The aim of this study was to characterize the signals transmitted by the neurons of the nucleus prepositus hypoglossal (NPH) to the middle zone of the flocculus of the cat. The methods, the behavioral testing, and the animals used in this study were the same as those used in the accompanying paper on medial vestibular nucleus neurons. 2. The rostral two-thirds of the NPH was explored in alert animals with microelectrodes during stimulation of the middle zone of both flocculi. Discharges of neurons were analyzed during spontaneous eye movements (head fixed) and during horizontal vestibuloocular reflex (VOR) activity elicited by sinusoidal stimulation (10, 20, 30, or 40 degrees at 0.1 Hz). Forty neurons were found to be antidromically activated from only one or the other of the two flocculi (latency: 0.99 +/- 0.17 ms, mean +/- SD): 37 from the contralateral flocculus and 3 from the ipsilateral one. None of the neurons could be activated antidromically from both flocculi. Floccular stimulation never resulted in direct inhibition of these NPH neurons. 3. Of the 37 units antidromically activated from the contralateral flocculus, 26 were recorded sufficiently long to allow full quantitative analysis. Most of these (20 neurons) were classified as burst-tonic (BT) neurons. The BT neurons exhibited during each saccade made in one direction (the ON direction) a burst of spikes, and during postsaccadic fixation a tonic activity that increased with gaze displacement in the ON direction. The mean sensitivity of the neurons to eye velocity during the "ON" saccades was 3.3 +/- 1.6 spikes.s-1.deg-1.s-1. During intersaccadic fixation, the mean sensitivity to eye position was 3.6 +/- 2.5 spikes.s-1.deg-1. During the VOR, the majority showed modulation in relation to both eye position and eye velocity. The mean sensitivity to eye position during the VOR was 3.4 +/- 2.6 spikes.s-1.deg-1 (range: 0.2-8.1 spikes.s-1.deg-1). The mean sensitivity to eye velocity during the VOR was 2.1 +/- 1.3 spikes.s-1.deg-1.s-1. The mean phase lead of with respect to eye position was 16.4 +/- 6.8 degrees (range: 6.0-28.9 degrees). Eighty percent of the BT neurons behaved as type I neurons. Forty-seven percent of the BT neurons also presented some head velocity sensitivity (1.48 +/- 0.6 spikes.s-1.deg-1.s-1, mean +/- SD). 4. Other NPH cells antidromically activated from the contralateral flocculus were classified in two groups: bidirectional burst (BB) neurons (n = 4) and burst-driving (BD) neurons (n = 2). The BB neurons were characterized by a burst discharge during every horizontal saccade or VOR quick phase, irrespective of the direction. The mean sensitivity of the BB neurons to eye velocity during saccades was 3.3 +/- 7.8 (SD) spikes.s-1.deg-1.s-1. Both BD neurons increased their firing rate during the slow VOR phases induced by an ipsilateral rotation (type I neurons) and exhibited high-frequency bursts in association with ipsilaterally directed quick phases. 5. The results indicate that the main projection of the NPH onto the middle zone of the flocculus comes from contralaterally located type I BT neurons. Signals transmitted in this path associate a high sensitivity for eye velocity with a high sensitivity for eye position. This type of input is consistent with the suggestion that the main function of the flocculus is to control the gain of downstream reflexes and to perform a fine adjustment of the gaze holding command.
