Bernhard J. M. Hess

Static Roll and Pitch in the Monkey: Shift and Rotation of Listing's Plane

In three rhesus monkeys three-dimensional eye positions were measured with the dual search coil technique. Recordings of spontaneous eye movements were made in the light and in the dark, with the monkeys in different static roll or pitch positions. Eye positions were expressed as rotation vectors. In all static positions eye rotation vectors were confined to a plane, i.e. Listings plane was conserved. Tilt about the roll axis shifted the plane along this axis, i.e. a constant torsional component was added to all eye positions. Tilt about the pitch axis changed the pitch angle of Listings plane.

Calibration of three-dimensional eye position using search coil signals in the rhesus monkey

A procedure is described to calibrate three-dimensional eye position with a dual-search coil implant in rhesus monkeys using a two-field magnetic system. The method allows one to determine the sensitivity of the search coils taking into account the presence of d.c. offset voltages. The orientation of the implant on the eye relative to a space-fixed reference frame is computed using fixations of targets arranged vertically. The critical steps of the procedure are discussed and documented by experimental data.

Deficits in torsional and vertical rapid eye movements and shift of Listing's plane after uni- and bilateral lesions of the rostral interstitial nucleus of the medial longitudinal fasciculus

The rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF) contains burst neurons whose activity precedes rapid eye movements with a vertical and/or torsional component. To ascertain their causal role in the generation of conjugate eye movements, we placed uni- and bilateral kainic acid lesions in that region. Unilateral inactivation of the riMLF leads to a loss of all rapid eye movements with an ipsitorsional component (ipsitorsional is defined as movement of the upper pole of the ipsilateral eye in a temporal direction). Vertical eye movements are impaired in an asymmetric way, with downward movements slowed and upward movements little affected. Listings plane is shifted in the contratorsional direction, i.e., we find a constant torsional offset for all eye positions. With bilateral lesions one observes a total loss of all vertical and torsional eye movements, while Listings plane retains its shape and position. These results show that burst neurons in the riMLF play a decisive role in generating rapid eye movements with a vertical and torsional component.

Control of eye orientation: where does the brain's role end and the muscle's begin?

Our understanding of how the brain controls eye movements has benefited enormously from the comparison of neuronal activity with eye movements and the quantification of these relationships with mathematical models. Although these early studies focused on horizontal and vertical eye movements, recent behavioural and modelling studies have illustrated the importance, but also the complexity, of extending previous conclusions to the problems of controlling eye and head orientation in three dimensions (3‐D). An important facet in understanding 3‐D eye orientation and movement has been the discovery of mobile, soft‐tissue sheaths or ‘pulleys’ in the orbit which might influence the pulling direction of extraocular muscles. Appropriately placed pulleys could generate the eye‐position‐dependent tilt of the ocular rotation axes which are characteristic for eye movements which follow Listings law. Based on such pulley models of the oculomotor plant it has recently been proposed that a simple two‐dimensional (2‐D) neural controller would be sufficient to generate correct 3‐D eye orientation and movement. In contrast to this apparent simplification in oculomotor control, multiple behavioural observations suggest that the visuo‐motor transformations, as well as the premotor circuitry for saccades, pursuit eye movements and the vestibulo‐ocular reflexes, must include a neural controller which operates in 3‐D, even when considering an eye plant with pulleys. This review summarizes the most recent work and ideas on this controversy. In addition, by proposing directly testable hypotheses, we point out that, in analogy to the previously successful steps towards elucidating the neural control of horizontal eye movements, we need a quantitative characterization first of motoneuron and next of premotor neuron properties in 3‐D before we can succeed in gaining further insight into the neural control of 3‐D motor behaviours.

Self-motion-induced eye movements: effects on visual acuity and navigation

Self-motion disturbs the stability of retinal images by inducing optic flow. Objects of interest need to be fixated or tracked, yet these eye movements can infringe on the experienced retinal flow that is important for visual navigation. Separating the components of optic flow caused by an eye movement from those due to self-motion, as well as using optic flow for visual navigation while simultaneously maintaining visual acuity on near targets, represent key challenges for the visual system. Here we summarize recent advances in our understanding of how the visuomotor and vestibulomotor systems function and interact, given the complex task of compensating for instabilities of retinal images, which typically vary as a function of retinal location and differ for each eye.

Simultaneous measurements of calcium oxalate crystal nucleation and aggregation: impact of various modifiers

Rates of nucleation and aggregation of calcium oxalate crystals were derived from 20-min time course measurements of OD620 after mixing solutions containing CaCl2 and K2C2O4 at 37°C, pH 5.7, ionic strength (IS) 0.21, with constant stirring (500 rpm); final assay concentrations were 4.25 mM calcium and 0.5 mM oxalate, respectively. The maximum increase of OD620 with time, termed SN, mainly reflects maximum rate of formation of new particles and thus crystal nucleation. After equilibrium has been reached, OD620 progressively decreases despite ionized calcium staying constant and no new particles being formed, due to crystal aggregation. Rate of aggregation, SA, is derived from the maximum decrease in OD620 with time. SN and SA are not independent, as indicated by a positive correlation (r=0.844, P=0.0001). Among the modifiers studied, citrate at 0.5–2.5 mM lowered both SN and SA in a concentration-dependent manner (P<0.01 for all comparisons vs control). Chondroitin-6-sulfate at 6.25–25 mg/l moderately lowered SN, whereas it strongly inhibited aggregation (P<0.01 vs control). At 6.8–20.4 mg/l, albumin did not affect nucleation, whereas it inhibited aggregation in a concentration-dependent manner (P<0.005 vs control for all comparisons).

Direction of heading and vestibular control of binocular eye movements

To optimize visual fixation on near targets against translational disturbances, the eyes must move in compliance with geometrical constraints that are related to the distance as well as the speed and direction relative to the target. It is often assumed that the oculomotor system uses the vestibular signals during such movements mainly to stabilize the foveal image irrespective of the peripheral vision. To test this hypothesis, trained rhesus monkeys were asked to maintain fixation on isovergence targets at different horizontal eccentricities during 10 Hz oscillations along different horizontal directions. We found that the two eyes moved in compliance with the geometrical constraints of the gaze-stabilization hypothesis, although response gains were generally small ( approximately 0.5). The best agreement with the gaze stabilization hypothesis occurred for heading directions within +/-30 degrees from straight-ahead, whereas lateral movements exhibited greater variability and larger directional errors that reflected the statistical response variability inherent in the non-linear dependence on heading direction. In contrast to undercompensatory version (conjugate) components, the disjunctive part of the response (vergence) exhibited unity or higher than unity gains. The high vergence gains might reflect a strategy that aims at maintaining the binocular coordination of the gaze lines despite the low gain of the version movements.

Low-frequency otolith and semicircular canal interactions after canal inactivation

Abstract. During sustained constant velocity and low-frequency off-vertical axis rotations (OVAR), otolith signals contribute significantly to slow-phase eye velocity. The adaptive plasticity of these responses was investigated here after semicircular canal plugging. Inactivation of semicircular canals results in a highly compromised and deficient vestibulo-ocular reflex (VOR). Based on the VOR enhancement hypothesis, one could expect an adaptive increase of otolith-borne angular velocity signals due to combined otolith/canal inputs after inactivation of the semicircular canals. Contrary to expectations, however, the steady-state slow-phase velocity during constant velocity OVAR decreased in amplitude over time. A similar progressive decrease in VOR gain was also observed during low-frequency off-vertical axis oscillations. This response deterioration was present in animals with either lateral or vertical semicircular canals inactivated and was limited to the plane(s) of the plugged canals. The results are consistent with the idea that the low-frequency otolith signals do not simply enhance VOR responses. Rather, the nervous system appears to correlate vestibular sensory information from the otoliths and the semicircular canals to generate an integral response to head motion.

Inertial vestibular coding of motion: concepts and evidence

Central processing of inertial sensory information about head attitude and motion in space is crucial for motor control. Vestibular signals are coded relative to a non-inertial system, the head, that is virtually continuously in motion. Evidence for transformation of vestibular signals from head-fixed sensory coordinates to gravity-centered coordinates have been provided by studies of the vestibulo-ocular reflex. The underlying central processing depends on otolith afferent information that needs to be resolved in terms of head translation related inertial forces and head attitude dependent pull of gravity. Theoretical solutions have been suggested, but experimental evidence is still scarce. It appears, along these lines, that gaze control systems are intimately linked to motor control of head attitude and posture.

Three-dimensional head angular velocity detection from otolith afferent signals

Afferent signals from the otolith organs can produce compensatory eye position and velocity signals which has been described as linear vestibulo-ocular reflex (LVOR). The afferent otolith signals carry information about head orientation and changes of head orientation relative to gravity. A head orientation (tilt) related position signal can be obtained from population vector coding of tonic otolith afferent signals during static or dynamic head tilts, which in turn could produce compensatory eye position signals in the LVOR. On the other hand, eye angular velocity signals may be extracted, as proposed in this study, from the population response of tilt-velocity sensitive otolith afferents. Such afferents are shown to encode instantaneous head orientation relative to gravity at onset of a head movement and, as the movement continues, the projection of head angular velocity onto the earth-horizontal plane, indicating the instantaneous direction of movement relative to gravity. Angular velocity components along the earth-vertical direction which are not directly encoded by otolith afferents can be detected by central signal processing. Central reconstruction of 3D head angular velocity allows to obtain information about absolute head orientation in space even in the absence of semicircular canal related information. Such information is important for generating compensatory eye movements as well as for dynamic control of posture.