A framework for considering the role of afference and efference in the control and perception of ocular position

It has been well established that extra-retinal information is used in the perception of visual direction and distance. Furthermore, a number of studies have established that both efference copy and afferent discharge contribute to the extra-retinal signal. Despite this, no model currently exists to explain how the signals which arise through oculomotor control contribute to perception. This paper attempts to provide such a framework. The first part of the paper outlines the framework [the cyclopean equilibrium point (EP) model] and considers the binoculus or cyclopean eye from the perspective of a current account of motor control (the EP hypothesis). An existing model is used to describe how the nervous system could utilise available efference copy and afferent extra retinal signals when determining the direction and distance of cyclopean fixation. Although the cyclopean EP model is speculative, it allows for a parsimonious framework when considering the oculomotor contribution to perception. The model has the additional advantage of being consistent with current theories regarding the control and perception of limb movement. The second part of the paper shows that the model is biologically plausible, demonstrates the use of the proposed model in describing the central control of eye movements with regard to non-conjugate peripheral adaptation and reconciles seemingly disparate empirical findings

The Role of Extraocular Muscle Afferent Signals in Oculomotor Control and Spatial Localisation

The extraocular muscles are richly endowed with sensory receptors. However, the precise role of afferent signals derived from these proprioceptors in visuomotor control is not fully understood, and has been the subject of considerable debate for more than a century. This has been investigated in more detail in these studies. Part 1 of this thesis provides a review of previously published work concerning both the existence and the function of extraocular muscle afferent signals in oculomotor control and spatial localisation. Part 2 of this thesis investigates oculomotor control. This was done by using an infrared corneal reflection device to record eye movements under different experimental conditions. Initially, an assessment of the reproducibility of this technique was performed in a population of normal adults. This confirmed that it was an accurate method for the repeated measurement of eye movements. The effect of experimentally impeding the movement of one eye, using a suction contact lens, on both saccades and smooth pursuit eye movements of the contralateral eye was then investigated. This technique is thought to modify non-visual afferent signals from the impeded eye, most likely to be derived from extraocular muscle proprioceptors. The results showed that for saccadic eye movements, the amplitude and peak velocity of the contralateral eye was reduced when one eye was impeded. However, the main sequence parameters remained unchanged. For smooth pursuit eye movements, the initial acceleration and velocity of the contralateral eye were reduced when one eye was impeded. These findings indicate that extraocular muscle afferent signals can under certain circumstances, influence the oculomotor control of both the saccadic and smooth pursuit systems. Part 3 of this thesis investigates spatial localisation. This was appraised by asking subjects to point at targets appearing on a computer touchscreen without being able to see the pointing hand. Initially an assessment of the reproducibility of this technique was performed in a population of normal children and adults to ensure that it was an accurate method for this purpose. Spatial localisation was then assessed in a group of 60 children with one particular type of strabismus, namely fully accommodative esotropia. A comparison was made of their pointing responses when their eyes are aligned (when wearing glasses) and when there is a manifest squint (not wearing glasses). The results showed that their perception of the central target position shifted in the direction of the non-squinting eye when their deviations are manifest. These findings are thought to be due to an alteration in extraretinal eye position information, derived in part, from extraocular muscle afferent signals, which helps to specify visual direction. A further study investigated the pointing responses of two groups of patients undergoing different forms of surgery for primary rhegmatogenous retinal detachment. The results showed that those patients undergoing conventional external scleral buckling procedures, and to a lesser extent those undergoing vitrectomy procedures, demonstrated significant changes in spatial localisation on the first postoperative day when viewing central and eccentric targets with their fellow unoperated eye. These changes had returned to normal by the subsequent follow-up assessmient approximately 10 days later. Again these findings are believed to be due to alterations in the extraretinal eye position signal, the source of which is likely to be modified extraocular muscle proprioception derived from the operated eye as a consequence of the surgical procedure. In conclusion, these studies have shown that under certain circumstances, an intervention affecting one eye, be it experimental or surgical, can influence both the oculomotor control and spatial localisation of the contralateral eye. This is the result of modified non-visual afferent information, most likely originating from within extraocular muscle proprioceptors. Not only do these findings contribute to our understanding of the basic mechanisms involved in visuomotor control, they may also have clinical implications by highlighting the potential effect of surgery involving the extraocular muscles, most notably strabismus procedures, on aspects of visual function that are often overlooked