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Proprioception is the sense that lets us perceive the location, movement and action of the body parts. The proprioceptive apparatus includes specialized sense organs (proprioceptors) which are embedded in the skeletal muscles. The eyeballs are moved by six pairs of eye muscles and binocular vision depends on fine-tuned coordination of the optical axes of both eyes. Although experimental studies indicate that the brain has access to eye position information, both classical proprioceptors (muscle spindles and Golgi tendon organ) are absent in the extraocular muscles of most mammalian species. This paradox of monitoring extraocular muscle activity in the absence of typical proprioceptors seemed to be resolved when a particular nerve specialization (the palisade ending) was detected in the extraocular muscles of mammals. In fact, for decades there was consensus that palisade endings were sensory structures that provide eye position information. The sensory function was called into question when recent studies revealed the molecular phenotype and the origin of palisade endings. Today we are faced with the fact that palisade endings exhibit sensory as well as motor features. This review aims to evaluate the literature on extraocular muscle proprioceptors and palisade endings and to reconsider current knowledge of their structure and function., (© 2023 The Authors. Experimental Physiology published by John Wiley & Sons Ltd on behalf of The Physiological Society.)

The electrical activity of antidromically identified abducens internuclear neurons selectively deprived of their target motoneurons was recorded in chronic alert cats. Target motoneurons were killed by the injection of the cytotoxic lectin of Ricinus communis into the medial rectus muscle. Following target removal, the discharge pattern of abducens internuclear neurons showed an overall decrease in firing rate, a significant reduction in their sensitivity to eye position and velocity, and the presence of anomalous responses such as bursts of spikes associated with off-directed saccades. The decreased excitability of abducens internuclear neurons correlated well with a marked reduction in the synaptic efficacy of their inputs. Thus, both excitatory and inhibitory synaptic potentials of vestibular origin showed a noticeable decrease in amplitude. The alterations in firing properties and synaptic transmission were only observed during an initial period of 3 weeks following ricin injection. Within 1 month the electrophysiological parameters returned to control values and remained unaltered for 1 year. Retrograde labelling of abducens internuclear neurons revealed that no cell death occurred after target loss. The anterograde axonal labelling of these neurons showed a progressive decrease in the density of their axonal terminals, and no sign of redistribution to other areas was found. These findings indicate that abducens internuclear neurons are not dependent on the presence of their natural target cells, either for the survival or for the maintenance of appropriate physiological signals.

The activity of identified medial rectus motoneurons was recorded in alert cats during spontaneous and vestibular induced eye movements. Medial rectus motoneurons fired a burst of spikes slightly preceding adducting saccades and increased their discharge rate linearly with successive eye positions in the adducting direction. Conduction velocity (21.3 - 98.2 m/s), eye position sensitivity (ks, 7.1 +/- 1.5 spikes/s/deg), and eye velocity sensitivity (rs, 1 +/- 0.2 spikes/s/deg/s) during spontaneous eye movements, and time constants calculated from phase lead analysis (To, 135 +/- 36 ms) showed values similar to those described previously for cat abducens motoneurons. The firing rate during repeated fixation of the same eye position was affected significantly by the direction of the preceding saccade and by the animal's level of alertness. Eye velocity sensitivity was not significantly affected by changes in the animal's level of alertness. A weak negative relationship (coefficient of correlation=-0.56) was observed between eye velocity sensitivity (rv) and sinusoidal rotational frequency, with no change in eye position sensitivity (kv) with stimulus frequency. The subsequent changes in the time constant (Tv) calculated as Tv=rv/kv in relation to stimulus frequency suggests that the oculomotor system deviates from a (linear) first-order model.