OCULOMOTOR SYSTEM Ralph M. Siegel ~/texts/admin/found92/ocular_lect.txt I. Types of eye movements A. Conjugate movements 1. VOR a. corrects for head rotation b. stimulus => acceleration of semicircular canals c. fast movements and short latency d. sensitive to high velocities; insensitive to low velocities e. define nystagmus with slow phase VOR and quick phase resetting 2. OKN a. corrects for slip of the visual scene across the retina b. stimulus => large field image velocity across the retina c. slow movements and long latency d. compliments VOR e. insensitive to high velocities; sensitive to low velocities f. nystagmoid 3. Saccades a. used to direct the fovea towards new visual targets of interest b. stimulus => retinotopic position of the stimulus c. fast and long latency 4. Smooth pursuit a. keeps smoothly moving visual targets from slipping off the fovea b. stimulus => target velocity c. moderate latency and moderate velocities B. Vergence 1. disjunctive or nonconjugate (opposite horizontal directions of rotation) 2. directs the fovea of the two eyes to cross at the distance of visual targets of interest 3. stimulus => target depth (many cues, primary: binocular disparity) 4. moderate latency and slow movements II. Motor plant A. more well understood than the somatic motor system B. simpler model system for study than somatic motor system or locomotion C. Ball & joint motion 1. one joint system 2. constant load 3. motion is restricted to rotation about the center of the globe; there are essentially no lateral motions of the eye a. must deal with only 3 of the potential 6 degrees of movement available in free space b. there is no interaction of multiple joints 4. easy to measure 12/06/93 - 2 - 5. inputs can be precisely presented and well controlled via the visual system D. Six extraocular muscles for each eye 1. fig 43-6 of Kandel & Schwartz 2. striated (skeletal) muscle 3. 3 sets of agonist-antagonist pairs a. lateral and medial rectus (1) primary pulling directions in the horizontal direction b. superior and inferior rectus (1) primary pulling directions in the vertical direction c. superior and inferior oblique (1) primary pulling directions to rotate the eye around the 'line of sight' (2) cyclotorsion (a) clockwise-counterclockwise 4. the motor neurons a. the motor neurons that innervate the extraocular muscles lie within several nuclei of the cranial nerves (1) the oculomotor nucleus (III) and the oculomotor nerve (a) autonomic NS motor efferents that innervate the intrinsic muscles of the eye also travel in the nerve III (b) ipsilateral medial rectus (c) ipsilateral inferior rectus (d) ipsilateral inferior oblique (e) contralateral superior rectus (2) the trochlear nucleus (IV) and nerve (a) contralateral superior oblique (3) the abducens nucleus (VI) and nerve (a) ipsilateral lateral rectus (b) contralateral medial rectus motor neurons in III (4) mnemonic rules (recall by exceptions): (a) IV:sup. oblique and VI:lateral rec.; all others:III (b) all ipsilateral but two (the superiors): i) superior oblique ii) superior rectus 5. Actions of the individual extraocular muscles a. each agonist-antagonist pair work together in one of the three directions of rotation of the eye (horiz., vert., cyclotorsion) b. each muscle has a primary pulling direction and several have secondary or tertiary pulling directions dependent on the geometry 6. potentially each of the 12 extraocular muscles could be controlled independently giving a potential of 12 degrees of freedom that the motor centers of the brain would have to control and specify a. instead, the oculomotor system obeys a set of 12/06/93 - 3 - rules that reduce the problem to only 2 degrees of freedom. That is to say that higher horizontal and vertical b. the direct brainstem inputs to the motor neurons are organized such that their pattern of recruitment intrinsically implements these orderly relations c. Sherrington's law of reciprocal innervation of agonist-antagonist pairs (1) when you send an excitatory signal to the medial rectus, you send the same signal with the opposite sign (relaxation) to the lateral rectus d. Herring's law of equal innervation of the two eyes (1) whatever combination of horizontal and vertical signals that are sent to the left eye are also send to the right eye e. Donder's law and Listing's law (1) for each combination of horizontal and vertical rotation, there is a unique cyclotorsion (Donder's) (2) that rotates in a plane perpendicular to the line of sight (Listing's) III. Motor control signals (emphasize the saccadic system) A. Activity of the motor neurons to drive the plant 1. There are two forces on the globe that the motor plant must overcome to move the eyes: a. viscous elements which tend to resist movement of the eye b. elastic elements that tend to return the eye to a default position near straight ahead 2. Therefore, to make quick phase eye movements (i.e. saccades) in the on-direction (pulling direction) the motor neurons produce a burst of activity to overcome the viscous drag of the eye, followed by a new, higher rate of tonic activity to counteract the elastic forces that pull the eye back toward straight ahead. a. this is called a pulse-step pattern of temporal activity b. in the off-direction oculomotor neurons have a reciprocal pause-step to a reduced rate of tonic activity 3. the pulse is related to the velocity of the eye movement and the step is related to the final eye position B. There are two inputs (that come from the brainstem reticular formation) to the motor neurons 1. burst neurons that provide the pulse 2. tonic neurons that provide the step 3. The inputs from higher centers of the brain stimulate these burst neurons in the brainstem a. larger movements produce larger bursts b. larger bursts produce faster movements 4. It is thought that the tonic signals are generated by somehow integrating the velocity-related bursts (much 12/06/93 - 4 - like the VOR integrated the signal related to head velocity) a. the integral of a faster movement, obviously, is a larger change in eye position (a large shift in eye position) C. Brainstem saccade generator 1. fig 43-12 of Kandel & Schwartz demonstrates the activity of several types of neurons that are known to be involved in controlling the motor neurons 2. Pause cells a. are tonically active, except to pause just before and during saccades b. These neurons inhibit the burst cells, working like a latch that prevents the burst neurons from producing a movements until a trigger says it's 'OK' c. by pausing just before a saccade, they release the burst cells to do there job 3. Burst neurons a. excitatory burst neurons excite the motor neurons on the ipsilateral side b. inhibitory burst neurons inhibit the burst neurons on the contralateral side, thus subserving Sherrington's law 4. Tonic cells a. represent the integral of the burst neurons b. stimulate the ipsilateral motor neurons to hold the eye in the current position 5. Burst-Tonic cells a. also project to the ipsilateral motor neurons b. probably represent the partial integration of the burst signal to the tonic signal IV. Oculomotor centers of the brain A. Brainstem 1. the cranial nuclei that contain the ocular motor neurons 2. all of the cells described above are found in and near regions of the pontine, medullary and midbrain reticular formation B. (Major) Higher centers of ocular control 1. Superior colliculus a. receives inputs from the retina, directly b. receives inputs from cortical structures (1) the frontal eye fields (2) the posterior parietal cortex c. receives inputs from the basal ganglia d. has a topographical map of visual-motor space (1) small movements => rostral (2) large movements => caudal (3) upward movements => medial (4) downward movements => lateral 2. fig 43-12 from Kandel & Schwartz 3. Frontal Eye Fields a. the eye representation of the motor system homunculus 12/06/93 - 5 - b. involved in voluntary control of eye movements 4. Posterior parietal cortex a. visual-spatial signals related to the 'where' pathway of vision b. reciprocally interconnected with FEF 5. area MST (medial superior temporal sulcus) in occipito-temporal cortex a. involved in controlling smooth pursuit in response to visual stimulus motion 12/06/93 - 6 - Ocular Motor Readings Kandel and Schwartz, chapter 43 Essay questions: 1. Describe the role of the pre-frontal cortex in the generation of eye movements and contrast it to the role of parietal cortex. Can these be considered two indenpent sequential processing regions or do they work together? 2. Describe the oculomotor plant in terms of any of the models that have been derived. Is there reasonable experimental evidence for these models or they hot air? 3. Cortex is often thought to acting alone in cognition. However it is clear in the study of eye movements that there is a synergy between cortex and sub-cortical regions (e.g. prefrontal cortex and the superior colliculus). Discuss evidence for and/or against interaction between cortical and sub-cortical regions and use particular eye movements as examples. 4. What representation of space is used to make eye movement and where are these representations found? Are they distributed or edonsl 12/06/93