Physio C11 - Ocular Movements PDF

PHYSIO C11 – Ocular mouvements Eye movements are easier to study than movements of other parts of the body. This fact arises in part from the relative simplicity of muscle actions on the eyeball. There are only 6 extraocular muscles, each of which has a specific role in adjusting eye position. More...

PHYSIO C11 – Ocular mouvements Eye movements are easier to study than movements of other parts of the body. This fact arises in part from the relative simplicity of muscle actions on the eyeball. There are only 6 extraocular muscles, each of which has a specific role in adjusting eye position. Moreover, there is a limited set of stereotyped eye movements, and the central circuits governing each one are partially distinct. 1.​ Retinal stabilization The spatial resolution of the transduction system is limited by the resolution of the retinal photoreceptors mosaic. In fact, the retina is not homogenous. The visual acuity depends on the properties of the receptors, in terms of receptive fields, and also on the architecture of the connections between the receptors, the bipolar and ganglion cells. The portion of the retina with the highest resolution is the fovea. The fovea is the maximal acuity region of the retina because it has cones with tiny receptive fields and a very low/no degree of convergence from the receptors to the ganglion cells (in some portions of the fovea the correspondence between the receptor and the ganglion is 1:1). The acuity and the discrimination of two different stimuli applied in two different points of the retina is the highest in the fovea with respect to all the rest of the retina. Therefore, to have a very refined quality of information of the object of interest, it is necessary to focus it on the fovea. This means that the points created by the light, that compose the object, has to fall into the fovea (which is very tiny). Unfortunately, there are limitations: -​ Size of the fovea: the image of a big object cannot fully fall into the fovea since the size of the fovea creates a limitation. -​ Degrees of freedom of eye movements: it is necessary to adjust the movement of the eyes in respect to the movement of the body in order to avoid impairing the visual acuity. To compensate these limitation, retinal stabilization (reflexes that occur all the time involuntarily)occurs. Based on their aim, three types of stabilization movements can be classified: -​ gaze stabilization, -​ gaze shifting -​ vergence 2.​ Gaze stabilization (all animals) These are movements common to all animals with a retina and they have the aim to counteract the effect of self-motion on visual acuity (to avoid having a blurred vision). After self-motion is detected, the movement of the eyes is adjusted accordingly in order to compensate for the motion. In this way a stabilization occurs: gaze stabilization. The sensors that detect this process are located in two systems that already monitor the self-motion and the reflexes produced are: the vestibulo-ocular reflex (VOR) and the optokinetic reflex. The effect of these two reflexes is the same despite the source of information being different. The sensors detect the movements and, as a result, in the brainstem are generated signals to activate the extraocular muscles to counteract the self-movements. So, if a person is moving to one side, the eyes will move to the other side and the image will remain stable. These reflexes are active from the minimal velocity that can degrade the retinal acuity to the maximal velocity of self-motion that the animal can perform. VOR The action of vestibulo-ocular movements though the vestibulo-ocular reflex (VOR) can be appreciated by fixating an object and moving the head from side to side: the eyes automatically compensate for the head movement by moving the same distance and at the same velocity but in the opposite direction, thus keeping the image of the object at more or less the same place on the retina. The vestibular system detects brief, transient changes in head position and produces rapid, corrective eye movements. Sensory information from the semicircular canals directs the eyes to move in a direction opposite to the head movement. Although the vestibular system operates effectively to counteract rapid movements of the head, it is relatively insensitive to slow movements (below 1 Hz) or to persistent rotation of the head. For example, if the vestibulo-ocular reflex is tested with continuous rotation of an individual and without visual cues about the movement of the image (i.e., with eyes closed or in the dark), the compensatory eye movements cease after only about 30 seconds of rotation. However, if the same test is performed with visual cues, eye movements persist. Optokinetic reflex The compensatory eye movements in this case are due to the activation of another system that relies not on vestibular information, but on visual cues indicating motion of the visual field. This optokinetic system is especially sensitive to slow movements (below 1 Hz) of large areas of the visual field, and its response builds up slowly. These features complement the properties of the vestibulo-ocular reflex, especially as head movements slow down and vestibular signals decay. Thus, should a visual image slowly “slip” across the retina, the optokinetic system will respond by inducing compensatory movements of the eyes at the same speed and in the opposite direction. The optokinetic system can be tested by seating an individual in front of a screen on which a series of horizontally moving vertical bars is presented. The eyes automatically track the stripes until the eyes reach the end of their excursion. Then there is a quick saccade in the direction opposite to the movement, followed once again by smooth pursuit of the stripes. This alternation of slow and fast movement of the eyes in response to such stimuli is called optokinetic nystagmus. Optokinetic nystagmus is a normal reflexive response of the visual and oculomotor systems in response to large-scale movements of the visual scene and should not be confused with the pathological nystagmus that can result from certain kinds of brain injury (for example, damage to the vestibular system or the cerebellum)  These blurry images represent the optic flow experienced when looking out the window of a moving train or when walking forward (the eyes are not tuned for a system that moves at a higher speed than the one possible for humans). 3.​ Gaze shifting Gaze shifting is a feature that is seen only in animals with a retinal specialization (e.g., the fovea). This class of movement mechanism directs the highest point of resolution of the retina (fovea) to the object of interest and stabilizes it with regard to the stimulus. There is an activation of the extraocular muscles to move the eye to limit the velocity of the stimuli that moves across the retina. There are two classes of movements: -​ saccadic movements -​ pursuit movements. Saccadic movements are rapid, ballistic movements of the eyes that abruptly change the direction of fixation. They range in amplitude from the small movements made while reading to the much larger movements made while gazing around a room. They happen simultaneously in both eyes and people are not able to realize that they are performing them since they are very fast. If the ocular movements are analysed by an eye-tracker, when shifting the gaze from one point to another, it can be seen that in order to “explore” an object the eyes are moving very rapidly. Saccadic movements are in fact the ones that shift the gaze from one point to another in order to focus the different points on the fovea. They are “voluntarily” movements: the person wants to focus on an object and the brain and the eyes explore it in a fast way obtaining a stable image at the end. Pursuit movements are much slower tracking movements of the eyes designed to keep a moving stimulus on the fovea once foveation is achieved. Such movements are under voluntary control in the sense that the observer can choose whether or not to track a moving stimulus. They are instead are the movements of the eyes when following a moving object. In this case, the moving object is focused (in order to be tracked) and the background is stable. In pursuit movements the extraocular muscles are activated to move the eyes “voluntarily” (the person doesn’t realize it). 4.​ Vergence It is a feature unique to animals not only with a retinal specialization but also with binocular vision. In order to give the correct vision, both eyes need to work perfectly together (it is needed to get both foveae on the object of interest). This is easy when one is looking from a distance to the object but from a closer distance the angle gets larger. Vergence is in fact the movements that can change the angle of the line of gaze.  Vergence is the mechanism controlling the angle formed by the line of gaze of the two eyes to scrutinize a single target with both eyes (converge or diverge the line of gaze). In close vision, light, lens and vergence are important since the eyes are not completely superimposable in terms of visual fields. 5.​ Eye mouvements All the mechanisms aimed at retinal stabilization use a common set of motoneurons and common sets of target muscles to perform all the possible movements of the eye. Extraocular muscles are organized in 3 antagonistic pairs: ​ Medial rectus - lateral rectus ​ Superior rectus – Inferior rectus ​ Superior oblique – Inferior oblique There are 3 cranial nerves control the eye movement muscles: -​ Oculomotor (III) -​ Trochlear (IV) -​ Abducens (VI) The nuclei of the three nerves are distributed in the brainstem and are interconnected in a pathway called Medial Longitudinal Fasciculus that is important to move the eyes in a coherent way. The resting centric position is the equilibrium position of the system: the natural position the eye keeps without any effort when the muscles are not being used. The centric position is kept passively by the muscles: they act like a perfectly balanced system of springs that tends to draw the eye in a central position (the muscles are not contracting). In order to move, the eyes need to shift from the resting centric position to a non-centric position. This implies an effort since it is necessary to unbalance the system to overcome the passive resistance of the muscles that hold the eye in resting centric position. In this case, the muscles are contracting. There are two sets of forces that can be applied on the eyes: ​ Dynamic: transient force overcoming the resistance of the eye to motion (e.g., accelerating the eye). ​ Static: maintained force holding the eye in the new position (e.g., keeping the eye in stationary position). The rate of motoneuronal discharge correlates to the force needed: the force is related to the degree of distance in respect to the resting position. 6.​ VOR VOR is the neural system by which rotations of the head are detected using the semicircular canals of the vestibular organs. In this case the eyes are counter-rotated in the opposite direction in an equal amount to stabilize the line of sight. It is a reflex that is in constant use. The VOR is suppressed in an awake, healthy person (e.g., if a person wants to turn their head and turn their eyes in a particular direction). The VOR is a way to assess the integrity of the brainstem: it is possible to detect impairment in the cranial nerves. To assess the reflex, the patient has to focus on a point and then the doctor moves their head quickly in order not to have saccades but the reflex. The image will never be blurry because there’s a perfect compensation. The VOR is also observed when tilting the head. The information comes from the semicircular canals, reaching the vestibular nuclei and then communicating to the oculomotor nuclei (3rd, 4th, 6th cranial nerve). A bilateral control on both eyes is needed to have a consensual movement and this is helped by the fact that the labyrinth gives opposite information to the two sides (inhibition and excitation of the muscles depends on the 2 labyrinths).  7.​ Nystagmus The VOR is able to counteract rotations from 80 degrees to 180 degrees (it is not possible to rotate the eye 360 degrees because the eyeball has its own constraints). If a person tries to rotate the eyes to an angle that cannot be reached, the eyes will adjust themselves, resetting to a central position in the orbit. After the reset is complete the compensatory eye rotation resumes. This is called nystagmus. If the eyes are observed with an eye tracker, quick phases and slow phases will be shown. The movements of the eyes are the opposite of the rotation but they periodically reset their position to the central one and then try adjusting again. This is a way to push the system to its limit. Doctors can assess the VOR and integrity of the vestibule inducing a nystagmus by inducing a vestibular stimulation. It can either be done by rotating the head or by inducing a thermal stimulation (illusionary stimulation of the vestibule). Above are shown three sections of the brainstem with the entrance of the stimulus, the elaboration at the level of the vestibular nuclei, the computation and the projection to the nuclei through the MLF. The whole mechanism works if all these sections are healthy. ` In the graph, the firing rate is plotted with respect to velocity. The firing rate of the canals codes for the velocity and decides which should be the dynamic force exerted by the muscles. The brain also has to know the velocity, since the eyes need to move accordingly to counterbalance perfectly the movements. The velocity is coded by the semicircular canals that are optimal detectors of velocity. The vestibular nucleus projects to the oculomotor and the motoneurons will fire. This means that the firing rate of the motoneurons is perfectly correlated to the velocity and thus, the force exerted will parallel the velocity of production of force by the muscles. An additional step force is needed to hold the eye on position This is due to the presence of a neural integrator. 🡪 This graph plots the frequency of the movement in respect to the gain of the reflex (how good is the reflex in order to counterbalance the movements of the eye). If a system is submitted to a sinusoidal movement and then the frequency is changed and the VOR is checked, it is possible to see that at 1 Hz the movement is perfectly counterbalanced while below 1 it is not adequate. This means that the VOR is good at compensating fast movements but not in compensating slow movements (the optokinetic reflex is the one that acts in these situations). ` 8.​ Optokinetic reflex The optokinetic system extracts from the global pattern of visual stimulation a measure of how fast and in which direction the visual world is moving across the retina (retinal slip), using visual information to generate an eye movement equal in velocity and opposite in direction to the retinal slippage, stabilizing the visual world on the retina. Afferents from the retina go to oculomotor muscles to compensate for slow movements (the retina is not able to compensate for fast movements). The image shows the pathway for the optokinetic reflex. If there is damage in this circuit the VOR will still be present but the optokinetic will not function. The gain of the reflex with respect to the frequency graph is completely opposite to the same graph for the VOR. In this case, the perfect gain is achieved when moving slowly. The optokinetic reflex complements the VOR and normally the two systems work together. 9.​ Saccades Saccadic eye movements are high velocity gaze-shifting responses that can rotate the line of the gaze as quickly as 800°/sec. They can be evoked by visual but also somatosensory and auditory stimuli. They are based on CNS computed distance between the current position of the eye and the desired new position, the saccades can be: ​ Ballistic: pre-programmed movement executed without feedback. The brain has a predetermined program for these movements that do not need any feedback. ​ Intentional saccades: voluntary saccades, characteristic of vision when gazing at a fixed object (they are slower). For example, it is used for reading. Ballistic saccadic movements of the eyes while figuring out the image of an object (continuous rapid movements: focused mainly where the contrast was difficult to understand). The end point of this process is the MLF and the ocular movements. This occurs in the brainstem (in the reticular formation: the pontine one) where there’s a part of the MLF. Here there’s a complex formation that is devoted to the operative organization of the saccades. Omnipause and burst neurons are present: to have a saccade the omnipause neurons have to be inhibited to avoid the inhibition of the burst ones. In this way the burst neurons will induce an alternate excitation of the oculomotor nucleus to have the saccades. A center is organizing the movements in the brainstem: to move a part of the body the brain either organizes the whole movement (voluntary and dexterous ones) while others are “stereotyped: (e.g., locomotion, respiration, chewing). In these last movements there is no need for the brain to give commands over and over, so a center of command executive for that kind of action is present. Since saccades happen fast and continuously, a center for these actions is present in the brainstem. These are the cortical areas involved in saccades. The frontal cortex and the posterior parietal cortex are both involved. There are lots of cortical centers that are devoted to switching on the system in the brainstem involved in saccades. These centers do not execute: they are involved in planning when and where to perform the saccades. 10.​Smooth pursuit Smooth pursuit eye movements allow the eyes to closely follow a moving object. They are considered as a subtype of the optokinetic ones since they minimize the retinal slip of a small visual target. They possess a separated neural circuit for information regarding small portions of the visual world. 11.​Clinical point (lesion of the III cranial nerve) The oculomotor nerve doesn’t only innervate the muscle so in the case of a lesion there are different features: ​ complete ptosis: the eye is not open (partial ptosis may occur with an incomplete lesion); ​ divergent strabismus (eye ‘down and out’): since one nerve is not working while the other does, the muscular tone of the extraocular muscles of one side is working differently (the muscles are flaccid and do not work as springs anymore); ​ dilated pupil: the pupillary reflex is transmitted in the oculomotor so it’s not possible to constrict the pupil; ​ unreactive to direct light (the consensual reaction in the opposite normal eye is intact); ​ unreactive to accommodation. 12.​VIDEOS​ These are two videos related to the terminology of the eye movements and extraocular muscles: ​ http://www.youtube.com/watch?v=6GliSCGkpZ4 (Terminology) ​ https://www.youtube.com/watch?v=vd7OOJ7c1q4 (Extraocular muscles) A video showing the eyes counteracting the movement of the head was given: http://www.youtube.com/watch?v=j_R0LcPnZ_w Videos showing ways to assess the optokinetic reflex: ​ http://www.youtube.com/watch?v=U3KHgkZHuzc (some kind of stimulation in the retina can give the illusion of movement: the reflex is induced without an actual movement). ​ http://www.youtube.com/watch?v=KSJksSA6Q-A (nystagmus due to the optokinetic reflex: the continuous movement of an object and the continuous attempt of the system to counterbalance it). Video related to saccades containing movements from both healthy and damaged systems: http://www.youtube.com/watch?v=p6utlnynats The video shows smooth pursuit movements: http://www.youtube.com/watch?v=sKrvQgoR2uk