Changes in dorsal neck muscle activity related to imposed eye movement in the decerebrate pigeon

Abstract

Movements of the head and eyes are known to be intimately related. Eye position has also been shown to be closely related to the electromyographic activity of dorsal neck muscles; however, extraocular muscle proprioception has not generally been considered to play a part in the control of such movements. We have previously shown that, in the pigeon, imposed movements of one eye modify the vestibular responses of several dorsal neck muscles in ways that are dependent on stimulus parameters such as the amplitude and velocity of imposed eye movement. The present study examines more closely the interactions between imposed eye movements and different muscle pairs. The three neck muscle pairs studied each responded to afferent signals from the extraocular muscles in discrete and specific ways which appeared to be correlated with their different actions. Complementary effects of imposed eye movements in the horizontal plane were seen for both the complexus and splenius muscle pairs, with imposed eye movements in one direction producing the largest inhibition of the ipsilateral muscle's vestibular response and imposed eye movements in the opposite direction the largest inhibition of the contralateral muscle's vestibular response. During roll–tilt oscillation (ear-up/ear-down) in the frontal plane, similar complementary effects of imposed eye movement were seen in the complexus muscle pair, but the splenius muscle pair showed little tuning, with similar inhibition for imposed eye movement directed either upwards or downwards. In contrast to these complementary effects, the biventer cervicis muscle pair showed no vestibular modulation during vestibular stimulation in the horizontal plane and their spontaneous activity was not altered by imposed eye movement. During roll–tilt oscillation (ear-up/ear-down) in the frontal plane imposed eye movement directed vertically upwards increased both muscles' vestibular responses and imposed eye movement directed vertically downwards inhibited both muscles' vestibular responses. Section of the ophthalmic branch of the trigeminal nerve (deafferenting the eye muscles) abolished the effects of imposed eye movement on the neck muscle pairs. In conjunction with further control experiments these results provide compelling evidence that proprioceptive signals from the extraocular muscles reach the neck muscles and provide them with a functionally significant signal. We have previously shown that signals from the extraocular muscles appear to be involved in the control of the vestibulo-ocular reflex. It follows from the experiments reported here that proprioceptive signals from the extraocular muscles are also likely to be involved in the control of gaze.