I.M.L. Donaldson

The anatomical substrate for cat extraocular muscle proprioception

The localization of cell bodies and of the central terminal projections of extraocular muscle afferent neurons was examined in adult cats using transport of horseradish peroxidase. The results confirm that primary afferent cell somata subserving extraocular muscle proprioception are located within the medial portion of the ipsilateral trigeminal ganglion. Occasional labeling of cell bodies in the mesencephalic nucleus of the trigeminal nerve occurred only in association with evidence of spread of tracer beyond the eye muscles. These results, taken together with work of others, make it unlikely that the trigeminal mesencephalic nucleus participates significantly in eye muscle proprioception. The central projections of extraocular muscle afferent neurons were found consistently in a restricted area in the ventral portion of the pars interpolaris of the spinal trigeminal nucleus. This corresponds exactly with their site of termination in the monkey [Porter (1986) J. comp. Neurol. 247, 133-143]. Terminal labeling was restricted to this area in cases in which there was no evidence of spread of the tracer beyond the extraocular muscles. In contrast to previous findings in the monkey, the cat did not exhibit a second muscle afferent representation in the cuneate nucleus. Though it is known that extraocular muscle afferent signals interact with both retinal and vestibular signals, and thus probably are involved in both visual processing and oculomotor control, the details of their roles in these processes are not yet clear.(ABSTRACT TRUNCATED AT 250 WORDS)

Afferent Signals from Pigeon Extraocular Muscles Modify the Vestibular Responses of Units in the Abducens Nucleus

Although the extraocular muscles contain stretch receptors it is generally believed that their afferents exert no influence on the control of eye movement. However, we have shown previously that these afferent signals reach various brainstem centres concerned with eye movement, notably the vestibular nuclei, and that the decerebrate pigeon is a favourable preparation in which to study their effects. If the extraocular muscle afferents do influence oculomotor control from moment‒to‒moment they should exert a demonstrable effect on the oculomotor nuclei. We now present evidence that extraocular muscle afferent signals do, indeed, alter the responses of units in an oculomotor nucleus (the abducens, VI nerve nucleus, which supplies the lateral rectus muscle) to horizontal, vestibular stimulation induced by sinusoidal oscillation of the bird. Such stimuli evoke a vestibulo-ocular reflex in the intact bird. The extraocular stretch receptors were activated by passive eye movement within the pigeon’s saccadic range; such movements modified the vestibular responses of all 19 units studied which were all, histologically, in the abducens nucleus. The magnitude of the effects, purely inhibitory in 15 units, depended both on the amplitude and the velocity of the eye movement and most units showed selectivity for particular combinations of plane (e. g. horizontal versus vertical) and direction (e. g. rostral versus caudal) of eye movement. The results show that an afferent signal from the extraocular muscles influences vestibularly driven activity in the abducens nucleus to which it carries information related to amplitude, velocity, plane and direction of eye movement in the saccadic range. They thus strongly support the view that extraocular afferent signals are involved in the control of eye movement.

Afferent signals from the extraocular muscles of the pigeon modify the vestibulo-ocular reflex.

Although the extraocular muscles (EOM) contain stretch receptors it is generally thought that the afferent signals which they provide play no role in the control of eye movement. We have previously shown that these afferent signals do modify both the vestibular responses of single units in the oculomotor control system and the electromyographic responses of the EOM during the vestibulo-ocular reflex (VOR). We have now investigated the effect of EOM afferent signals on the VOR itself, by recording the electro-oculogram of one eye while imposing movements on the other eye during the VOR. Moving the eye in a manner which mimics the slow phase of the VOR, we have found that, as the peak velocity of the imposed eye movement increases, the amplitude of eye movement of the other eye decreases. These results confirm that the output of the VOR itself, expressed as movement of the globe, and not merely some of its component parts, is modified by EOM afferent signals.

Evidence for corrective effects of afferent signals from the extraocular muscles on single units in the pigeon vestibulo-oculomotor system

The role of extraocular muscle (EOM) afferent feedback signals in the control of eye movement is still controversial. We recorded from 106 single units in the vestibular nuclei, oculomotor nuclei and reticular formation of 80 decerebrate, paralysed pigeons. EOM afferents were stimulated by passive eye movement (PEM) during vestibular stimulation by sinusoidal oscillation in the horizontal plane. We found that EOM afferent signals profoundly modified the vestibular responses of 91 (86%) of the single units recorded. As well as using PEM to simulate eye movements similar to saccades, we moved the eye in a manner which mimicked the slow phase of the vestibulo-ocular reflex (artificial VOR, AVOR). We have found evidence that, as well as providing signals closely related to the parameters of eye movement, PEM alters the vestibular responses of cells during AVOR in a manner which suggests that EOM afferent signals may play a corrective role in the moment-to-moment control of eye movement in the vestibulo-ocular reflex.

The primary afferent pathway of extracular muscle proprioception in the pigeon

Recent physiological experiments in our laboratory suggest that extraocular muscle proprioceptive signals are involved in oculomotor control in the pigeon [e.g., Knox and Donaldson (1993) Proc. R. Soc. Lond. B 253, 77-82]; the present results provide information about the primary afferent pathway involved in these actions. In other physiological experiments [Hayman et al. (1993) Proc. R. Soc. Lond. B 254, 115-122] we have shown that extraocular muscle afferent signals modify vestibularly driven neck reflexes in the pigeon; the present results suggest an anatomical substrate for these effects. The localization of the cell bodies and of the central terminations of afferent fibres from the extraocular muscles of the pigeon was examined using transport of horseradish peroxidase. The results showed that primary afferent cell somata subserving extraocular muscle proprioception are located within the ipsilateral trigeminal ganglion. The presence of heavily labelled brainstem neurons reported in a previous study [Eden et al. (1982) Brain Res. 237, 15-21] was confirmed; however, these cells were shown to be accessory abducens motoneurons innervating the quadratus muscle, and presumably the pyramidalis muscle also, and not proprioceptive afferent somata as had been suggested. The central projections of extraocular muscle afferent neurons were found consistently in a restricted area of the external cuneate nucleus. This is in contrast to findings in a number of mammals in which the terminal label has been seen to cluster in portions of the spinal trigeminal nucleus. The presence of a lateral trigeminal tract in the pigeon, through which the afferent axons course, which terminates exclusively in the ventral portion of the external cuneate nucleus may explain this finding.

Afferent signals from the extraocular muscles affect the gain of the horizontal vestibulo-ocular reflex in the alert pigeon

We have shown previously that the gain of the horizontal vestibulo-ocular reflex (HVOR) is modified by afferent signals from extraocular muscle proprioceptors in the decerebrate pigeon. We have now analysed the variability of the HVOR in intact, alert pigeons and, using the artificial vestibulo-ocular reflex method, have found that in all of the pigeons tested afferent signals from the extraocular muscle proprioceptors modify the gain, but not the phase, of the HVOR. While this effect was seen in a given bird only on some occasions, when present it was consistent in magnitude and direction and closely similar to our previous observations on decerebrate pigeons. These results from alert, intact birds strengthen the evidence that extraocular muscle afferent signals play a part in the control of the vestibulo-ocular reflex.

The Effect of Afferent Signals from Extraocular Muscles on Visual Responses of Cells in the Optic Tectum of the Pigeon

Feedback signals from the muscles that move the eye in the orbit, the extraocular muscles, are generally assumed to play no important role either in visual processing or in oculomotor control. However, we have recently shown that these signals are involved in the vestibular control of eye movement, the vestibulo-ocular reflex. To investigate whether they might also be involved in visual processing, we have recorded from single units in the primary visual system of the pigeon, in the optic tectum. We demonstrate here that the visual responses of these units can be modified by extraocular muscle afferent signals induced by passive eye movement, and that information concerning the direction and amplitude of eye movement reaches the tectum and interacts with visually responsive units in a directionally selective manner. These results suggest that extraocular muscle afferent signals may be involved in the processing of visual information in the optic tectum of the pigeon.

Signals of eye position and velocity in the first-order afferents from pigeon extraocular muscles

Responses of first-order afferents from the extraocular muscles of the pigeon were studied by extracellular recording in the ophthalmic part of the trigeminal ganglion of decerebrate, paralysed pigeons. The afferents responded to both the amplitude and velocity of ramp displacements of the intact eye with amplitude sensitivities ranging from 0.9 to 8 impulses/s/deg of eye displacement beyond the response threshold. Once a new stable position had been reached, the afferent signal depended only upon the absolute position of the eye within the orbit. The responses adapted in seconds rather than minutes so these units would not provide a continuous signal of the position of an immobile eye; they are best described as signalling position and velocity in relation to eye movements.