Otolith inputs to pursuit neurons in the frontal eye fields of alert monkeys

The smooth-pursuit system must interact with the vestibular system to maintain the accuracy of eye movements in space during head movement. Maintenance of a target image on the foveae is required not only during head rotation which activates primarily semi-circular canals but also during head translation which activates otolith organs. The caudal part of the frontal eye fields (FEF) contains pursuit neurons. The majority of them receive vestibular inputs induced by whole body rotation. However, it has not been tested whether FEF pursuit neurons receive otolith inputs. In the present study, we first classified FEF pursuit neurons as belonging to one of three groups (vergence + fronto-parallel pursuit, vergence only, fronto-parallel pursuit only) based on their responses during fronto-parallel pursuit and mid-sagittal vergence-pursuit. We, then, tested discharge modulation of these neurons during fore/aft and/or right/left translation by passively moving the whole body sinusoidally at 0.33 Hz (+/-10 cm, peak velocity 19 cm/s; 0.04g). The majority of FEF pursuit neurons in all three groups were activated by fore/aft and right/left translation without a target in complete darkness. There was no correlation between the magnitude of discharge modulation and translational vestibulo-ocular reflex (VOR). Preferred directions of translational responses were distributed nearly evenly in front of the monkeys. Discharge modulation was also observed when a target moved together with whole body, requiring the monkeys to cancel the translational VOR. These results indicate that the discharge modulation of FEF pursuit neurons during whole body translation reflected otolith inputs.