control of the visual attention. In: R. Nickerson, Attention and performance, Hillsdale: Erlbaum), the premotor theory of Rizzolati (1983) (Mechanisms of selective attention in mammals. In: J.P. Ewart, R.R. Capranica, D.J. Ingle, Advances in vertebrate Neuroethology (pp. 261–297). New York: Plenum) and the sequential attention theory of Henderson (1992) (Visual attention and eye movement control during reading and scene perception. In K. Rayner, Eye movements and visual cognition (260–283). New York: Springer-Verlag), propose a link between shifts in spatial attention and the generation of saccadic eye movements. In this paper we show that a winner-take-all model of spatial attention, combined with a simple model for the link between attention and eye movements, can account for the variation in saccadic latency observed in many oculomotor phenomena. These phenomena include the gap effect (Saslow M.G. (1967). Effects of components of displacement-step stimuli upon latency for saccadic eye movement. Journal of the Optical Society of America, 57, 1024–1029), the effect of target jumps on saccadic latency (Becker W. & Jurgens R. (1979). An analysis of the saccadic system by means of double step stimuli. Vision Research, 19, 967–983), the increase of saccadic latency as target eccentricity drops (Kalesnykas R.P. & Hallett P.E. (1994). Retinal eccentricity and the latency of eye saccades. Vision Research, 34, 517–531), and the modulation of saccadic accuracy using target predictability and saccadic latency (Coëffé C. & O’Regan J.K. (1987). Reducing the influence of non-target stimuli on saccade accuracy: predictability and latency effects. Vision Research, 27 (2), 227–240).

Perceptual, oculomotor, and neural responses to moving color plaids.

Moving plaids constructed from two achromatic gratings of identical luminance contrast are known to yield a percept of coherent pattern motion, as are plaids constructed from two identical chromatic (e.g. isoluminant red/green) gratings. To examine the interactive influences of chromatic and luminance contrast on the integration of visual motion signals, we constructed plaids with gratings that possessed both forms of contrast. We used plaids of two basic types, which differed with respect to the phase relationship between chromatic and luminance modulations (after Kooi et al, 1992 Perception 21 583-598). One plaid type ('symmetric') was made from component gratings that had identical chromatic/luminance phase relationships (e.g. both components were red-bright/green-dark modulation). The second plaid type ('asymmetric') was made from components that had complimentary phase relationships (i.e. one red-bright/green-dark grating and one green-bright/red-dark grating). Human subjects reported that the motion of symmetric plaids was perceptually coherent, while the components of asymmetric plaids failed to cohere. We also recorded eye movements elicited by both types of plaids to determine if they are similarly affected by these image cues for motion coherence. Results demonstrate that, under many conditions, eye movements elicited by perceptually coherent vs noncoherent plaids are distinguishable from one another. To reveal the neural bases of these perceptual and oculomotor phenomena, we also recorded the responses of neurons in the middle temporal visual area (area MT) of macaque visual cortex. Here we found that individual neurons exhibited differential tuning to symmetric vs asymmetric plaids. These neurophysiological results demonstrate that the neural mechanism for motion coherence is sensitive to the phase relationship between chromatic and luminance contrast, a finding which has implications for interactions between 'color' and 'motion' processing streams in the primate visual system.

Torsional rebound nystagmus in a patient with type I Chiari malformation

In a 41-year old female patient with a type I Chiari malformation, the authors observed the following symmetrical oculomotor phenomenon: (1) With gaze straight ahead, eye position was rather stable with some drift about the torsional axis. (2) With lateral gaze, nystagmus developed with extorsional quick phases of the abducting, and intorsional quick phases of the adducting eye. (3) After returning to gaze straight ahead, there was rebound nystagmus with a torsional component in the opposite direction. The failure to keep the torsional eye position component constant independent of the actual direction of gaze and the preceding gaze displacement implies that the oculomotor output in this patient is violating Listing's law. Based on magnetic resonance imaging of the head, the authors hypothesize that important neural structures implementing Listing's law are localized in the caudal cerebellum or lower brainstem.