Neuronal Control of Eye Movements - part 3 ppt

The sensory input for the generation of the VOR is provided by aset of motion sensors, which send the information about head angular velocity,linear acceleration, and orientation of the

The main features of the eye movement recording devices mentioned in thischapter are summarized in table 1 Since the EOG is still the only method thatallows measurement of eye movements while the eyes are closed, it remainsimportant for specialized applications that require this possibility Modern VOGsystems can measure 2-D gaze direction at spatial resolutions comparable tothose of search coil systems The accuracy of VOG devices is also comparable tothat of the search coil, but it depends on the ability of the subjects to fixate accu-rately System noise and accuracy of ocular torsion is slightly better in search coilsystems than in VOG The main disadvantage of the search coil is that it is inva-sive compared with the EOG, IRD, or VOG Therefore, search coil measurementsare advisable only for relatively short recordings requiring high temporal resolu-tion, high accuracy, and an objective calibration For most other applications,VOG seems to provide a good alternative to the search coil technique Untilrecently, the IRD was still a reasonable noninvasive alternative to the search coil,

at least for measuring horizontal (1-D) eye movements In the meantime, the poral resolution of VOG improved and is now sufficient to cover the temporalbandwidth of physiological eye movements The robustness of the system linear-ity with respect to displacements between the device and the eye is much better inVOG than in the IRD Therefore, the IRD appears to have been outdated by VOG

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Dev Ophthalmol Basel, Karger, 2007, vol 40, pp 35–51

of the SCCs within the head and of the functional properties of the otolith organs allows to localize and interpret certain patterns of nystagmus and ocular misalignment This is based

on the experimental observation that stimulation of a single SCC leads via the VOR to phase eye movements that rotate the globe in a plane parallel to that of the stimulated canal Furthermore, knowledge of the mechanisms that underlie compensation for vestibular dis- orders is essential for correctly diagnosing and effectively managing patients with vestibular disturbances.

slow-Copyright © 2007 S Karger AG, Basel

The vestibulo-ocular reflex (VOR) helps to stabilize the retinal image byrotating the eyes to compensate for movements of the head An ideal VOR, thattries to compensate for any arbitrary movement of the head in 3-D space, wouldgenerate eye rotations at the same speed as, but in the opposite direction to, headrotation independent of the momentary rotation axis of the head The desiredresult is that the eye remains still in space during head motion, enabling clearvision The VOR has two different physical properties The angular VOR, mediated

by the semicircular canals (SCCs), compensates for rotation The linear VOR,mediated by the otolith organs (saccule and utricle), compensates for translation.The angular VOR is primarily responsible for gaze stabilization The linear VOR

is most important in situations where near targets are being viewed [1, 2].The VOR has three main components: the peripheral sensory apparatus(the labyrinth), a central processing mechanism, and the motor output (the eyemuscles) [3] The sensory input for the generation of the VOR is provided by aset of motion sensors, which send the information about head angular velocity,linear acceleration, and orientation of the head with respect to gravity to thecentral nervous system (specifically the vestibular nucleus complex and thecerebellum) In the central nervous system, these signals are combined withother sensory information (e.g from the somatosensors) at as early stages as thevestibular nucleus complex to estimate head orientation The output of the cen-tral vestibular system is sent to the ocular muscles and the spinal cord to servethe VOR and the vestibulospinal reflex (VSR), the latter generating compen-satory body movement in order to maintain head and postural stability, therebypreventing falls The information goes also to cortical structures (e.g posteriorinsular vestibular cortex, PIVC) where it is further integrated with visual, pro-prioceptive, auditory and tactile input to generate a best possible perception ofmotion and space orientation [4] The performance of the VOR and VSR ismonitored by the central nervous system, and readjusted as necessary by adap-tive processes with immense capability of repair and adaptation mainly involv-ing cerebellar function (fig 1) [5]

The Peripheral Sensory Apparatus

The peripheral vestibular system includes the membranous and bonylabyrinths, and the motion sensors of the vestibular system, the hair cells Each

Visual

Vestibular

Proprioceptive

Adaptive processor (cerebellum)

Vestibular nuclear complex

Oculomotor neurons

Fig 1 Schematic drawing illustrating the VOR.

labyrinth consists of three SCCs, the cochlea, and the vestibule containing theutricle and saccule) The geometric arrangement of the SCCs allows for detec-tion of head rotation about any axis in space They are positioned in three nearlyorthogonal planes in the head and act as angular accelerometers working in apush-pull arrangement with the other labyrinth (right and left lateral SCC; rightanterior and left posterior SCC; left anterior and right posterior SCC) Theplanes of the SCCs are close to the planes of the extraocular muscles, thusallowing relatively simple neural connections between sensory neurons related

to individual canals, and motor output neurons, related to individual ocularmuscles (fig 2) [6] One end of each SCC is widened in diameter to form anampulla containing the cupula The cupula causes endolymphatic pressure dif-ferentials, associated with head motion, to be coupled to the hair cells embed-ded in the cupula These specialized hair cells are biological sensors thatconvert displacement due to head motion into neural firing When hairs are benttoward or away from the longest process of the hair cells, firing rate increases ordecreases in the vestibular nerve [7, 8] The hair cells of the saccule and utricle,the maculae, are located on the medial wall of the saccule and the floor of theutricle The otolithic membranes are structures similar to the cupulae, but asthey contain calcium carbonate crystals called otoconia, they have substantiallymore mass than the cupulae The mass of the otolithic membrane causes themaculae to be sensitive to gravity In contrast, the cupulae normally have thesame density as the surrounding endolymphatic fluid and are insensitive togravity By virtue of their orientation, the SCC and otolith organs are able torespond selectively to head motion in particular directions [9]

Central Processing of Vestibular Signals

The coplanar pairing of canals is associated with a push-pull change in thequantity of SCC output With rotation in the plane of a coplanar SCC pair, theneural firing increases from tonic resting discharge in one vestibular nerve anddecreases on the opposite site For the lateral canals, displacement of the cupulatowards the ampulla (ampullopetal flow) is excitatory, whereas for the verticalcanals, displacement of the cupula away from the ampulla (ampullofugal flow)

is excitatory (fig 3)

There are certain advantages to the push-pull arrangement of coplanarpairing First, pairing provides sensory redundancy If disease affects the SCCsfrom one member of a pair (e.g as in vestibular neuritis), the central nervoussystem will still receive vestibular information about head velocity within thatplane from the contralateral member of the coplanar pair Second, such a pair-ing allows the brain to ignore changes in neural firing that occur on both sides

mlf so

in lr

bc bc

Fig 2 The VOR network: corresponding SCCs and the main brainstem connections to

the oculomotor nuclei are shown lr, sr, ir, mr ⫽ Left, superior, inferior, medial rectus cle; IO, SO ⫽ inferior, superior oblique muscle; III ⫽ third nerve nucleus with inferior (ir), superior (sr), medial rectus (mr), and inferior oblique (io) motor neurons; IV ⫽ fourth nerve nucleus with superior oblique motor neurons (so); bc ⫽ brachium conjunctivum;

mus-VI ⫽ sixth nerve nucleus with lateral rectus (lr) and internuclear (in) motor neurons; mlf ⫽ medial longitudinal fasciculus; la, lh, lp ⫽ left anterior, horizontal and posterior SCC; ra, rh, rp ⫽ right anterior, horizontal and posterior SCC (Courtesy of D.A Robinson, Baltimore.)

simultaneously, such as might occur due to changes in body temperature orchemistry.

In the otoliths, as in the canals, there is a push-pull arrangement of sensors,but in addition to splitting the sensors across sides of the head, the push-pullprocessing arrangement for the otoliths is also incorporated into the geometry

of the otolithic membranes Within each otolithic macula, a curving zone, thestriola, separates the direction of hair cell polarization on each side.Consequently, head tilt results in increased afferent discharge from one part of amacula, while reducing the afferent discharge from another portion of the samemacula [10, 11]

There are two main targets for vestibular input from primary afferents: thevestibular nuclear complex and the cerebellum The vestibular nuclear complex

is the primary processor of vestibular input, and implements direct, fast nections between incoming afferent information and motor output neurons

con-R

Resting

Fig 3 With rotation toward the left side, the neural firing increases from tonic resting

discharge (shown as horizontal dotted line) in the vestibular nerve of the left lateral canal and decreases in the vestibular nerve of the right lateral canal During rotation, the head velocity corresponds to the difference in firing rate between SCC pairs.

The erebellum is the adaptive processor – it monitors vestibular performanceand readjusts central vestibular processing if necessary [12] At both locations,vestibular sensory input is processed in association with somatosensory andvisual sensory input [5].

The vestibular nuclear complex consists of 4 major nuclei (superior,medial, lateral, and descending) and at least 7 minor nuclei This large struc-ture, located primarily within the pons, also extends caudally into the medulla.The superior and medial vestibular nuclei are relays for the VOR The medialvestibular nucleus is also involved in the VSR, and coordinates head and eyemovements that occur together The lateral vestibular nucleus is the principalnucleus for the VSR The descending nucleus is connected to all of the othernuclei and the cerebellum, but has no primary outflow of its own [13] Thevestibular nuclei are connected via a system of commissures, which for themost part, are mutually inhibitory The commissures allow information to beshared between the two sides of the brainstem and implements the push-pullpairing of vestibular canals Extensive connections between the vestibularnuclear complex, cerebellum, ocular motor nuclei, and brainstem reticular acti-vating systems convey the efferent signals to the VOR and VSR effector organs,the extraocular and skeletal muscles [14] The output neurons of the VOR arethe motor neurons of the ocular motor nuclei, which drive the extraocular mus-cles resulting in conjugate movements of the eyes in the same plane as headmotion (fig 2)

VOR – Pathology

It is crucial to carefully evaluate the eye movements during clinical ination, as the physiological and anatomical substrate of the ocular motor sys-tem is intimately connected with the vestibular system via the VOR The VOR

exam-is responsible for the nystagmus phenomena seen in patients [15] Caloricstimulation provides perhaps the clearest analogy to what the patient withpathological vertigo and nystagmus experiences For example, warm stimula-tion of the left ear increases neural activity from the left lateral SCC and there-fore in the left vestibular nerve; it thereby produces not only left-beatinghorizontal nystagmus but a sense of turning about the body long axis, towardthe left Conversely, cold stimulation of the right ear reduces neural activity inthe right lateral SCC, the right vestibular nerve; and by commissural disinhibi-tion it also increases neural activity in the left vestibular nucleus and, there-fore, produces left-beating nystagmus and a sense of turning to the left (thenystagmus always beating toward the side of higher vestibular activity) [16,17] In a patient with sudden unilateral loss of peripheral vestibular function

(such as in vestibular neuritis), the situation is in some way analogous to a coldcaloric stimulus.

An example of vertigo due to pathological unilateral increase in vestibularactivity is benign paroxysmal positioning vertigo (BPPV), the most commonvestibular disorder With appropriate positioning, there is a sudden briefincrease in activity from one SCC The result is a sudden intense sense of self-rotation in the plane of the activated canal and a nystagmus beating in thisplane For example, if a patient with left posterior canal BPPV is rapidly placed

in the provocative left lateral position, there is a sense of self-rotation in a planehalfway between the roll and the pitch plane toward the patient’s left side with avertical – torsional nystagmus beating upward and with the torsional compon-ent to the lower ear [18–21]

Practical Aspects for Bedside Clinical Evaluation

An acute unilateral peripheral vestibular lesion reduces or eliminates inputfrom one or more SCCs and otolith organs on that side In the acute phase, acomplete lesion abolishes the tonic neuronal discharge (resting activity) in thevestibular nerve [22] The resulting loss of accelerometer function on one side

of the head and the imbalance between the tonic inputs on the two sides lead toboth spontaneous nystagmus and decreased and asymmetrical dynamic vestibu-lar responses Thus, there are both static and dynamic imbalances which need to

be evaluated

Static Imbalance

Spontaneous nystagmus (with the head still) is the hallmark of an ance in the tonic levels of activity mediating SCC-ocular reflexes Whenperipheral in origin, spontaneous nystagmus characteristically is damped byvisual fixation and is increased or only becomes apparent when fixation iseliminated Hence, one must look for spontaneous nystagmus behind Frenzellenses (magnifying lenses that prevent the patient from using visual fixation tosuppress any spontaneous nystagmus) or during ophthalmoscopy (with theopposite eye occluded to prevent fixation) The intensity of nystagmus is com-pared with that observed when the patient is fixing on a visual target.Nystagmus is sometimes seen or even palpated through closed eyelids Notethat during ophthalmoscopy the direction of any horizontal or vertical slowphases is opposite to the direction of the motion of the optic disk

imbal-The nystagmus should also be inspected for dependence on the position ofthe eye in the orbit Nystagmus arising from a peripheral lesion and most cen-tral lesions is more intense or may be evident only when the eye is deviated in