Smooth pursuit

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Predictive smooth pursuit for a sinusoidal target movement

In the scientific study of vision, smooth pursuit describes a type of eye movement in which the eyes remain fixated on a moving object. It is one of two ways that visual animals can voluntarily shift gaze, the other being saccadic eye movements. Pursuit differs from the vestibulo-ocular reflex, which only occurs during movements of the head and serves to stabilize gaze on a stationary object. Most people are unable to initiate pursuit without a moving visual signal. The pursuit of targets moving with velocities of greater than 30°/s tends to require catch-up saccades. Smooth pursuit is asymmetric: most humans and primates tend to be better at horizontal than vertical smooth pursuit, as defined by their ability to pursue smoothly without making catch-up saccades. Most humans are also better at downward than upward pursuit. [1] Pursuit is modified by ongoing visual feedback.

Contents

Measurement

There are two basic methods for recording smooth pursuit eye movements, and eye movement in general. The first is with a search coil. This technique is most common in primate research, and is extremely accurate. An eye movement shifts the orientation of the coil to induce an electric current, which is translated into horizontal and vertical eye position. The second technique is an eye tracker. This device, while somewhat more noisy, is non-invasive and is often used in human psychophysics and recently also in instructional psychology. It relies on the infrared illumination of the pupil to track eye position with a camera. [2]

During oculomotor experiments, it is often important to ensure that no saccades occurred when the subject was supposed to be smoothly pursuing a target. Such eye movements are called catch-up saccades and are more common when pursuing at high speeds. Researchers are able to discard portions of eye movement recordings that contain saccades, in order to analyze the two components separately. Saccadic eye movements differ from the smooth pursuit component by their very high initial acceleration and deceleration, and peak velocity. [3]

Neural circuitry

The neural circuitry underlying smooth pursuit is an object of debate. The first step towards the initiation of pursuit is to see a moving target. Signals from the retina ascend through the lateral geniculate nucleus and activate neurons in primary visual cortex. Primary visual cortex sends the information about the target to the middle temporal visual cortex, which responds very selectively to directions of movement. The processing of motion in this area is necessary for smooth pursuit responses. [4] This sensory area provides the motion signal, which may or may not be smoothly pursued. A region of cortex in the frontal lobe, known as the frontal pursuit area, responds to particular vectors of pursuit, and can be electrically stimulated to induce pursuit movements. [5] Recent evidence suggests that the superior colliculus also responds during smooth pursuit eye movement. [6] These two areas are likely involved in providing the "go"-signal to initiate pursuit, as well as selecting which target to track. The "go"-signal from the cortex and the superior colliculus is relayed to several pontine nuclei, including the dorsolateral pontine nuclei and the nucleus reticularis tegmenti pontis. [7] The neurons of the pons are tuned to eye velocity and are directionally selective, and can be stimulated to change the velocity of pursuit. The pontine nuclei project to the cerebellum, specifically the vermis and the paraflocculus. These neurons code for the target velocity and are responsible for the particular velocity profile of pursuit.[ citation needed ] The cerebellum, especially the vestibulo-cerebellum, is also involved in the online correction of velocity during pursuit. [8] The cerebellum then projects to optic motoneurons, which control the eye muscles and cause the eye to move.

Stages of smooth pursuit

Pursuit eye movement can be divided into two stages: open-loop pursuit and closed-loop pursuit. Open-loop pursuit is the visual system's first response to a moving object we want to track and typically lasts ~100 ms. Therefore, this stage is ballistic: Visual signals have not yet had time to correct the ongoing pursuit velocity or direction. [9] The second stage of pursuit, closed-loop pursuit, lasts until the pursuit movement has ceased. This stage is characterized by the online correction of pursuit velocity to compensate for retinal slip. In other words, the pursuit system tries to null retinal velocity of the object of interest. This is achieved at the end of the open-loop phase. In the closed-loop phase, the eye angular velocity and target angular velocity are nearly equal.

Smooth pursuit and spatial attention

Various lines of research suggests a tight coupling for closed loop pursuit and spatial attention. For instance, during the close loop phase selective attention is coupled to the pursuit target such that untracked targets which move in the same direction with the target are poorly processed by the visual system. [10] Recently, a loose coupling of open loop pursuit and attention was suggested, when there is only one possible moving target. [11] This difference between pursuit and saccades may be accounted for by the differences in latency. Pursuit eye movements are initiated within 90-150 ms, while typical latencies for voluntary saccades are in the order of 200-250 ms [12]

Smooth pursuit in the absence of a visual target

Performing smooth pursuit without a moving visual stimulus is difficult, [13] and typically results in a series of saccades. However, pursuit without a visible target is possible under some particular conditions, that show the importance of high-level functions in smooth pursuit maintenance.

If you know which way a target will move, or know the target trajectory (because it is periodic for instance), you can initiate pursuit before the target motion actually starts, especially if you know exactly when the motion will start. [12] [14] It is also possible to maintain pursuit if a target momentarily disappears, especially if the target appears to be occluded by a larger object. [14]

Under conditions in which there is no visual stimulation (in total darkness), we can still perform smooth pursuit eye movements with the help of a proprioceptive motion signal (e.g. your moving finger). [15]

Following stimuli from peripheral gaze

When a bright light appears in the periphery, the fastest it can achieve a smooth pursuit is 30°/second. It first fixes the gaze to the peripheral light, and if not in excess of 30°/second, will follow the target equally with the movement. At higher velocities, the eye will not move smoothly, and requires corrective saccades. Unlike saccades, this process uses a continuous feedback system, which is based strictly on error. [16]

Distinction between smooth pursuit, optokinetic nystagmus, and ocular following response

Although we can clearly separate smooth pursuit from the vestibulo-ocular reflex, we can not always draw a clear separation between smooth pursuit and other tracking eye movements like the slow phase of the optokinetic nystagmus and the ocular following response (OFR), discovered in 1986 by Miles, Kawano, and Optican, [17] which is a transient ocular tracking response to full-field motion. The latter are both slow eye movements in response to extended targets, with the purpose of stabilizing the image. Therefore, some processing stages are shared with the smooth pursuit system. [18] Those different kinds of eye movements may not be simply differentiated by the stimulus that is appropriate to generate them, as smooth pursuit eye movements can be generated to track extended targets as well. The main difference may lie in the voluntary nature of pursuit eye movements. [19]

Smooth-pursuit deficits

Smooth pursuit requires the coordination of many brain regions that are far away from each other. This makes it particularly susceptible to impairment from a variety of disorders and conditions.[ citation needed ]

Schizophrenia

There is significant evidence that smooth pursuit is deficient in people with schizophrenia and their relatives. People with schizophrenia tend to have trouble pursuing very fast targets. This impairment is correlated with less activation in areas known to play a role in pursuit, such as the frontal eye field. [20] However, other studies have shown that people with schizophrenia show relatively normal pursuit, compared to controls, when tracking objects that move unexpectedly. The greatest deficits are when the patients track objects of a predictable velocity which begin moving at a predictable time. [21] This study speculates that smooth pursuit deficits in schizophrenia are a function of the patients' inability to store motion vectors.

Autism

People with autism show a plethora of visual deficits. One such deficit is to smooth pursuit. Children with autism show reduced velocity of smooth pursuit compared to controls during ongoing tracking. [22] However, the latency of the pursuit response is similar to controls. This deficit appears to only emerge after middle adolescence.

Trauma

People with post traumatic stress disorder, with secondary psychotic symptoms, show pursuit deficits. [23] These patients tend to have trouble maintaining pursuit velocity above 30 degree/second. A correlation has also been found between performance on tracking tasks and a childhood history of physical and emotional abuse. [24]

Drugs and Alcohol

"Lack of Smooth Pursuit" is a scorable clue on the NHTSA's standardized field sobriety tests. The clue, in combination with others, may be used to determine if a person is impaired by alcohol and/or drugs. Drugs causing lack of smooth pursuit include depressants, some inhalants, and dissociative anesthetics (such as phencyclidine or ketamine).[ citation needed ]

Preterm Birth

Children born very preterm show smooth pursuit deficits compared to paired controls born at full term. [25] This delay in smooth pursuit has also been linked to later neurodevelopment in toddlerhood in children born very preterm. [26]

See also

Related Research Articles

<span class="mw-page-title-main">Saccade</span> Eye movement

A saccade is a quick, simultaneous movement of both eyes between two or more phases of focal points in the same direction. In contrast, in smooth-pursuit movements, the eyes move smoothly instead of in jumps; it could be associated with a shift in frequency of an emitted signal or a movement of a body part or device. Controlled cortically by the frontal eye fields (FEF), or subcortically by the superior colliculus, saccades serve as a mechanism for focal points, rapid eye movement, and the fast phase of optokinetic nystagmus. The word appears to have been coined in the 1880s by French ophthalmologist Émile Javal, who used a mirror on one side of a page to observe eye movement in silent reading, and found that it involves a succession of discontinuous individual movements.

Saccadic masking, also known as (visual) saccadic suppression, is the phenomenon in visual perception where the brain selectively blocks visual processing during eye movements in such a way that neither the motion of the eye nor the gap in visual perception is noticeable to the viewer.

<span class="mw-page-title-main">Vestibulo–ocular reflex</span> Reflex where rotation of the head causes eye movement to stabilize vision

The vestibulo-ocular reflex (VOR) is a reflex that acts to stabilize gaze during head movement, with eye movement due to activation of the vestibular system, it is also known as the Cervico-ocular reflex. The reflex acts to stabilize images on the retinas of the eye during head movement. Gaze is held steadily on a location by producing eye movements in the direction opposite that of head movement. For example, when the head moves to the right, the eyes move to the left, meaning the image a person sees stays the same even though the head has turned. Since slight head movement is present all the time, VOR is necessary for stabilizing vision: people with an impaired reflex find it difficult to read using print, because the eyes do not stabilise during small head tremors, and also because damage to reflex can cause nystagmus.

<span class="mw-page-title-main">Superior colliculus</span> Structure in the midbrain

In neuroanatomy, the superior colliculus is a structure lying on the roof of the mammalian midbrain. In non-mammalian vertebrates, the homologous structure is known as the optic tectum or optic lobe. The adjective form tectal is commonly used for both structures.

<span class="mw-page-title-main">Eye movement</span> Movement of the eyes

Eye movement includes the voluntary or involuntary movement of the eyes. Eye movements are used by a number of organisms to fixate, inspect and track visual objects of interests. A special type of eye movement, rapid eye movement, occurs during REM sleep.

Oscillopsia is a visual disturbance in which objects in the visual field appear to oscillate. The severity of the effect may range from a mild blurring to rapid and periodic jumping. Oscillopsia is an incapacitating condition experienced by many patients with neurological disorders. It may be the result of ocular instability occurring after the oculomotor system is affected, no longer holding images steady on the retina. A change in the magnitude of the vestibulo-ocular reflex due to vestibular disease can also lead to oscillopsia during rapid head movements. Oscillopsia may also be caused by involuntary eye movements such as nystagmus, or impaired coordination in the visual cortex and is one of the symptoms of superior canal dehiscence syndrome. Those affected may experience dizziness and nausea. Oscillopsia can also be used as a quantitative test to document aminoglycoside toxicity. Permanent oscillopsia can arise from an impairment of the ocular system that serves to maintain ocular stability. Paroxysmal oscillopsia can be due to an abnormal hyperactivity in the peripheral ocular or vestibular system.

The pars reticulata (SNpr) is a portion of the substantia nigra and is located lateral to the pars compacta. Most of the neurons that project out of the pars reticulata are inhibitory GABAergic neurons.

Dysmetria is a lack of coordination of movement typified by the undershoot or overshoot of intended position with the hand, arm, leg, or eye. It is a type of ataxia. It can also include an inability to judge distance or scale.

Microsaccades are a kind of fixational eye movement. They are small, jerk-like, involuntary eye movements, similar to miniature versions of voluntary saccades. They typically occur during prolonged visual fixation, not only in humans, but also in animals with foveal vision. Microsaccade amplitudes vary from 2 to 120 arcminutes. The first empirical evidence for their existence was provided by Robert Darwin, the father of Charles Darwin.

<span class="mw-page-title-main">Frontal eye fields</span> Region of the frontal cortex of the brain

The frontal eye fields (FEF) are a region located in the frontal cortex, more specifically in Brodmann area 8 or BA8, of the primate brain. In humans, it can be more accurately said to lie in a region around the intersection of the middle frontal gyrus with the precentral gyrus, consisting of a frontal and parietal portion. The FEF is responsible for saccadic eye movements for the purpose of visual field perception and awareness, as well as for voluntary eye movement. The FEF communicates with extraocular muscles indirectly via the paramedian pontine reticular formation. Destruction of the FEF causes deviation of the eyes to the ipsilateral side.

<span class="mw-page-title-main">Supplementary eye field</span> Region of the frontal cortex of the brain

Supplementary eye field (SEF) is the name for the anatomical area of the dorsal medial frontal lobe of the primate cerebral cortex that is indirectly involved in the control of saccadic eye movements. Evidence for a supplementary eye field was first shown by Schlag, and Schlag-Rey. Current research strives to explore the SEF's contribution to visual search and its role in visual salience. The SEF constitutes together with the frontal eye fields (FEF), the intraparietal sulcus (IPS), and the superior colliculus (SC) one of the most important brain areas involved in the generation and control of eye movements, particularly in the direction contralateral to their location. Its precise function is not yet fully known. Neural recordings in the SEF show signals related to both vision and saccades somewhat like the frontal eye fields and superior colliculus, but currently most investigators think that the SEF has a special role in high level aspects of saccade control, like complex spatial transformations, learned transformations, and executive cognitive functions.

<span class="mw-page-title-main">Fixation (visual)</span> Maintaining ones gaze on a single location

Fixation or visual fixation is the maintaining of the gaze on a single location. An animal can exhibit visual fixation if it possess a fovea in the anatomy of their eye. The fovea is typically located at the center of the retina and is the point of clearest vision. The species in which fixational eye movement has been verified thus far include humans, primates, cats, rabbits, turtles, salamanders, and owls. Regular eye movement alternates between saccades and visual fixations, the notable exception being in smooth pursuit, controlled by a different neural substrate that appears to have developed for hunting prey. The term "fixation" can either be used to refer to the point in time and space of focus or the act of fixating. Fixation, in the act of fixating, is the point between any two saccades, during which the eyes are relatively stationary and virtually all visual input occurs. In the absence of retinal jitter, a laboratory condition known as retinal stabilization, perceptions tend to rapidly pass away. To maintain visibility, the nervous system carries out a procedure called fixational eye movement, which continuously stimulates neurons in the early visual areas of the brain responding to transient stimuli. There are three categories of fixational eye movement: microsaccades, ocular drifts, and ocular microtremor. At small amplitudes the boundaries between categories become unclear, particularly between drift and tremor.

Within computer technology, the gaze-contingency paradigm is a general term for techniques allowing a computer screen display to change in function depending on where the viewer is looking. Gaze-contingent techniques are part of the eye movement field of study in psychology.

Eye–hand coordination is the coordinated motor control of eye movement with hand movement and the processing of visual input to guide reaching and grasping along with the use of proprioception of the hands to guide the eyes, a modality of multisensory integration. Eye–hand coordination has been studied in activities as diverse as the movement of solid objects such as wooden blocks, archery, sporting performance, music reading, computer gaming, copy-typing, and even tea-making. It is part of the mechanisms of performing everyday tasks; in its absence, most people would not be able to carry out even the simplest of actions such as picking up a book from a table.

Listing's law, named after German mathematician Johann Benedict Listing (1808–1882), describes the three-dimensional orientation of the eye and its axes of rotation. Listing's law has been shown to hold when the head is stationary and upright and gaze is directed toward far targets, i.e., when the eyes are either fixating, making saccades, or pursuing moving visual targets.

<span class="mw-page-title-main">Visual processing abnormalities in schizophrenia</span>

Visual processing abnormalities in schizophrenia are commonly found, and contribute to poor social function.

The anti-saccade (AS) task is a way of measuring how well the frontal lobe of the brain can control the reflexive saccade, or eye movement. Saccadic eye movement is primarily controlled by the frontal cortex.

<span class="mw-page-title-main">Doug Crawford</span> Canadian neuroscientist

John Douglas (Doug) Crawford is a Canadian neuroscientist and the Scientific Director of the Connected Minds program. He is a professor at York University where he holds the York Research Chair in Visuomotor Neuroscience and the title of Distinguished Research Professor in Neuroscience.

<span class="mw-page-title-main">Peter Schiller (neuroscientist)</span> German-born neuroscientist (born 1931)

Peter H. Schiller was a German-born neuroscientist. At the time of his death, he was a professor emeritus of Neuroscience in the Department of Brain and Cognitive Sciences at the Massachusetts Institute of Technology (MIT). Schiller is well known for his work on the behavioral, neurophysiological and pharmacological studies of the primate visual and oculomotor systems.

The tectopulvinar pathway and the geniculostriate pathway are the two visual pathways that travel from the retina to the early visual cortical areas. From the optic tract, the tectopulvinar pathway sends neuronal radiations to the superior colliculus in the tectum, then to the lateral posterior-pulvinar thalamic complex. Approximately 10% of retinal ganglion cells project onto the tectopulvinar pathway.

References

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