PHASE-RELATIONS OF PURKINJE-CELLS IN THE RABBIT FLOCCULUS DURING COMPENSATORY EYE-MOVEMENTS

1. Purkinje cells in the rabbit flocculus that respond best to rotatio n about the vertical axis (VA) project to flocculus-receiving neurons (FRNs) in the medial vestibular nucleus. During sinusoidal rotation, t he phase of FRNs leads that of medial vestibular nucleus neurons not r eceiving floccular inhibition (non-FRNs). If the FRN phase lead is pro duced by signals from the flocculus, then the Purkinje cells should fu nctionally lead the FRNs. In the present study we recorded from VA Pur kinje cells in the flocculi of awake, pigmented rabbits during compens atory eye movements to determine whether Purkinje cells have the appro priate 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. Th e phase of the simple spike (SS) modulation in reference to eye and he ad 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 Purkin je cells increased with contralateral head rotation. During rotation i n the light, the SS modulation showed a phase lead in reference to con tralateral head position that increased with increasing frequency (med ian 56.9 degrees at 0.05 Hz, 78.6 degrees at 0.8 Hz). The SS modulatio n led the FRN modulation significantly at all frequencies. The differe nce of medians was greatest (19.2 degrees) at 0.05 Hz and progressivel y decreased with increasing frequency (all Ps < 0.005, Wilcoxon rank-s um test). 4. During rotation in the dark, the SS modulation had a grea ter 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 S S modulation in the dark led that of the FRNs significantly at all fre quencies (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) act ivity of all VA Purkinje cells increased with ipsilateral head rotatio n in the light. Fourier analysis of the cross-correlogram of the CS an d SS activity showed that the phase lag of the CS modulation in refere nce 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 th ese two frequencies were significantly different (P < 0.001). These da ta indicate that the average temporal reciprocity between CS and SS mo dulation is fixed across the range of frequencies used in the present study. 6. The CS activity of most Purkinje cells did not modulate duri ng 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, cases (14%) showed C S modulation. In the majority (15 of 17) of these cases, the CS activi ty increased with contralateral head rotation; these modulations occur red predominantly at the higher stimulus velocities. 7. On the basis o f the finding that FRNs of the medial vestibular nucleus lead non-FRNs , we predicted that floccular VA Purkinje cells would in turn lead FRN s. This prediction is confirmed in the present study. The data are the refore consistent with the hypothesis that the phase-leading character istics of FRN modulation could come about by summation of VA Purkinje cell activity with that of cells whose phase would otherwise be identi cal to that of non-FRNs. The floccular SS output appears to increase t he phase lead of the net preoculomotor signal, which is in part compos ed of the FRN and non-FRN signals. 8. The phase lead of the floccular output may be created by emphasizing the velocity component of messy f iber signals originating in the vestibular nuclei.