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Department of Neurobiology, Pharmacology, and Physiology, University of Chicago, Illinois 60637
Submitted 4 March 2004; accepted in final form 30 March 2004
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSREFERENCES |
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; Hepp et al. 1989; Moschovakis et al. 1996; Scudder et al. 2002). The premotor signals that produce gaze stabilizing eye movements at the end of the eye-head gaze shift arise primarily from cells in the vestibular nuclei that mediate the vestibuloocular reflex (VOR) (McCrea and Gdowski 2003; McCrea et al. 1996; Phillips et al. 1996; Roy and Cullen 1998, 2001, 2002).
The eye-movement commands generated within brain stem VOR pathways during gaze shifts are complex (McCrea and Gdowski 2003). Most secondary VOR neurons are either insensitive to active head movements or cease firing altogether during saccadic gaze shifts. The insensitivity is due primarily to eye- and head-movement efference copy signals that cancel vestibular signals related to active head movements and produce saccade-related pauses in discharge (McCrea and Gdowski 2003; Roy and Cullen 2002). Near the end of the eye-head saccade, secondary VOR pathways begin producing signals that help stabilize gaze. One class of secondary vestibular neurons, the eye-head-velocity (EHV) neurons, have greater firing rate modulation during eye-head (gaze) saccade-related VOR eye movements than other secondary VOR neurons (Gdowski and McCrea 2000; McCrea and Gdowski 2003). Those cells putatively receive inputs from the cerebellar flocculus region (FLR), which includes the flocculus and the ventral paraflocculus (Lisberger et al. 1994a; Partsalis et al. 1995; Zhang et al. 1995b). The observation suggests the possibility that the cerebellar flocculus region might play an important role in stabilizing gaze immediately after saccades because many secondary EHV vestibular nucleus neurons receive inputs from FLR Purkinje (Pk) cells.
Although FLR Pk cells are largely insensitive to eye-head saccadic gaze shifts (Belton and McCrea 1999), their firing behavior during the VOR evoked immediately after gaze saccades has not been examined in detail. In this study, we compared the signals generated by FLR Pk cells during the VOR evoked by gaze saccade-related active head movements to the signals generated during the VOR evoked by passive head movements. We report that FLR Pk cells respond differently to the VOR evoked by saccadic head movements than they do to the VOR evoked by passive head movements. We discuss this different sensitivity to VOR eye movements in relation to the previously described responses of VOR pathway neurons and the role of the flocculus in controlling gaze during saccadic eye-head movements.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSREFERENCES |
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,2000b; McCrea and Gdowski 2003). All practices complied with National Institutes of Health principles of laboratory animal care (National Institutes of Health Publication No. 86-23). Surgical preparation
Two adult squirrel monkeys were prepared for recording both single-unit activity and eye movements. A woven coil of fine, Teflon-coated wire (Cooner) was sutured to the sclera of one eye for recording eye movements using the magnetic search coil technique. A Plexiglas well was fitted onto the parietal bone for the placement of microelectrodes, and a metal reference pin was affixed to the skull adjacent to the probe insertion site.
Experimental recording conditions
Animals were seated in a Plexiglas primate chair atop a vestibular turntable (Inland 832). A harness that was fitted over the shoulders and in front of the trunk inhibited arm-raising and trunk-twist movements. A rod was attached to a keyed metal stud affixed to the occipital bone. The rod was coaxial with the rotational axis of the turntable and positioned within 5 mm of the C1–C2 axis. It rotated within a low-friction ball bearing assembly fixed to the table, which allowed ±45° head movements in the plane of the horizontal semicircular canals. A universal joint 5 cm above the head allowed pendular head position adjustments around the universal joint axis. The head could be reversibly fixed to the turntable by disabling the universal joint and blocking angular rotation of the vertical axis rod. The monkeys were trained to fixate and pursue a small visual target (0.5 W HeNe laser, <0.2° diam) projected onto a cylindrical, surrounding projection screen 90 cm distant from the monkey. The background presented by the screen was not an effective optokinetic stimulus during constant-velocity turntable rotations (30–60°/s). Target movement was produced with a pair of galvanometer-controlled mirrors mounted on the turntable. The animals were rewarded for fixation of the target using a sweetened milk mixture according to a variable reinforcement schedule. After training the monkeys were able to produce on-demand performance for sustained periods of 
5 h, three to four times per week. Eye and head movements were measured using a magnetic search-coil system mounted on the turntable. These signals were low-pass filtered (5–10 kHz) and sampled (200–500 Hz) at 16-bit resolution using a Cambridge Electronics 1401 data-acquisition system. Eye position was computed off-line as the difference between gaze and head position. Head- and gaze-velocity signals were created by digitally differentiating and filtering (low-pass smoothing, 20–50 Hz) the position signals.
Eye-head saccades with concomitant Pk cell activity were recorded both in the absence of a visual target, when the room lights were dim with the monkey facing the monochrome screen, and during periods of combined eye-head tracking of the target light when the monkey made adventitious eye-head saccades to re-acquire the target after looking away. Pk cell firing behavior was also recorded during ocular pursuit of the visual target, during head-restrained passive whole body rotation (WBR) when the visual target was stationary in space, and during head restrained WBR when the target was stationary with respect to the head. The activity of some Pk cells (14) was also recorded during passive head-on-trunk rotation generated by manual rotation of the axis rod and therefore the attached head (2.5–4 Hz, 200–400°/s) when the trunk was stationary in space. During forced head-on-trunk rotation the monkey sat either in darkness or in dim room light.
Purkinje cell recordings
Purkinje cell simple spike activity was recorded using tungsten microelectrodes (3–6 M
) and identified by the simultaneously recorded complex spike activity. Spike potentials were band-pass filtered (300 Hz to 8 kHz), and a dual window discriminator (Bak) was used to generate event input to the 1401 peripheral device (0.1-ms resolution) for storage in a personal computer. The spike events were converted into values of instantaneous firing frequency with a bin width that matched A/D acquisition (Gdowski and McCrea 1999).
Pk cells were selected for this study according to their responsiveness during horizontal ocular pursuit of the laser target (0.5 Hz, 40°/s peak velocity) and during VOR suppression (also at 0.5 Hz, 40°/s). Pk cells with greater responses during vertical pursuit were not usually responsive to horizontal pursuit stimuli and were not included in this study.
Location of recording sites
Recordings were obtained from the flocculus and ventral paraflocculus in a region extending 4 mm caudal from the rostral end of the ventral paraflocculus and 2–3 mm medial from the lateral edge of the FLR. We did not find qualitative differences in Pk cell activity during pursuit or VOR behaviors across the flocculus-ventral paraflocculus border (posterolateral fissure) (Belton and McCrea 2000a). The most salient anatomical landmark during recording was the presence of VIIIth nerve axons 300–500 µm ventral to the cerebellar cortex. In one monkey, the position and orientation of microelectrode tracts was confirmed histologically.
Data analysis
Analysis of Pk cell sensitivity to eye and head movements.
Pk cell sensitivity to eye velocity was assessed from the records of sinusoidal ocular pursuit (0.5 Hz, 40°/s). Their sensitivity to head velocity was assessed from the records made during sinusoidal WBR (0.5 Hz, 40°/s) in which the monkey suppressed the VOR by fixating a head stationary target. Cycles where the gaze was not within 2.5° of the visual target were discarded. Records from 20–100 selected cycles (mean = 26 at 0.5 Hz) were concatenated, desaccaded, cycle-averaged, and fit with sinusoidal functions. An iterative fitting technique was used to eliminate low firing frequency responses that deviated significantly from linearity during periods of inhibitory saturation (Chen-Huang et al. 1997). A significant minority of the Purkinje cells exhibited nonlinear responses during sinusoidal pursuit and VOR suppression that was not due to inhibitory saturation. In these cells, an estimate of sensitivity to eye and head movements was confined to the portion of the cycle in which the response was linearly related to the stimulus (Belton and McCrea 2000a; Lisberger et al. 1994a; Miles et al. 1980; Noda and Warabi 1982).
Analysis of PK cell responses during gaze saccade-related VOR. Pk cells were selected for analysis that had relatively large responses during the VOR evoked by passive whole body rotation or during ocular pursuit. Pk cells that generated bursts of spikes during ocular saccades or had very large eye position-related changes in firing rate were excluded from analysis due to the difficulty of separating saccade-related eye movement signals from signals related to the compensatory eye movement at the end of eye-head saccades.
Records of eye-head (gaze) saccades were grouped according to direction and amplitude and whether the saccades were made to or in the absence of a visual target. Only gaze saccades that had peak head velocities >20°/s were included in the analysis. Saccade records were averaged after aligning the records on the peak compensatory eye velocity at the end of the gaze shift. For the saccades made to a visual target, gaze position at saccade-end was required to be within 2° of the target for inclusion in the average.
The firing rate modulation recorded during the epoch of VOR at the end of gaze saccades was quantified using linear regression analysis. For each saccade-related VOR epoch, the firing rate observed during VOR eye movements was regressed against the modulation predicted from the cell's sensitivity to eye velocity measured during ocular pursuit, to eye position during steady fixation, and to head velocity during VOR cancellation. Firing rate modulation during saccade-related VOR eye movements was measured after subtracting the mean baseline firing rate within a 100-ms window that ended 30 ms before saccade onset. The eye-velocity sensitivity during the VOR related to gaze saccades was also calculated using linear regression analysis, where for each saccade the firing rate modulation during the VOR epoch was regressed against recorded eye velocity.
For purposes of illustration in this paper, averages of 7–14 saccades are aligned on peak compensatory eye velocity at the end of the gaze shift. The spike rasters associated with each saccade are illustrated above the averaged response histogram.
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RESULTS |
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FLR Pk cells insensitive to VOR evoked by active head movements during gaze saccades
Most (42/48) FLR Pk cells were insensitive to eye and head velocity during the VOR eye movements evoked during both ipsiversive and contraversive saccade-related head movements. This was true whether the saccades were spontaneously generated or made to the visual target. Figures 1 and 2 show the responses of an EV Pk cell and an EHV Pk cell during VOR eye movements related to active head movements during gaze saccades.
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Figure 1C plots the peak change in firing rate observed during the VOR related to individual gaze saccades versus the predicted change in firing rate expected from the cell's sensitivity to eye velocity during pursuit and passive VOR. The expected response if the cell was equally sensitivity to the VOR during passive and active head movements is represented by the dashed line. The linear regression of the observed sensitivity to saccade-related VOR is also shown (—). The slope of the regression was –0.03, which was not significantly different from zero. The probability that this cell was equally sensitive to passive and active VOR eye movements was <0.01 (Student's t-test, P < 0.01).
The EHV Pk cell illustrated in Fig. 2 was sensitive to ipsilateral head velocity during VOR cancellation (0.61 spikes/s per °/s, Fig. 2A2) as well as to eye velocity during ocular pursuit (1.43 spikes/s per °/s, Fig. 2A1). The cell was, however, like most EHV Pk cells in the FLR, more sensitive to eye velocity than it was to head velocity. The traces superimposed on the firing rate histograms in Fig. 2 are the responses expected based on the cells sensitivity to eye movements during pursuit and to passive head movements during suppression of the VOR. Although the two signals tend to cancel one another during the VOR, the cell's firing rate was still modulated during the VOR evoked by passive whole body rotation (Fig. 2A3) due to the much stronger sensitivity to eye velocity. On the other hand, the cell's firing rate was poorly modulated during gaze saccade-related VOR eye and head movements in both the eye movement on direction (2B1) and off direction (2B2. Figure 2C plots the peak change in firing rate observed during the VOR related to individual gaze saccades versus the predicted change in firing rate expected from the cell's sensitivity to eye velocity during pursuit and passive VOR. The slope of regression (0.06) was not significantly different from zero.
Pk cells that were insensitive to VOR eye movements evoked by active head-on-trunk rotations during gaze saccades were sensitive to VOR eye movements evoked by passive head-on-trunk rotation. Figure 3A shows the responses of an EHV Pk cell during high-frequency passive head-on-trunk rotation at 3.5 Hz. The cell's firing rate was modulated, although the response was smaller than that predicted from its responses during pursuit and VOR cancellation (trace superimposed on firing rate histogram), possibly because the cell received neck proprioceptive inputs or was sensitive to the absence of a visual target (Belton and McCrea 2000a; Gdowski et al. 2001). Figure 3B shows the cell's response during on direction saccade-related VOR eye movements the temporal duration of which was comparable to a half cycle of the passive head-on-trunk rotation stimulus (3.5 Hz) shown in Fig 3A. Figure 3C plots the change in firing rate of the cell during individual saccade-related VOR epochs versus predicted change in firing rate based on its sensitivity to passive head-on-trunk rotation. The slope of regression (0.024) was not significantly different from zero. Similar analysis was carried out in 13 other Pk cells. The mean sensitivity of all 14 Pk cells to VOR evoked by high-frequency passive head-on-trunk rotation was 0.39 ± 0.27 spikes/s per °/s, whereas their sensitivity to gaze saccade-related VOR evoked by comparable head movements was not significantly different from zero.
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Six EHV Pk cells generated bursts of spikes immediately after gaze shifts when the saccadic head movement produced VOR eye movements to the cell's on direction. The responses of one of them is shown in Fig. 4. The cell was sensitive to ipsilateral eye velocity during smooth pursuit eye movements (Fig. 4A1) and to ipsilateral head velocity during VOR cancellation (Fig. 4A2). During passive WBR, the firing rate of the cell was also strongly modulated (Fig. 4A3) because its sensitivity to VOR eye velocity was greater than its sensitivity to head velocity. Near the end of contraversive gaze saccades it generated a burst of spikes (Fig. 4B1). The burst began 81 ± 6 ms after the onset and 55 ± 12 ms prior to the end of saccades and continued as long as the active head movement and the compensatory eye movements were present. Because the EHV Pk cell was not sensitive to ocular saccades, the burst was presumably related to the active head movement component of the gaze shift and the VOR eye movements generated at the end of the saccade (defined in this case as the time at which the eye began to move opposite in direction to the saccade). The lines superimposed on the average firing rate histograms in Fig. 5B are the predicted firing rate of the cell based on its sensitivity to eye and head velocity during ocular pursuit and VOR cancellation. Each of the six EHV cells that were sensitive to gaze saccade head movements exhibited similar bursts. On average the beginning of the burst was 1.0 ± 13 (SD) ms after the end of the gaze saccade (which was the beginning of "rollback" or VOR eye movements). The latency to the beginning of VOR eye movements was, on average, 76 ± 11 ms after the onset of the gaze saccade.
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Figure 4C plots the change in the cells’ firing rate observed during the VOR during individual gaze saccades versus the predicted change in firing rate based on its sensitivity to eye velocity during pursuit and head velocity during VOR cancellation. Equal responsiveness during passive and active head movements is indicated by the dashed line. The slope of the linear regression for saccade-related VOR for 29 saccades in the cell's on direction was 1.3, although the correlation between expected and actual peak firing rate was weak (R2 = 0.43). The slope of the regression for 17 saccades in the cell's off direction was –0.17, which was not significantly different from zero.
Similarity of Purkinje cell gaze saccade-related responses in the presence and absence of visual targets
FLR Pk cells are often more sensitive to eye and head movements in the presence of a visual target than when a target is absent (Belton and McCrea 2000a; Fukushima et al. 1996; Ghelarducci et al. 1975). However, during saccade-related VOR, most FLR Pk cells were insensitive to the compensatory eye movements regardless of whether saccades were directed to a visual target or not. Figure 5 shows the firing behavior of an EHV Pk cell during the VOR evoked by passive WBR (Fig. 5A) and during saccade-related VOR generated in the absence (Fig. 5B1) and in the presence (Fig. 5B2) of a visual target. The traces superimposed over the firing rate histograms are the responses expected based on the cell's sensitivity to eye and head movements during ocular pursuit and VOR cancellation. The cell was insensitive to VOR eye movements related to gaze saccades both in the presence and in the absence of visual targets. Similar observations were made in 34 other Pk cells.
Population sensitivity of FLR Pk cells to saccade-related VOR eye movements
Considered as a population, FLR Pk cells were insensitive to saccade-related VOR eye movements. Figure 6A is a cumulative histogram of the responses of all the FLR Pk cells during individual saccade-related VOR eye movements. Pk cell response to each saccade-related VOR eye movement was calculated by linear regression of the change in firing rate versus predicted change in firing rate. Each value plotted is the estimated relative sensitivity of an individual Pk cell during a single saccade. Values <1.0 occurred when the change in firing rate was less than predicted. Values near zero correspond to no change in firing rate. Negative values were obtained when the cell's response was opposite in direction to that predicted. The mean relative sensitivity of FLR Pk cells during the 1,710 saccades included in this analysis was 0.07 ± 0.36. The thickness of the hatched bar plotted at 1.0 represents the average cycle-to-cycle variance (1 SD) in Pk cell responses during passive WBR.
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) (see above). The dashed diagonal line indicates equal sensitivity to VOR during passive and saccade-related head movements. Estimated in this manner, the sensitivity of FLR Pk cells to saccade-related VOR was attenuated by 97%. Considered together, the analyses in Fig. 6, A and B, suggest that the output of the FLR is attenuated by 
95% during on direction saccade-related VOR eye movements compared with its output during VOR eye movements evoked by passive rotation of the head. The small, residual sensitivity was due primarily to the six EHV Pk cells described above (indicated as square symbols in the plot). During off-direction saccade-related VOR eye movements the population response was not significantly different from zero. |
DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSREFERENCES |
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; Noda and Warabi 1986; Noda et al. 1981; Stone and Lisberger 1990). The firing rates of most Purkinje cells in the cerebellar flocculus region are modulated during the VOR when it is evoked by passive movement of the head (Belton and McCrea 2000a; De Zeeuw et al. 1995; Fukushima et al. 1996, 1999; Hirata and Highstein 2001). In the present study, we report that most of the FLR Pk cells whose firing rate was modulated during VOR eye movements evoked by passive head movements were insensitive to gaze saccade-related VOR. The observations provide further evidence that signal processing in the FLR related to VOR eye movements is strongly context contingent.
Figure 7 illustrates one possible way context contingent signal processing of vestibular and eye-movement-related signals in the FLR may be accomplished. The FLR receives mossy fiber inputs from flocculus projection neurons (FPN) in the vestibular nuclei that carry signals related to head velocity and from neurons in the nuclei of the paramedian tracts (NPT) and the prepositus nucleus that carry signals related to eye movements (Langer et al. 1985). These mossy fiber inputs indirectly influence the firing rate of FLR Pk cells via the granule cell–parallel fiber pathway. FLR Pk cells in turn modify signal processing in a subset of central VOR pathways. The signal processing in the granule cell–parallel fiber pathway is gated by Golgi cells. Eye- and head-movement signals related to gaze saccades could be gated out by Golgi cells that receive inputs from brain stem circuits related to saccade generation. The purpose of this circuitry would be to prevent the flocculus from modifying signal processing in VOR pathways during self-generated head movements when the behavioral goal is to shift gaze from one image to another rather than to stabilize an image on the retina. Future studies of the firing behavior of FLR Golgi cells during passive and active head movements should reveal whether this is the mechanism for context contingent signal processing in the FLR during gaze saccades.
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FLR Pk cells generate smooth pursuit eye-movement command signals and vestibular signals that are essential for modifying the gain of the VOR during passive head movements, but the output of the FLR is apparently less important for this function during active head movements. Inactivation of the FLR strongly affects the ability to suppress or enhance the VOR during passive head movements (Belton and McCrea 2000a; Takemori and Cohen 1974; Waespe and Cohen 1983; Zee et al. 1981; Zhang et al. 1995b) but has little effect on this ability during active smooth tracking head movements (Belton and McCrea 2000b). Saccade-related head movements are probably at least as common as passively evoked head movements, and the function of the VOR would appear to be equally important in each circumstance. But the comparatively weak modulation of the firing rate of FLR Pk cells during active head movements during gaze saccades suggests that this region of the cerebellum is less involved in maintaining gaze stability during and immediately after active gaze shifts than it is when the head is passively perturbed.
The FLR provides visual, and vestibular sensory reafferent feedback signals, oculomotor feedback signals and possibly predictive signals that help stabilize gaze during passive head perturbations (Kettner et al. 2002; Miles et al. 1980; Stone and Lisberger 1990). These signals presumably would also be useful for producing gaze stability immediately after saccadic head movements. So why is the flocculus less active during the VOR eye movements following gaze saccades? One possibility is that different neural circuits regulate the gain of the VOR in different behavioral circumstances. The flocculus appears to be primarily involved in modifying VOR eye movements produced by passive perturbations of the head. Other cerebellar circuits, e.g., the vermis-fastigial pathway, may play the crucial role in modifying the VOR during active head movements.
Conclusion
The output of the flocculus and ventral paraflocculus plays an essential role in modifying signal processing in VOR pathways so that images of interest remain stable on the retina. This image stabilizing signal is highly dependent on the behavioral context and is called on primarily when external forces unrelated to self-generated eye and head movements are the cause of image instability.
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FOOTNOTES |
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Address for reprint requests and other correspondence: R.A. McCrea, Dept. Neurobiology, Pharmacology and Physiology, University of Chicago, 5830 S. Ellis Ave., MC 0926, Chicago, IL 60637 (E-mail: tbelton2{at}uchicago.edu).
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSREFERENCES |
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, saccade-related VOR responses when a moving visual target was present. 
, changes in firing rate during saccade-related VOR when no target was present. Separate regressions (—) were done for ipsiversive, on direction saccadic VOR eye movements (positive values) and contraversive, off direction saccadic VOR eye movements. Conventions and abbreviations are the same as in 
