Extreme vestibulo‐ocular adaptation induced by prolonged optical reversal of vision

Abstract

1. These experiments investigated plastic changes in the vestibulo‐ocular reflex (VOR) of human subjects consequent to long‐term optical reversal of vision during free head movement. Horizontal vision‐reversal was produced by head‐mounted dove prisms. Four normal adults were continuously exposed to these conditions during 2, 6, 7 and 27 days respectively. 2. A sinusoidal rotational stimulus, previously shown to be nonhabituating (1/6 Hz; 60°/sec amplitude), was used to test the VOR in the dark at frequent intervals both during the period of vision‐reversal and an equal period after return to normal vision. D.c. electro‐oculography (EOG) was used to record eye movement, taking care to avoid changes of EOG gain due to light/dark adaptation of the retina. 3. All subjects showed substantial reduction of VOR gain (eye velocity/head velocity) during the first 2 days of vision‐reversal. The 6‐, 7‐ and 27‐day subjects showed further reduction of gain which reached a low plateau at about 25% the normal value by the end of one week. At this time the attenuation of some EOG records was so marked as to defy extraction of a meaningful sinusoidal signal. 4. After removal of the prisms VOR gain recovered along a time course which approximated that of the original adaptive attenuation. 5. In the 27‐day experiment large changes of phase developed in the VOR during the second week of vision‐reversal. These changes generally progressed in a lagging sense, to reach 130° phase lag relative to normal by the beginning of the third week. Accompanying this was a considerable restoration of gain from 25 to 50% the normal value. These adapted conditions, which approximate functional reversal of the reflex, were then maintained steady, even overnight, until return to normal vision on the 28th day. 6. Thereafter, whereas VOR phase returned to near‐normal in 2 hr, restoration of gain occupied a further 2‐3 weeks. 7. There was a highly systematic relation between instantaneous gain and phase, even during periods of widely fluctuating change associated with transition from one steady state to another. During such transition there was a tendency for directional preponderance to occur in the VOR. 8. All the observed changes were highly specific to the plane of vision‐reversal, no VOR changes being observed in the sagittal plane. 9. VOR changes were adaptive, in the sense that they were always goal‐directed towards the requirements of retinal image stabilization during head movement. They were plastic to the extent that there was extensive and retained remodelling of the reflex towards this goal. 10. It is inferred that all the observed changes in gain and phase are compatible with a simple neural network employing known vestibulo‐ocular projections via brainstem and cerebellar pathways, providing that the reversed visual tracking task can produce plastic modulation of efficacy in the cerebellar pathway and that this pathway exhibits a dynamic characteristic producing moderate phase lead in a sinusoidal signal at 1/6 Hz.