Input from proprioceptors in the extrinsic ocular muscles to the vestibular nuclei in the giant toad, bufo marinus

Abstract

Extracellular unit records were made from the left brain stem of decerebrate, paralysed giant toads (Bufo marinus) during passive movement of the ipsilateral eye. Units in the vestibular nuclear complex (VN) were identified by their short-latency responses to electrical stimulation of the anterior branch of the ipsilateral VIII cranial nerve. Of 58 units in the region of VN, as judged from field potentials to VIII nerve stimulation, fourteen gave phasic excitatory responses to passive movement of the eye and were also identified as vestibular nuclear units. A further twelve units which responded to eye-movement could not be assigned to VN; the remaining 32 units were in VN but did not respond to passive eye-movement. Also, of 16 units whose recording sites were identified histologically in the VN complex, 11 gave responses to vestibular nerve stimulation and to passive eye-movement and 5 responded to eye-movement only. Control experiments eliminated auditory, visual and cutaneous sources for the signal produced by passive eye-movement; thus, the signal must have arisen from intraorbital proprioceptors. Units in VN were also found which were excited by electrical stimulation of the intraorbital part of the fourth (trochlear) nerve; this provides strong evidence that proprioceptors in the extrinsic ocular muscles (EOM) are included in the receptors which provide the signal to VN during passive eye-movement. The effects of vestibular stimulation and of passive eye-movement were found to interact upon units in VN. When passive eye-movement and vestibular stimulation were paired the response to the second stimulus was significantly reduced over a range of interstimulus intervals. The conclusions are that orbital proprioceptive signals, including those from the EOM, project to the vestibular nuclei in the toad and, there, are able to influence processing of vestibular afferent signals. We suggest, therefore, that orbital proprioceptive signals may play a part in oculomotor control. The significance of the results is discussed in relation to the strategic position of the VN in the oculomotor control system.