Does extraocular muscle proprioception influence oculomotor control?

Disorders of ocular motility are encountered on a regular basis within ophthalmic practice. They include a wide variety of conditions from non-paralytic strabismus commonly seen in paediatric clinics to acquired restrictive and paralytic conditions, which may be indicative of more serious underlying pathology. For an accurate diagnosis to be made an understanding of the basic mechanisms involved in oculomotor control is desirable. Eye movements are mediated by a complex hierarchy of neuronal systems. While the final common pathway consists of the motor nuclei and associated structures in the brainstem, oculomotor behaviour is shaped by the cerebellum, the superior colliculus, the basal ganglia, and the cortical eye fields. In order to coordinate the movement of the eyes, a process vital for both vision and visually guided behaviour, these brain centres must “know” the direction in which the eyes are pointing. If the eyes were fixed within the orbits then retinal (that is, visual) information would be suYcient to tell us where we are looking. However, the eyes, as well as the visual world, can and do move, and under these circumstances extraretinal (that is, non-visual) information is required to determine gaze direction. There are two broad hypotheses that seek to explain the source of this extraretinal information; while not mutually exclusive, they are often presented as alternatives. The “inflow” hypothesis holds that aVerent signals from the eVector muscles in the oculomotor system, the extraocular muscles (EOM), provide the necessary information about the positions of the eyes in the orbits and about movements of the eyes. This view can be attributed to Sherrington, although it fell out of favour, particularly in the 1960s, when the role of muscle receptors in general came to be doubted (see Matthews for review). The outflow hypothesis, attributed to Helmholtz, holds that central monitoring of a copy of the motor command sent to the EOM (eVerence copy or corollary discharge) provides the necessary extraretinal information. While in reality both aVerent and eVerent copy signals are probably involved, the relative contribution of each has been the subject of considerable debate for over a century. In this review we summarise the evidence concerning the existence of proprioceptive inflow from the EOM, and review recent physiological and clinical findings that it plays some part in oculomotor control.