Fig. 19.1 The major inputs to the vertical and horizontal gaze centres are saccadic and pursuit commands from the cerebral hemispheres and the vestibular ocular reflexes from the vestibular nuclei in the medulla. These impulses are then transmitted to the individual ocular motor nuclei in the midbrain and pons. Internuclear pathways coordinate the movements generated in the gaze centres with each other and with the third, fourth and sixth nerve nuclei. Excitatory impulses to an agonist muscle are accompanied by inhibitory impulses to its antagonist.

Fig. 19.2 Saccadic movements have been shown biomechanically to be generated by impulses in the form of a pulse and step. To change eye position a rapid burst of neuronal signals (the pulse) is fired by the gaze centre and this rapidly moves the eye to the new position. This rapid burst is integrated in the ‘pulse-step generator’ (a neuronal complex within the gaze centre) to produce an increased tonic discharge (the step) which holds the eye in its new position. Similar responses take place in the agonist of the fellow eye and reciprocal impulses relax the antagonist muscles. These changes are reflected by the EMG recording in an individual muscle. Neurophysiologically saccades are initiated by burst cells in the paramedian pontine reticular formation (PPRF) which are inhibited from firing by pause cells at all times except during a saccade. Thus the saccadic input suppresses the pause cell which permits the burst cell to discharge immediately.

Fig. 19.3 The pulse–step generator exists physiologically in the horizontal gaze centre—otherwise known as the paramedian pontine reticular formation (PPRF)— in the pons and various mismatches of the pulse to step signals have been shown to explain some types of nystagmus and eye movement abnormalities seen in clinical practice.

Fig. 19.4 Saccadic eye movements can be elicited simply by asking patients to look right and left or up and down. This is a useful strategy where the observation of large amplitude saccades may reveal subtle abnormalities of saccadic velocity. An alternative strategy is to ask patients to shift fixation from one target to another, in this way saccades of large and small amplitude and involving a variety of gaze shifts can be observed. The accuracy of saccades (under- or over-shooting) can be tested. Slowing of the velocity of saccades may be conjugate (as in a gaze palsy), dysconjugate (as in a lateral rectus paresis or internuclear ophthalmoplegia) or global (as in an ocular myopathy or some forms of cerebellar disease).

Fig. 19.5 When asking a subject to follow a target it is essential that the target is clearly visible and is moved neither too slowly nor too rapidly. The reader should experiment by trying to follow his or her own finger as it is moved in a 180° arc from one side of the head to the other at arm’s length. A comfortable speed is about 30° per seconds (6 seconds from ear to ear). Pursuit movements are used to examine ductions and versions but, instead of looking at the range of movement, we are now interested in the accuracy of the following movement itself. The observer must watch for saccadic intrusions which will indicate that the eye is not keeping up with the target (in other words, there is reduced gain of the smooth pursuit reflex). This is a universal finding in cerebellar disease.

Fig. 19.6 Vestibular ocular reflexes (VORs) are tested by asking the patient to fixate a distant target (such as an acuity chart) and then gently moving the patient’s head from side to side or up and down with increasing frequency until the patient reports movement of the target or the subjective acuity falls, indicating retinal slip of the image. Alternatively a retinal landmark can be fixed using the direct ophthalmoscope while the examiner rocks the head to and fro. Loss of the VOR causes symptoms such as instability of the horizon as the patient walks and is seen not uncommonly with multiple sclerosis.

Fig. 19.7 Suppression of the VOR can be tested by asking the patient to grip a target mounted on a spatula between the teeth and to move the head from side to side or up and down with increasing rapidity until the patient reports an inability to keep the image ‘still’ or saccadic eye movements are observed as fixation is lost and taken up again. The mechanism used to suppress the VOR is the pursuit mechanism; if smooth pursuit is abnormal then so will be VOR suppression, and vice versa. Patients who are able to suppress their VOR complain of unusual symptoms such as difficulty with reading when travelling.

Fig. 19.8 Only one functioning labyrinth is required for the tests described in Fig. 19.6 to be normal. Caloric testing can be used to examine each labyrinth separately. Caloric reflexes are produced by stimulating the semicircular canals and vestibular nuclei with warm or cold water and can provide useful information on the integrity of these pathways in the brainstem; this is especially useful in the neurological assessment of brainstem damage in an unconscious patient. In a conscious patient cold water in the external auditory meatus generates a nystagmus of both eyes with a fast phase to the opposite side but in unconscious patients the saccadic phase is lost and a tonic deviation to the same side is seen. This indicates an intact pons but the results must be interpreted with caution after acute drug overdoses when false-negative responses may be seen. Calorics can be adapted to test vertical gaze (and therefore the integrity of the midbrain) by syringing both ears.

Fig. 19.9 Unilateral labyrinthine function can be tested at the bedside. If the head is rotated abruptly, the initial phase of the VOR is mediated by the labyrinth towards which the head is turned. If that labyrinth is not functioning initially the eyes move with the head and there is a corrective saccade as fixation is taken up again.

Fig. 19.10 The vestibular system responds only to acceleration and slow head movements (less than 1° per second) stimulate the optokinetic reflex (OKN). The hand-held OKN drum is useful as a bedside test of the pursuit and saccadic systems. If there is a saccadic palsy the eyes will deviate tonically in the direction of the stripe movement: the pursuit mechanism has been elicited but there is no saccade to return gaze towards primary position. Turning the drum to the right elicits an ipsilateral pursuit movement to the right and a contralateral saccade to the left. In essence turning the drum to the right tests the right hemisphere and vice versa to the left.

Fig. 19.18 Following an acute cerebrovascular accident involving supranuclear pathways, saccadic gaze is lost in the direction opposite to the side of the lesion and input from the remaining hemisphere deviates the eyes towards the side of the lesion. (Occasionally, irritative lesions, such as cerebral tumours or abscesses, produce deviation of the eyes to the contralateral side.)

Fig. 19.19 (Left) On command the patient is unable to make a gaze movement to the target on his right. (Right) On doll’s head rotation to the left, however, the eyes deviate fully to the right demonstrating intact pontine reflexes and the supranuclear nature of the lesion.

Fig. 19.20 A CT scan of the patient seen in Fig. 19.18, showing a large infarct in the internal capsule due to the occlusion of middle cerebral artery branches, corresponding to lesion 1 in Fig. 19.21. If the patient survives the acute ocular deviation recovers rapidly. Horizontal gaze becomes full and saccades return to normal. This is probably due to a restoration of control mechanisms by the superior colliculus.

Fig. 19.21 A ‘wiring diagram’ shows that lesion 1 would result in a right-sided supranuclear gaze palsy whereas lesion 2 destroys the pontine gaze centre producing a right-sided pontine gaze palsy.

Fig. 19.22 This elderly woman suffered a cerebrovascular accident in the upper midbrain. She retained the ability to make rapid and full horizontal saccades.

Fig. 19.23 In the same patient, voluntary up and down gaze to saccadic command is lost and compensated for by head movement. ‘Doll’s head’ rotation shows that vertical movements can be produced and that pontine reflexes are intact.

Fig. 19.24 Convergence retraction nystagmus is an interesting ocular movement abnormality sometimes seen with vertical gaze palsies. Bursts of convergence with retraction of both eyes into the orbits are seen either spontaneously or on attempting an upward saccade. These movements may also be accompanied by accommodative spasm which accounts for the frequent complaint of blurred vision. Convergence retraction nystagmus is shown particularly well if the patient views a downward rotating optokinetic drum which stimulates upward refixational saccades.

Fig. 19.25 In convergence retraction nystagmus the lesion is thought to cause disinhibition of the ocular motor nuclei allowing bursts of co-firing of the external ocular muscles. The medial recti muscles are the most powerful of the external ocular muscles and consequently the globes converge and retract into the orbits.

Fig. 19.26 Light–near dissociation of the pupils is the third sign of the triad of Parinaud’s syndrome. The pupils are normally moderately dilated and show a poor or absent light reaction but preserve the near reaction. It has been suggested that light reflex fibres are more dorsal in the midbrain and are therefore selectively damaged by lesions in this area with comparative sparing of the more ventrally sited near reflex pathways.