Phase relations of Purkinje cells in the rabbit flocculus during compensatory eye movements

1. Purkinje cells in the rabbit flocculus that respond best to rotation about the vertical axis (VA) project to flocculus-receiving neurons (FRNs) in the medial vestibular nucleus. During sinusoidal rotation, the phase of FRNs leads that of medial vestibular nucleus neurons not receiving floccular inhibition (non-FRNs). If the FRN phase lead is produced by signals from the flocculus, then the Purkinje cells should functionally lead the FRNs. In the present study we recorded from VA Purkinje cells in the flocculi of awake, pigmented rabbits during compensatory eye movements to determine whether Purkinje cells have the appropriate firing rate phases to explain the phase-leading characteristics of the FRNs. 2. Awake rabbits were sinusoidally rotated about the VA in the light and the dark at 0.05-0.8 Hz with different amplitudes. The phase of the simple spike (SS) modulation in reference to eye and head position was calculated by determining the eye position sensitivity and the eye velocity sensitivity using multivariate linear regression and Fourier analysis. The phase of the SS modulation in reference to head position was compared with the phase of the FRN modulation, which was obtained in prior experiments with the same stimulus paradigms. 3. The SS activity of nearly all of the 88 recorded floccular VA Purkinje cells increased with contralateral head rotation. During rotation in the light, the SS modulation showed a phase lead in reference to contralateral head position that increased with increasing frequency (median 56.9 degrees at 0.05 Hz, 78.6 degrees at 0.8 Hz). The SS modulation led the FRN modulation significantly at all frequencies. The difference of medians was greatest (19.2 degrees) at 0.05 Hz and progressively decreased with increasing frequency (all Ps < 0.005, Wilcoxon rank-sum test). 4. During rotation in the dark, the SS modulation had a greater phase lead in reference to head position than in the light (median 110.3 degrees at 0.05 Hz, 86.6 degrees at 0.8 Hz). The phase of the SS modulation in the dark led that of the FRNs significantly at all frequencies (difference of medians varied from 24.2 degrees at 0.05 Hz to 9.1 degrees at 0.8 Hz; all Ps < 0.005). 5. The complex spike (CS) activity of all VA Purkinje cells increased with ipsilateral head rotation in the light. Fourier analysis of the cross-correlogram of the CS and SS activity showed that the phase lag of the CS modulation in reference to the SS modulation at 0.05 Hz in the light was not significantly different from that at 0.8 Hz (median 199.7 degrees at 0.05 Hz, 198.3 degrees at 0.8 Hz), even though the phases of the SS modulation at these two frequencies were significantly different (P < 0.001). These data indicate that the average temporal reciprocity between CS and SS modulation is fixed across the range of frequencies used in the present study. 6. The CS activity of most Purkinje cells did not modulate during rotation in the dark. Of 124 cases (each case consisting of the CS and SS data of a VA Purkinje cell obtained at 1 particular frequency) examined over the frequency range of 0.05-0.8 Hz, 17 cases (14%) showed CS modulation. In the majority (15 of 17) of these cases, the CS activity increased with contralateral head rotation; these modulations occurred predominantly at the higher stimulus velocities. 7. On the basis of the finding that FRNs of the medial vestibular nucleus lead non-FRNs, we predicted that floccular VA Purkinje cells would in turn lead FRNs. This prediction is confirmed in the present study. The data are therefore consistent with the hypothesis that the phase-leading characteristics of FRN modulation could come about by summation of VA Purkinje cell activity with that of cells whose phase would otherwise be identical to that of non-FRNs. The floccular SS output appears to increase the phase lead of the net preoculomotor signal, which is in part composed of the FRN and non-FRN signals.