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Smooth pursuit eye movements

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Pursuit movement is the ability of the eyes to smoothly follow 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 find pursuit extremely difficult, if not impossible, to initiate without a moving visual signal.


Measurement

There are two basic methods for recording smooth pursuit eye movements, and eye movements in general. The first is with a search coil. This technique is most common in primate research, and is extremely accurate. Eye movements shift the orientation of the coil to induce an electrical 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. It relies on the infrared illumination of the pupil to track eye position with a camera.

During oculomotor experiemnts, it is often important to ensure that no saccades occurred when the subject was supposed to be smoothly pursuing a target. Such mistakes are called catch-up saccades and are more common when pursuing at high speeds. Tools are available which allow researchers to look at traces of eye movement and discard sections of the data that contain saccades, which differ qualitatively from smooth pursuit because of their very high acceleration and decceleration.

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[1] 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[2]. Recent evidence suggests that the superior colliculus also responds during smooth pursuit eye movements[3]. 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 nucli and the nucleus reticularis tegmenti pontis[4] 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[5]. The cerebellum, especially the vestibulo-cerebellum, is also involved in the online correction of velocity during pursuit.[6]. The cerebellum then projects to optic motoneurons, which control the eye muscles and cause the eye to move.

Stages of Smooth Pursuit

Pursuit eye movements 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 it wishes to track and typically lasts ~100ms. This stage of pursuit is ballistic in the sense that visual signals have not yet had time to travel through the visual system and correct the ongoing pursuit velocity[7]. The second stage of pursuit is called closed-loop pursuit. This stage lasts from 100ms after the initiation of pursuit 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, if you are trying to pursue a target, but that target is getting farther and farther away from your fovea, during closed loop pursuit you will increase the gain of pursuit until you stabilize the image.

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

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.[8] Recently, a loose coupling of open loop pursuit and attention was suggested, when there is only one possible moving target.[9] 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 [10]

Smooth pursuit in the absence of a visual target

Performing smooth pursuit without a moving visual stimulus is difficult,[11] 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.[10][12] It is also possible to maintain pursuit if a target momentarily disappears, especially if the target appears to be occluded by a larger object.[12] 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).[13]

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.[14]

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), recently discovered by Miles, Kawano and Optican,[15] 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.[16] 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.[17]


Smooth Pursuit Deficits

Schizophrenia

There is significant evidence that smooth pursuit is deficient in schizophrenic patients and their relatives. Schizophrenic patients 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 [18] However, other studies have shown that schizophrenic patients 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. [19] This study speculates that smooth pursuit deficits in schizophrenia are a function of the patients' inability to store motion vectors.

Autism

Autistic patients 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 [20] However, the latency of the pursuit response is similar to controls. This deficit appears to only emerge after middle adolescence.

Trauma

Patients with post traumatic stress disorder, with secondary psychotic symptoms, show pursuit deficits[21]. These patients tend to have trouble maintaining pursuit velocity above 30 degrees/second. A correlation has also been found between performance on tracking tasks and a childhood history of physical and emotional abuse[22].

Smooth Pursuit Trivia

  • Smooth pursuit is asymmetric- most people and primates tend to be much better at horizontal smooth pursuit than vertical smooth pursuit, as defined by their ability to pursue smoothly without making catch-up saccades. Most people are also better at downward pursuit than upward pursuit.[23]
  • Usually, pursuit is impossible without a moving target[24]. But there are a few exceptions:
    • It is possible to pursue an imaginary target (eg. your moving finger) in total darkness. [25]
    • It is possible to maintain pursuit even if a target momentarily disappears, especially if the target appears to be occluded by a larger object. [26]
    • If you know which way a target will move, or how quickly it will move, you can initiate pursuit before the movement actually begins, especially if you know exactly when the motion will start.[27]
  • Latencies for smooth pursuit are actually faster than latencies for saccades.[28]

See also

References

Notes

  1. Newsome WT, Wurtz RH, Dursteler MR, Mikami A. Deficits in visual motion processing following ibotenic acid lesions of the middle temporal visual area of the macaque monkey. J Neurosci. 1985 Mar;5(3):825-40. PMID 3973698.
  2. Tian JR, Lynch JC. Corticocortical input to the smooth and saccadic eye movement subregions of the frontal eye field in Cebus monkeys. J Neurophysiology 1996 Oct;76(4):2754-71.PMID 8899643
  3. Krauzlis RJ. Neuronal activity in the rostral superior colliculus related to the initiation of pursuit and saccadic eye movements. J Neuroscience 2003 May 15;23(10):4333-44.PMID 12764122
  4. Leigh, RJ., Zee, DS. The Neurology of Eye Movements. Pages 209-211. Oxford University Press, 4th Edition
  5. ibid page 211
  6. Coltz JD, Johnson MT, Ebner TJ. Population code for tracking velocity based on cerebellar Purkinje cell simple spike firing in monkeys. Neurosci Lett. 2000 Dec 15;296(1):1-4. PMID 11099819
  7. Krauzlis RJ, Lisberger SG. Temporal properties of visual motion signals for the initiation of smooth pursuit eye movements in monkeys. J Neurophysiol. 1994 Jul;72(1):150-62. PMID 7965001
  8. Khurana, B., & Kowler, E. (1987). Shared attentional control of smooth eye movement and perception. Vision Research, 27, 1603–1618.
  9. Souto, D., & Kerzel, D. (2008). Dynamics of attention during the initiation of smooth pursuit eye movements. Journal of Vision, 8(14):3, 1-16, http://journalofvision.org/8/14/3/, DOI:10.1167/8.14.3 .
  10. 10.0 10.1 Joiner WM., Shelhamer M. Pursuit and saccadic tracking exhibit a similar dependence on movement preparation time. Exp Brain Research 2006 Sep;173(4):572-86 PMID 16550393
  11. Krauzlis, RJ. The control of voluntary eye movements: new perspectives. The Neuroscientist. 2005 Apr;11(2):124-37. PMID 15746381
  12. 12.0 12.1 Barnes GR. Cognitive processes involved in smooth pursuit eye movements.Brain Cogn. 2008 Dec;68(3):309-26.PMID 18848744
  13. Berryhill ME, Chiu T, Hughes HC. Smooth pursuit of nonvisual motion. J Neurophysiology 2006 Jul;96(1):461-5. PMID 16672304
  14. "Sensory Reception: Human Vision: Structure and function of the Human Eye" vol. 27, p. 179 Encyclopaedia Britannica, 1987
  15. Miles, F. A., Kawano, K. & Optican, L. M. Short-latency ocular following responses of monkey. I. Dependence on temporospatial properties of visual input. J Neurophysiol 56, 1321-1354 (1986).PMID 3794772
  16. 1 Ilg, U. J. Slow eye movements. Prog Neurobiol 53, 293-329, doi:S0301-0082(97)00039-7 [pii] (1997). PMID 9364615
  17. Krauzlis, RJ. Recasting the Smooth Pursuit Eye Movement System. Journal of Neurophysiology. 2004 Apr;J Neurophysiol 91: 591-603. PMID 14762145
  18. Hong LE, Tagamets M, Avila M, Wonodi I, Holcomb H, Thaker GK. Specific motion processing pathway deficit during eye tracking in schizophrenia: a performance-matched functional magnetic resonance imaging study. Biol Psychiatry 2005 Apr 1;57(7):726-32. PMID 15820229
  19. Avila MT, Hong LE, Moates A, Turano KA, Thaker GK. Role of anticipation in schizophrenia-related pursuit initiation deficits.J Neurophysiology 2006 Feb;95(2):593-601. PMID 16267121
  20. Takarae Y, Minshew NJ, Luna B, Krisky CM, Sweeney JA. Pursuit eye movement deficits in autism. Brain. 2004 Dec;127. PMID 15509622
  21. Cerbone A, Sautter FJ, Manguno-Mire G, Evans WE, Tomlin H, Schwartz B, Myers L. Differences in smooth pursuit eye movement between posttraumatic stress disorder with secondary psychotic symptoms and schizophrenia. Schizophr Research 2003 Sep 1;63(1-2):59-62. PMID 12892858
  22. Irwin HJ, Green MJ, Marsh PJ.Dysfunction in smooth pursuit eye movements and history of childhood trauma.Percept Mot Skills. 1999 Dec;89(3 Pt 2):1230-6. PMID 10710773
  23. Grasse KL, Lisberger SG. Analysis of a naturally occurring asymmetry in vertical smooth pursuit eye movements in a monkey. J Neurophysiology 1992 Jan;67(1):164-79. PMID 1552317
  24. Krauzlis, RJ. The control of voluntary eye movements: new perspectives. The Neuroscientist. 2005 Apr;11(2):124-37. PMID 15746381
  25. Berryhill ME, Chiu T, Hughes HC. Smooth pursuit of nonvisual motion. J Neurophysiology 2006 Jul;96(1):461-5. PMID 16672304
  26. Bennet SJ., Barnes, GR. Predictive smooth ocular pursuit during the transient disappearance of a visual target. J Neurophysiol. 2004 Jul;92(1):578-90. PMID 14960562
  27. Joiner WM., Shelhamer M. Pursuit and saccadic tracking exhibit a similar dependence on movement preparation time. Exp Brain Research 2006 Sep;173(4):572-86 PMID 16550393
  28. Krauzlis, RJ., Miles, FA. Release of fixation for pursuit and saccades in humans: Evidence for shared inputs acting on different neural substrates J. Neurophysiol., 76: 2822-2833, 1996 PMID 8985910
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