Neuro-ophthalmology : neuronal control of eye moments

Chapter 4 - Extraocular movement
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Can I benefit from free shipping internationally? This requires some form of feedback to create two stable states, on and off, that are controlled by two inputs, usually called set and reset. Robinson's original gate circuit acts as a latch circuit because it feeds back the output of the pulse generator to the suppressor cell. However, it only has the set input, which is the trigger. The circuit unlatches automatically when the motor error estimate is reduced to the dead-zone which stops the burst cell activity.

The problem of making accurate saccades still comes down to how and when to restart the OPNs. The saccade normally ends when the ipsilateral cerebellum fires the contralateral brainstem IBNs, choking off i. By making the latch circuit independent of motor error, the effect of time jitter on movement accuracy is significantly reduced.

Bridging Knowledge About Gaze Control Across Applications, Disorders, Levels and Species

Accuracy can be maintained by the cerebellar circuit, and stability can be guaranteed as long as the OPNs reactivate soon after. A more detailed hypothesis for a latch circuit is developed below in A model of the latch circuit. LLBN Table 3 are found in the brainstem and receive input from the SC and cortical areas responsible for saccades, such as the frontal eye field, parietal eye field and supplementary eye field Scudder et al. Some of the LLBN probably project to the premotor burst neurons, whereas others [in the nucleus reticularis tegmenti pontis NRTP ] project to the cerebellum.

Scudder proposed a saccade model that used the LLBN as a re-settable integrator in the feed-forward path. The re-settable integrator was thought to be distinct from the common final integrator and to apply only to saccadic signals see below , in Conceptual evolution of saccadic models. However, later evidence suggests that the re-settable integrator does not really exist, and that the cerebellum replaces its function Quaia et al. Thus, LLBN seem to act as a summing junction for combining saccade commands from different areas involved in the preparation for a saccade. Tonic and burst—tonic neurons carry a signal related to the step component of MNs.

The step is assumed to be obtained by integrating in the mathematical sense velocity signals from PBN that generate the pulse of innervation this is an oversimplification, but sufficient for our needs here. Neurons that carry a vertical and torsional eye position step signal are present in and around the INC.

The mechanism that performs the integration is not well understood, although models that integrate because of reciprocal innervation positive or negative across the midline have been developed Cannon and Robinson, ; Cova and Galiana, ; Arnold and Robinson, , and recent work has cast light on how networks of neurons could perform this mathematical operation Aksay et al.

Thus, the integration of ocular motor signals depends on both cerebellar and brainstem circuits, but their respective roles remain enigmatic.

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The SC is laid out in a retinotopic map Robinson, , with small contralateral movements related to activity in the rostral SC, and large contralateral movements related to caudal SC. Neurons in the superficial layer are related to visual events, but neurons in the intermediate and deep layers are related to both visual and motor events.

Schiller et al.

Later it was also shown that ablations of the cerebellum caused persistent deficits in saccade amplitude e. Optican and Robinson, Despite these early observations, until the early s the SC was widely assumed to control saccadic amplitude, direction and trajectory. Many studies have since shown that the major role of the SC seems to be in selecting a target for foveation—either with saccadic or pursuit movements Krauzlis, —initiating the movement Bell et al.

The intermediate and deep layers of the SC contain two major types of neurons that are laid out in a retinotopic map. The other bursts just before the saccade, but has no prelude of activity SCBN.

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The SC projection is not uniform. The level of activity in the prelude of SCBUN corresponds to the likelihood that the target at that location will be the goal of a saccade Basso and Wurtz, SC activity is also a function of retinal error, whether for a saccade or a pursuit movement Krauzlis et al. In every experiment where the saccade goal is not the same as the visual target, such as adapted saccades FitzGibbon et al. Ablations of the SC significantly increase saccade latency and reduce peak speed, but do not affect accuracy Hanes et al.

Thus, the most parsimonious interpretation of SC function is that it contributes to identifying the target in retinotopic coordinates that is to be foveated, generates a trigger signal to shut down the OPN, and sends a fixed-direction drive to LLBNs to begin the saccade. Cells in the cMRF that are related to saccades discharge for contraversive movements, and can be divided into two groups Waitzman et al. Some cells have an abrupt, or clipped, end to the burst, at the end of the saccade. Lesions in the cMRF result in hypermetric contralateral saccades, reduced latency, and macrosaccadic square-wave jerks Waitzman et al.

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These results suggest that the cMRF is important for saccade function at both the initiation and termination stages. One possible model of their contribution is described below. A second influence on PBN and OPN is the cerebellum, which plays an important role in steering and stopping saccades, thus determining their accuracy. The posterior pole of the midline cerebellum has been most intensively studied. This region is divided into a cortical part vermis and paravermis and the underlying deep cerebellar nuclei fastigial, interpositus and dentate.

All relevant signals e. Climbing fibres bring a signal from the inferior olive to the cerebellar cortex. Climbing fibre activity is related to the distance to the target motor error at the beginning and end of a movement Kitazawa et al. The climbing fibre activity is assumed to be necessary to learn proper motor control, but its role is not well understood.

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Stimulation of vermal lobule V evokes saccades that range from upward to horizontal, while stimulation of lobules VI and VII evokes saccades that range from horizontal to downward. The amplitude of the elicited saccade, and the amount of post-saccadic drift, depend upon the initial position of the eye in the orbit. Purkinje cells that discharge in relation to saccades are located in a more restricted region, lobes VI c —VII, called the oculomotor vermis Noda and Fujikado, The oculomotor vermis projects to the caudal part of the fastigial nuclei.

Stimulation of the vermis produces saccades with an ipsilateral component Ron and Robinson, With currents near threshold, a topographic organization is evident Noda and Fujikado, The caudal part of the fastigial nucleus cFN is responsible for sending saccade commands to the region of the PBN in the contralateral brainstem.

FNN fire tonically with a low rate, and burst near the time of a saccade Ohtsuka and Noda, ; Fuchs et al. FNN fire for saccades in all directions, but electrical stimulation in the cFN elicits contralateral saccades Noda et al.

The latency of the burst is a function of the direction of the movement. FNN burst before saccade start for contralateral movements, but burst near saccade end for ipsilateral movements. Thus, the same neurons are firing for ipsi- and contralateral saccades, with the only difference being that they fire later for ipsilateral saccades. This issue is addressed further in the section Cerebellar models. Many areas of the cerebral cortex e.

The basal ganglia are involved in selecting and preventing movements, and in reward Hikosaka et al.

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The substantia nigra pars reticulata tonically inhibits the intermediate layers of the SC. This tonic activity can be suppressed by inhibition from the caudate nucleus, allowing a saccade. As important as they are for selecting the target for saccades, these areas do not play a role in generating the saccadic pulse itself.

Thus, a discussion of their function is beyond the scope of this review. In this section we present a brief history of saccadic models, beginning with the first model that was physiologically plausible. Robinson proposed that the innervation needed to make a saccade had to consist of two components: a pulse to overcome the viscous drag in the orbit, allowing for a fast movement, and a step to overcome the elastic restoring force in the orbit.

Robinson proposed that the step could be computed as a function of the pulse, which simplified the problem of generating saccadic innervation to that of generating the pulse Robinson, Furthermore, extraocular muscle proprioception, unlike skeletal muscle spindles, does not participate in a stretch reflex Keller and Robinson, Thus, it was assumed that saccades were ballistic, i.

Shortly after this, Zee et al. Indeed, these movements were so slow that visual re-afference returned in time to influence the saccadic system.


Neuronal Control of Eye Movements. Wong, Agnes MD, PhD, FRCSC. Journal of Neuro-Ophthalmology: December - Volume 28 - Issue 4 - p Neuro-ophthalmology: Neuronal Control of Eye Movements. Front Cover. Andreas Straube, U. Büttner. Karger Medical and Scientific Publishers, Jan 1,

They found that if the target jumped to a new location after the patient began a saccade, the eye would turn around in mid-flight and go to the new target. This demonstrated that the saccadic system was not ballistic and led Zee and Robinson to propose that the pulse of innervation was generated during the movement by an internal, or local, feedback loop based on an efference copy of eye position. This efference copy was obtained by integrating the pulse that came from the brainstem burst neurons Zee et al. This model immediately found wide acceptance because it generated both normal and slow saccades that stopped automatically i.

An important refinement of the original local feedback loop model was made by Zee and Robinson in , stimulated by an attempt to explain microsaccadic oscillations see Section on high-frequency saccadic oscillations. In developing that model they used a new non-linear function to represent the activity of the burst neurons for a given motor error which is still widely used today van Gisbergen et al.

To explain the small amplitude, high-frequency oscillations observed in some patients, they added a delay in the local feedback loop around the high-gain amplifier representing the burst neurons Zee and Robinson, ; Ashe et al. The original version of the model had an efference copy of the eye position signal which was fed back to a comparator that computed the instantaneous, or dynamic motor error: the difference between desired eye position and current eye position. The efference copy was also used to reconstruct an internal estimate of the target's position in spatial coordinates.

However, all saccade-related neurons found to date encode retinotopic error and change in eye position, not position in space.