RESPONSES DURING EYE-MOVEMENTS OF BRAIN-STEM NEURONS THAT RECEIVE MONOSYNAPTIC INHIBITION FROM THE FLOCCULUS AND VENTRAL PARAFLOCCULUS IN MONKEYS

1. We have identified a group of brain stem cells caned ''flocculus target neurons'' (or FTNs) because they are inhibited at monosynaptic latencies by stimulation of the flocculus and the ventral paraflocculus with single electrical pulses. We report the responses of FTNs, as well as those of other brain stem cells, during horizontal eye movements with the head stationary and during natural vestibular stimulation in monkeys. 2. FTNs discharged primarily in relation to eye movements. The majority (71%) showed increased firing for eye movement away from the side of the recording (''contraversive''), which is consistent with their inhibition by Purkinje cells that show increased firing for eye movement toward the side of recording. However, a significant and surprisingly large percentage (29%) of FTNs showed increased firing for eye movement toward the side of recording (''ipsiversive''). 3. The firing rate of FTNs showed modulation pursuit of sinusoidal target motion with the head stationary and during the compensatory eye movements evoked by fixation of an earth-stationary target with sinusoidal head rotation. In addition, firing rate was related to eye position during steady fixation at different positions. Of the FTNs that showed increased firing for contraversive eye motion during pursuit with the head stationary, most had an inflection in the relationship between firing rate and eye position so that the sensitivity to eye position was low for eye positions ipsilateral to straight-ahead gaze and high for eye positions contralateral to straight-ahead gaze. 4. When the monkey canceled the vestibuloocular reflex (VOR) by tracking a target that moved exactly with him during sinusoidal head rotation, the firing rate of FTNs was modulated much less strongly than during pursuit with the head stationary. In the FTNs that showed increased firing for contraversive eye motion during pursuit, firing rate during cancellation of the VOR increased for contraversive head motion during sinusoidal vestibular rotation at 0.4 Hz but was only weakly modulated during rotation at 0.2 Hz. 5. The position-vestibular-pause cells (PVP-cells), previously identified as interneurons in the disynaptic VOR pathways, were not inhibited by stimulation of the flocculus and ventral paraflocculus and had response properties that were different from FTNs. The majority (69%) showed increased firing for contraversive eye motion during pursuit and for ipsiversive head motion during cancellation of the VOR, whereas some (31%) showed the opposite direction preferences under both conditions. Unlike FTNs, PVP-cells had responses during cancellation of the VOR that were as large as or larger than their responses during pursuit with the head stationary. 6. We conclude that FTNs are likely to be interneurons in the pathways from the flocculus and ventral paraflocculus to the extraocular motoneurons. On the basis of the findings of other investigators, we suggest that FTNs also are interneurons in the disynaptic brain stem VOR pathways and that they may play an important role in pursuit eye movements as well as in motor learning in the VOR.