Introductory
We live in a world in which we are always on the move. Our environment itself is continually changing as well. To avoid living in a blurry world, smooth pursuit helps us keep up with the movement of objects. For most of the population, a dynamic visual stimulus is needed to perform smooth pursuit. When watching an object we have a conjugated fix on the object, and it is projected on the fovea to increase the visual clarity of the object. This placement of the object on the retina triggers pathways that will carry the visual information to integration centers. This is the reason why most need visual stimuli to perform smooth pursuit, because without an object one would most likely perform a saccadic eye movement. [3] An object falling off the retina, called a retinal slip, confirms that the object is indeed moving. If one’s interest is to follow the movement of the object, they would have to move their eyes at the same velocity as the moving object to keep track of it. Normally our VOR would enforce eye movement in the opposite direction of head turning in attempts to help maintain gaze. [15] Thankfully, the smooth pursuit systems inhibit VOR components, which allows the head to turn in the same direction as the eyes, which aid in tracking the moving object. Due to the fact that that one can choose whether to track the movement of an object it is called a voluntary eye movement.

Anatomy review
  • Retina: A layer in the back of the eye that is sensitive to light and color. It has two types of photoreceptors. These types are rods, which are found in the periphery, and cones, which are found in the center of the retina. Rods are light sensitive but do not pick up color. They are most helpful to see in the dark because of their light sensitivity, but have low resolution. Cones are color sensitive, and thus have high resolution. They are the only photoreceptor type found in the fovea. The fovea is located at the center of the retina and is the place of highest visual acuity. [5]

  • Occipital eye field: A physical area of the cerebral cortex. It can also be called Brodmann’s area 18. This motor area deals with control of voluntary and involuntary movement of the eye muscles. [1][6]

  • Frontal eye fields: An area in the frontal cortex. When stimulated the FEF creates eye movements. This area has motor and visual cells, which make the FEF an important integrating site.[7] The ventral region is most important in smooth pursuit because it affects motion-induced acceleration, anticipatory initiation, and predictive continuation of the trajectory of the moving object. [8]

  • Pontine nuclei: The gray matter that has many nuclei in the pons. The corticobulbar, corticospinal, and corticopontine tracts that cross through the pontine nuclei. [11][14]

  • Cerebellum: Sits at the back of the head behind the 4th ventricle where the brainstem and spinal cord meet. Information from sensory systems, motor systems and the spinal cord travel in and out through the peduncles. The cerebellum plays a major role in balance, coordination, motor activity, and spatial temporal coordination. [13]

  • Flocculus: A small lobe of the cerebellum located posterior to the middle cerebellar peduncle. The flocculus and the nodulus work together to form the vestibular part of the cerebellum. It is involved in the processing difference between the eye velocity and the head velocity. It becomes crucial in calculating the smooth pursuit gain and calculating information to perform a saccade. [9]

  • CN III: Oculomotor nerve. It innervates extraocular muscles that move the top eyelid (levator palpabrae superioris, superior tarsal muscle) and muscles that move the eyeball (superior rectus, inferior rectus, medial rectus, inferior oblique). [10]

  • CN V1: Abducens nerve. It innervates the lateral rectus muscle of the eye allowing the eye to move outward. [10]

  • PPRF: Paramedian pontine reticular formation. It is a collection of cells in the pons next to the abducens nerve’s nucleus. It helps in coordinating eye movements like saccades and smooth pursuit. [12]

  • MLF: Medial Longitudinal Fasciculus. Located in the brainstem and made up of ascending and descending fibers. It links the oculomotor, trochlear and abducens nerves and vestibulocochlear nerve. It processes information of the eye and head movements. Its influence allows the eye to follow an object and then return back to the initial position. [12

Visual aids
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Neuronal connections [1][2][15]
  1. 1. Retinal slip will be detected by the MST (medial superior temporal region that detects motion) and MT (middle temporal region that detects direction of motion). These regions are located in the occipital eye fields and are part of the dorsal stream. After a period of latency, the MT and MST neurons start firing once the stimulus comes into the visual field. They track the motion by calculating the average velocity vectors. Although they often work together, the MT and MST regions do have separate roles in pursuit. MT is utilized in the initiation of smooth pursuit while MST is utilized in the maintenance of tracking.
  2. 2. After the visual information reaches the MT/MST regions, it can ipsilaterally travel to the dorsal pontine nuclei directly or indirectly. The direct pathway goes straight from MT/MST to the pontine nuclei, while the indirect pathway goes through the frontal eye fields.
  3. 3. The frontal eye field (FEF) neurons are very motion direction specific even before pursuit begins, and they play a role in the initiation and maintenance of pursuit. Input coming into the FEF comes from the principle sulcus region, lateral intraparietal area, supplementary eye fields, and the MST region.
  4. 4. All information that goes to the cerebellum travels via the pons. In this case, information goes through the dorsolateral pontine nucleus (DLPS) which has a vast receptive field and is direction and velocity specific. It responds best to large visual stimuli, but also responds to small stimuli as well.
  5. 5. When the information reaches the cerebellum, it goes to both the ventral paraflocculus (VPF) and the cerebellar flocculus. Stimulating the VPF has a quick response in performing smooth eye movements. Their firing rates are analogous to the eye speed. Since the CPF now knows the motor command going out, it is now able to adjust eye speed as part of a positive-feedback system. The cerebellar flocculus has ipsilateral connections of the vestibulo-ocular system. The vestibular nerve terminates in the cerebellar flocculus as well as its own vestibular nucleus. The flocculus assesses the output motor nuclei for the eye muscles, in this case it travels contralaterally to the abducens (CN VI).
  6. 6. When the Abducens nuclei is activated it contracts the lateral rectus. We do that by an excitatory burst neuron, which is located in horizontal gaze center called the Paramedian pontine reticular formation. (PPRF)
  7. 7. The abducens has an interneuron that travels in the medial longitudinal fasciculus (MLF), exciting the contralateral occulomotor nuclei activating CN III, which contracts the medial rectus of contralateral eye and lateral rectus of ipsilateral eye, which results in conjugate gaze.
  8. 8. The PPRF sends inhibitory signals through inhibitory burst neurons to the contralateral abducens. It will inhibit the contralateral lateral rectus and the ipsilateral medial rectus so you don’t have co-contraction while trying to hold eyes stable.

Smooth pursuit in detail
Since one needs a visual stimulus to perform smooth pursuit, it is obvious that motor-visual processing is necessary for smooth pursuit. There are three phases in smooth pursuit. Phase I comprises of saccading in the same direction of the object to catch it and place it on the fovea. There is a 80-110 ms latency period between the acknowledgement of the stimulus entering the visual fields and the activation of the pursuit systems. This phase also isn’t too concerned with the specifics of the moving object, like the object’s velocity, contrasts of color, or texture. [15] Phase II, also named the open-loop period, is compromised of a saccade due to the latency in phase I helping the eyes catch up to the velocity of the object in a period of 200-300 ms. [4] Due to visual feedback, the system is highly specific about the information that it picks up from the object. The system is working hard to decrease the difference between the movement happening on the retina and the motor commands that drive eye movement. The challenge to minimize the difference in velocity between the afferent and efferent signals helps the eye, tracking the velocity of the eye to match the velocity of the object. If these velocities are matched, the object will stay on the fovea, thereby decreasing retinal slip, which is preferred for visual acuity. This is all taking place in real time. The visual system is seeing the deceleration as it is taking place, and commands the eye muscles, within milliseconds, to adjust. Your eyes will move as quickly as they’re being innervated. This ratio of eye and object velocity is called pursuit gain. Pursuit gain is equal to angular velocity of the eye divided by the angular velocity of the object. The goal is to get this ratio to be 1. If it isn’t, the eyes will compensate by saccading in either direction, depending if the eye is moving too slow or fast. Phase III, also named the closed loop period, is comprised of the eye keeping a constant velocity while tracking the object. The target remains on the fovea and therefore retinal slip is none. [15]

Summary
The ability to perform smooth pursuit is important to keep up with our dynamic environment. To perform pursuit, a visual stimulus is required to activate the initiation of systems that guide the movement. Once stimulus is acknowledged, the eyes work hard to focus the object on the fovea with a conjugate fix. Then the system has to adjust if the object moves faster or slower than the eye. This is detected by a retinal slip. The goal is for the eye movement velocity to match the velocity of the moving object. This matching causes the pursuit to be smooth and uninterrupted.

Glossary of terms:
  • VOR: Vestibular ocular reflex is used to keep the eyes in place when the head moves. It is inhibited in smooth pursuit. [1]
  • MT/MST: Middle temporal and medial superior temporal areas. They are located in the superior temporal sulcus. They have a visual and motor affect needed for smooth pursuit. [2]
  • Ipsilateral: Staying on the same side, not decussating.
  • Contralateral: Crossing midline and decussating
  • SEF: supplementary eye fields are located in the supplementary motor areas. It does not have a direct role in smooth pursuit however it helps in eye velocity when smooth pursuit is being initiated. The influence of the SEF adds to the latency in performing saccades to catch the object on the fovea. [2]
  • LIP: Lateral intraparietal area. It is stimulated in both smooth pursuit and saccades. Only some of its neurons are direction specific. They seem to be more concerned with how the spatial processing and representation affects the rest of the body (limbs) affected by the movement. [2]
  • Burst neuron: This burst neuron is responsible for producing the pulse/velocity needed to move the eye.
  • Interneuron: a neuron that is located between the primary afferent neuron and the efferent motor neuron.

Further Readings

  • https://www.youtube.com/watch?v=R-57vDBi55E
    • A video of someone performing smooth pursuit being explained by her doctor. He explains how tests are conducted made to check for normal performance.

  • Signal Processing and Distribution in Cortical-Brainstem Pathways for Smooth Pursuit Eye Movements Article written by Mustari, Ono, and Das.
    • It has helpful flow charts of the pathways in smooth pursuit with explanations.


Quiz questions
What is the function of the trochlear nerve?
a. somatic sensory
b. somatic motor
c. visceral motor
d. visceral sensory
e. A and B

Which muscle does the occulomotor nerve not innervate?
a. Lateral rectus
b. Superior rectus
c. Inferior oblique
d. Medial rectus
e. More that one muscle is not innervated by the occulomotor nerve

What does PPRF stand for?
a. parietal pontine rednuclear fasciculus
b. Paralateral parietal reticular formation
c. Paramdeian pontine reticular formation
d. paramedian pedunculopontine regional fibers

What brain region/structure detects retinal slip?
a. Basal ganglia
b. MT/MST
c. Optic chiasm
d. Frontal Eye fields
e. C and D

What muscles does the oculomotor cranial nerve contract?
a. Lateral rectus of ipsilateral eye and medial rectus of contralateral eye
b. Lateral rectus of contralateral eye and medial rectus of ipsilateral eye
c. Medial rectus of contralateral eye and lateral rectus of ipsilateral eye
d. medial rectus of ipsilateral eye and lateral rectus of ipsilateral eye
e. There is more than one answer

True/ False
Smooth pursuit require conjugate fixation on the moving object. T/F
To perform smooth pursuit, the VOR is activated. T/F
In phase III retinal slip decreases. T/F
One can activate smooth pursuit systems by imagining a moving object. T/F
When tracking an object, it is projected on the peripheral retina. T/F/

Short Answer:
What are the characteristics that define the phases in performing smooth pursuit?
Name and describe the roles of the cranial nerves activated that enable smooth pursuit.
Write out the equation that defines pursuit gain. Explain what the ideal ratio would be and why.

Essay:
Describe the pathways that are activated when a stimulus with velocity comes into the visual field in smooth pursuit that are not activated without a physical stimulus.

References:
1. https://www.dartmouth.edu/~rswenson/NeuroSci/chapter_8D.html#Tracking

2. http://jn.physiology.org/content/91/2/591.full

3. https://www.ncbi.nlm.nih.gov/books/NBK10991/

4.http://www.ski.org/sites/default/files/publications/1991_keller_heinen_neurosci_res.pdf

5. http://hyperphysics.phy-astr.gsu.edu/hbase/vision/retina.html

6. http://braininfo.rprc.washington.edu/centraldirectory.aspx?ID=1544

7. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4141567/

8. https://www.ncbi.nlm.nih.gov/pubmed/1822728/

9. http://www.gregdetre.co.uk/notes/neuro_generals/cerebellar%20flocculus.html

10. http://www.medicinenet.com/script/main/art.asp?articlekey=7610

11.http://www.sciencedirect.com/topics/page/Paramedian_pontine_reticular_formation

12. http://www.sciencedirect.com/topics/page/Medial_longitudinal_fasciculus

13. http://www.healthline.com/human-body-maps/cerebellum

14. http://www.medilexicon.com/dictionary/61642

15. Wolf, C. (2015). Audio-Visual Integration in Smooth Pursuit Eye Movements. doi:10.1007/978-3-658-08311-3
pictures:

Picture references
http://2.bp.blogspot.com/-lO9JkoIE1Kk/VLBAX8LhvtI/AAAAAAAAC9I/aBbvDG_4x_c/s1600/Eye%20Rods%20and%20Cones.gif

https://www.dartmouth.edu/~rswenson/NeuroSci/figures/Figure_30.htm

http://jn.physiology.org/content/91/2/591.full

http://1.bp.blogspot.com/-lnysLuMoj6M/Trlya-w6rUI/AAAAAAAAEFM/By2siExgihw/s640/voulantary+horizontal+conjugate+gaze.png

Quiz Answers
Multiple choice: BACB
T/F: TFTFF