Zangemeister WH, Stark L: Annals NY Acad Sci 1981; 374: 540-559 Summary.
Head movements play an important role in gaze: the interaction between eye and head movements involves both their shared role in directing gaze and the compensatory vestibular ocular reflex. This shared role and interaction with respect to body posture and locomotion have attracted the interest of neurologists since the time of Barany, Magnus, and Dodge. Coordinated gaze movement normally has an initial eye-in-orbit saccade onto the target followed by a synkinetic and much slower head movement. At the level of electromyographic [EMG] signal latencies, these are synchronous: but because the viscoinertial dynamics of head and neck muscles are different from the viscoelastic dynamics of eye and extraocular muscles. the saccade is over before head position has changed. The vestibular ocular reflex [VOR] generated by head acceleration drives the compensatory eye movement [CEM], eye-in-orbit, in the opposite direction so that gaze, eye-in-space, remains on target. The CEM and its VOR component are influenced by visual input and other factors that modify its gain; resultant overshoots or undershoots are corrected by later saccades. The features have been defined in monkeys and man, and some clinical studies have begun exploration of pathological changes.
Beside this classical coordinated gaze movement [type I]. Other gaze patterns exist, generally determined by asynchronicity of the neural controller signals as reflected in the experimentally recorded EMGs. Sometimes head movement occurs very late [type II], at times with an anticipatory, non-VOR, compensatory eye movement [ACEM] appearing during the interval before the head movement. When the head movement occurs early, [type III], eye saccades often are slowed or truncated by the interaction with the ongoing VOR.
A very late eye saccade, occurring after the head movement and the VOR are completed [type IV], is a consequence of the early head movement influenced by a variety of experimental protocol conditions. These gaze patterns reflect the increased flexibility of head movements as compared with the rather stereotyped
generation of eye saccades.
Clinical Examples of Gaze Plane Analysis in patients with homonymous hemianopia (see figure).
Clinical examples demonstrate the variety of interactions of eye and head in gaze movments in patients with homonymous hemianopia. The upper left shows a gaze movement toward the seeing hemifield [SHH], placed in the upper-right direction in this figure [directions are plotted positively in graphs, [eye position ordinate; head position abscissa ], with eye movement undershooting the target so that the right hemianopic field [represented by diagonal slashes] does not obscure the view of the target either after the first eye saccade or during head movement and CEM, or with the second eye saccade – compensating or correcting for initial undershoot [small upward vertical arrow]. The upper left also shows a gaze movement toward the blind homonymous hemifield [BHH], which overshoots the target on initial eye movement saccade [vertical arrow downward from the
origin] so that the right hemianopic field does not obscure the view of the target. This upper-left corner of the FIGURE shows saccadic eye movements adaptive for safe acquisition of target. Contrariwise, maladaptive saccadic eye movements [middle left] overshoot a target in the SHH or undershoot a target in the BHH, so
that view of the target is obscured by the hemianopic field.
Similarly, a change in CEM gain can be adaptive [upper middle] or maladaptive [lower middle]. Unity gain has a minus 45° slope in contrast to CEM gains, greater with greater slope, or lower with less slope. Corrective saccades [small vertical arrow] are required to compensate for non-unity CEM gains. The effect of the ACEM, occurring before actual head movement, is shown on the upper and middle right. On gaze to target in the SHH with secure eye saccade, the occurrence of an adaptive ACEM places the hemianopic field away from the
target and permits safe viewing of the target during head movement and CEM. A corrective saccade is necessary [small vertical upward arrow] at the end of gaze movement. A maladaptive ACEM [lower right] moves gaze off the target so that the HH obscures view of the target. More frequently occurring clinical exam-
ples are interpreted easily in the light of these less often occurring examples. Compensating discrepancies [left] permit safe viewing. With gaze to the SHH, undershooting saccade [upward vertical arrow] prevents low CEM gain [downward oblique arrow] from obscuring view of the target in many instances [about 60%]. Similarly, an overshooting saccade [downward vertical arrow] with gaze to the BHH prevents high CEM gain [upward oblique arrow] from obscuring the target in many instances [about 60%]. An especially interesting compensatory discrepancy sometimes occurs [about 25%; lowermost row, middle] when saccadic overshoot [large downward vertical arrow] with gaze to the BHH is corrected by an ACEM [small upward vertical arrow] so that the fovea is on target but without a safety margin. A pure saccadic undershoot discrepancy also sometimes occours [about 25%; upward vertical arrow], which permits safe target acquisition. Maladaptive discrepancies may occur [right] with low CEM gain [downward oblique arrow] on gaze to the SHH, or with ACEM [small upward vertical arrow] and high CEM gain [upward oblique arrow]. Both place target into the hemianopic field during CEM and require corrective saccades into the BHH.