Anatomy and Discharge Properties of Pre-Motor Neurons in the Goldfish Medulla That Have Eye-Position Signals During Fixations

2000 ◽  
Vol 84 (2) ◽  
pp. 1035-1049 ◽  
Author(s):  
E. Aksay ◽  
R. Baker ◽  
H. S. Seung ◽  
D. W. Tank

Previous work in goldfish has suggested that the oculomotor velocity-to-position neural integrator for horizontal eye movements may be confined bilaterally to a distinct group of medullary neurons that show an eye-position signal. To establish this localization, the anatomy and discharge properties of these position neurons were characterized with single-cell Neurobiotin labeling and extracellular recording in awake goldfish while monitoring eye movements with the scleral search-coil method. All labeled somata ( n = 9) were identified within a region of a medially located column of the inferior reticular formation that was ∼350 μm in length, ∼250 μm in depth, and ∼125 μm in width. The dendrites of position neurons arborized over a wide extent of the ventral half of the medulla with especially heavy ramification in the initial 500 μm rostral of cell somata ( n = 9). The axons either followed a well-defined ventral pathway toward the ipsilateral abducens ( n = 4) or crossed the midline ( n = 2) and projected toward the contralateral group of position neurons and the contralateral abducens. A mapping of the somatic region using extracellular single unit recording revealed that position neurons ( n > 120) were the dominant eye-movement-related cell type in this area. Position neurons did not discharge below a threshold value of horizontal fixation position of the ipsilateral eye. Above this threshold, firing rates increased linearly with increasing temporal position [mean position sensitivity = 2.8 (spikes/s)/°, n = 44]. For a given fixation position, average rates of firing were higher after a temporal saccade than a nasal one ( n = 19/19); the magnitude of this hysteresis increased with increasing position sensitivity. Transitions in firing rate accompanying temporal saccades were overshooting ( n = 43/44), beginning, on average, 17.2 ms before saccade onset ( n = 17). Peak firing rate change accompanying temporal saccades was correlated with eye velocity ( n = 36/41). The anatomical findings demonstrate that goldfish medullary position neurons have somata that are isolated from other parts of the oculomotor system, have dendritic fields overlapping with axonal terminations of neurons with velocity signals, and have axons that are capable of relaying commands to the abducens. The physiological findings demonstrate that the signals carried by position neurons could be used by motoneurons to set the fixation position of the eye. These results are consistent with a role for position neurons as elements of the velocity-to-position neural integrator for horizontal eye movements.

1988 ◽  
Vol 60 (6) ◽  
pp. 1874-1895 ◽  
Author(s):  
A. F. Fuchs ◽  
C. A. Scudder ◽  
C. R. Kaneko

1. Single neurons in the abducens nucleus were recorded extracellularly in alert rhesus macaques trained to make a variety of eye movements. An abducens neurons was identified as a motoneuron (MN) if its action potentials triggered an averaged EMG potential in the lateral rectus muscle. Abducens internuclear neurons (INNs) that project to the oculomotor nucleus were identified by collision block of spontaneous with antidromic action potentials evoked with a stimulating electrode placed in the medial rectus subdivision of the contralateral oculomotor nucleus. 2. All abducens MNs and INNs had qualitatively similar discharge patterns consisting of a burst of spikes for lateral saccades and a steady firing whose rate increased with lateral eye position in excess of a certain threshold. 3. For both MNs and INNs the firing rates associated with different, constant eye positions could be described accurately by a straight line with slope, K (the eye position sensitivity in spikes.s-1.deg-1), and intercept, T (the eye position threshold for steady firing). For different MNs, K increased as T varied from more medial to more lateral values. In contrast, the majority of INNs already were active for values of T more medial than 20 degrees and showed little evidence of recruitment according to K. 4. During horizontal sinusoidal smooth-pursuit eye movements, both MNs and INNs exhibited a sinusoidal modulation in firing rate whose peak preceded eye position. From these firing rate patterns, the component of firing rate related to eye velocity, R (the eye velocity sensitivity in spikes.s-1.deg-1.s-1), was determined. The R for INNs was, on average, 78% larger than that for MNs. Furthermore, R increased with T for MNs, whereas INNs showed no evidence of recruitment according to R. If, as in the cat, the INNs of monkeys provide the major input to medial rectus MNs and if simian medial rectus MNs behave like our abducens MNs, then recruitment order, which is absent in INNs, must be established at the MN pool itself. 5. Unexpectedly, the R of MNs decreased with the frequency of the smooth-pursuit movement. Furthermore, the eye position sensitivity, K, obtained during steady fixations was usually less than that determined during smooth pursuit. Therefore, conclusions about the roles of MNs and premotor neurons based on how their R and K values differ must be viewed with caution if the data have been obtained under different tracking conditions.(ABSTRACT TRUNCATED AT 400 WORDS)


1991 ◽  
Vol 66 (6) ◽  
pp. 2125-2140 ◽  
Author(s):  
A. M. Pastor ◽  
B. Torres ◽  
J. M. Delgado-Garcia ◽  
R. Baker

1. The discharge of antidromically identified medial rectus and abducens motoneurons was recorded in restrained unanesthesized goldfish during spontaneous eye movements and in response to vestibular and optokinetic stimulation. 2. All medial rectus and abducens motoneurons exhibited a similar discharge pattern. A burst of spikes accompanied spontaneous saccades and fast phases during vestibular and optokinetic nystagmus in the ON-direction. Firing rate decreased for the same eye movements in the OFF-direction. All units showed a steady firing rate proportional to eye position beyond their recruitment threshold. 3. Motoneuronal position (ks) and velocity (rs) sensitivity for spontaneous eye movements were calculated from the slope of the rate-position and rate-velocity linear regression lines, respectively. The averaged ks and rs values of medial rectus motoneurons were higher than those of abducens motoneurons. The differences in motoneuronal sensitivity coupled with structural variations in the lateral versus the medial rectus muscle suggest that symmetric nasal and temporal eye movements are preserved by different motor unit composition. Although the abducens nucleus consists of distinct rostral and caudal subgroups, mean ks and rs values were not significantly different between the two populations. 4. Every abducens and medial rectus motoneuron fired an intense burst of spikes during its corresponding temporal or nasal activation phase of the "eye blink." This eye movement consisted of a sequential, rather than a synergic, contraction of both vertical and horizontal extraocular muscles. The eye blink could act neither as a protective reflex nor as a goal-directed eye movement because it could not be evoked in response to sensory stimuli. We propose a role for the blink in recentering eye position. 5. Motoneuronal firing rate after ON-directed saccades decreased exponentially before reaching the sustained discharge proportional to the new eye position. Time constants of the exponential decay ranged from 50 to 300 ms. Longer time constants after the saccade were associated with backward drifts of eye position and shorter time constants with onward drifts. These postsaccadic slide signals are suggested to encode the transition of eye position to the new steady level. 6. Motoneurons modulated sinusoidally in response to sinusoidal head rotation in the dark, but for a part of the cycle they went into cutoff, dependent on their eye position recruitment threshold. Eye position (kv) and velocity (rv) sensitivity during vestibular stimulation were measured at frequencies between 1/16 and 2 Hz. Motoneuronal time constants (tau v = rv/kv) decreased on the average by 25% with the frequency of vestibular stimulation.(ABSTRACT TRUNCATED AT 400 WORDS)


1995 ◽  
Vol 74 (1) ◽  
pp. 273-287 ◽  
Author(s):  
T. Kitama ◽  
Y. Ohki ◽  
H. Shimazu ◽  
M. Tanaka ◽  
K. Yoshida

1. Extracellular spikes of burster-driving neurons (BDNs) were recorded within and immediately below the prepositus hypoglossi nucleus in the alert cat. BDNs were characterized by short-latency activation after stimulation of the contralateral vestibular nerve (latency: 1.4-2.7 ms) and the ipsilateral superior colliculus (latency: 1.7-3.5 ms). Convergence of vestibular and collicular inputs was found in all of 85 BDNs tested. Firing of BDNs increased during contralateral horizontal head rotation and decreased during ipsilateral rotation. A burst of spikes was induced in association with contralateral saccades and quick phases of nystagmus. 2. BDNs showed irregular tonic discharges during fixation. There was no significant correlation between the firing rate during fixation and horizontal or vertical eye position in most BDNs. During horizontal sinusoidal head rotation, the change in firing rate was approximately proportional to and in phase with contralateral head velocity. The phase lag of the response relative to head angular velocity was 13.8 +/- 20.1 degrees (mean +/- SD) at 0.5 Hz and 7.2 +/- 13.5 degrees at 0.2 Hz on the average. The gain was 0.88 +/- 0.25 (spikes/s)/(degrees/s) at 0.5 Hz and 1.19 +/- 0.49 (spikes/s)/(degrees/s) at 0.2 Hz. 3. Quantitative analysis of burst activity associated with saccades or quick phases indicated that the ON direction of BDNs was contralateral horizontal. The number of spikes in the burst was linearly related to the amplitude of the contralateral component of rapid eye movements. The slope of regression line was, on the average, 1.14 +/- 0.48 spikes/deg. There was no significant difference between the mean slopes for saccades and quick phases. The number of spikes depended on the difference between initial and final horizontal eye positions and not on the absolute eye position in the orbit. The mean burst firing rate was proportional to the mean velocity of the contralateral component of rapid eye movements. The slope of the regression line was 0.82 +/- 0.34 (spikes/s)/(degrees/s). Significant correlation was also found between intraburst instantaneous firing rate and instantaneous component eye velocity. 4. Objects presented in the contralateral visual field elicited a brief burst of spikes in BDNs independent of any eye movement. Contralateral saccades to the target were preceded by an early response to the visual stimulus and subsequent response associated with eye movement. 5. Excitation of BDNs produced by stimulation of the ipsilateral superior colliculus was facilitated by contralateral horizontal head rotation. Therefore saccadic signals from the superior colliculus to BDNs may be augmented by vestibular signals during head rotation.(ABSTRACT TRUNCATED AT 400 WORDS)


1994 ◽  
Vol 72 (6) ◽  
pp. 2754-2770 ◽  
Author(s):  
E. L. Keller ◽  
J. A. Edelman

1. We recorded the spatial and temporal dynamics of saccade-related burst neurons (SRBNs) found in the intermediate layers of the superior colliculus (SC) in the alert, behaving monkey. These burst cells are normally the first neurons recorded during radially directed microelectrode penetrations of the SC after the electrode has left the more dorsally situated visual layers. They have spatially delimited movement fields whose centers describe the well-studied motor map of the SC. They have a rather sharp, saccade-locked burst of activity that peaks just before saccade onset and then declines steeply during the saccade. Many of these cells, when recorded during saccade trials, also have an early, transient visual response and an irregular prelude of presaccadic activity. 2. Because saccadic eye movements normally have very stereotyped durations and velocity trajectories that vary systematically with saccade size, it has been difficult in the past to establish quantitatively whether the activity of SRBNs temporally codes dynamic saccadic control signals, e.g., dynamic motor error or eye velocity, where dynamic motor error is defined as a signal proportional to the instantaneous difference between desired final eye position and the actual eye position during a saccade. It has also not been unequivocally established whether SRBNs participate in an organized spatial shift of ensemble activity in the intermediate layers of the SC during saccadic eye movements. 3. To address these issues, we studied the activity of SRBNs using an interrupted saccade paradigm. Saccades were interrupted with pulsatile electrical stimulation through a microelectrode implanted in the omnipauser region of the brain stem while recordings were made simultaneously from single SRBNs in the SC. 4. Shortly after the beginning of the stimulation (which was electronically triggered at saccade onset), the eyes decelerated rapidly and stopped completely. When the high-frequency (typically 300-400 pulses per second) stimulation was terminated (average duration 12 ms), the eye movement was reinitiated and a resumed saccade was made accurately to the location of the target. 5. When we recorded from SRBNs in the more caudal colliculus, which were active for large saccades, cell discharge was powerfully and rapidly suppressed by the stimulation (average latency = 3.8 ms). Activity in the same cells started again just before the onset of the resumed saccade and continued during this saccade even though it has a much smaller amplitude than would normally be associated with significant discharge for caudal SC cells.(ABSTRACT TRUNCATED AT 400 WORDS)


1986 ◽  
Vol 56 (4) ◽  
pp. 1129-1146 ◽  
Author(s):  
H. Noda ◽  
A. Mikami

Extracellular recordings were obtained from 319 input units and 304 Purkinje cells (P-cells) in the dorsal paraflocculus of alert monkeys trained to fixate a visual target. They changed discharge rates with either eye movement, eye position, or visual stimulus movement. Of the 319 input units, recorded in the granular layer or white matter, most were mossy fibers (MFs), but 90 (28%) showed characteristic cellular spikes. The latter units were probably granular cells (p-GC). Of the 319 input units, 163 (51%) showed bursts with saccades (burst units) and 62 (19%) showed a prelude on the average 124 ms prior to the onset of saccade (long-lead burst units). Sixty-five (20%) had tonic activity related to eye position and also showed bursts with saccades (burst-tonic units), and the remaining 29 (9%) showed only tonic activity (tonic units). MFs and p-GCs showed no significant differences in the proportion of each type of unit or in their response properties. The majority of burst units (63%) were pan directional, whereas all long-lead burst units had directional selectivity. The preferred directions of long-lead burst, burst tonic, and directionally selective burst units were found in all four quadrants. Position-related activity was found in 48% of the burst-tonic and tonic units to be linearly related to eye position and to show position threshold. The other units also had position thresholds but their activity was not monotonically related to fixation position. Six climbing fibers (CFs), 32 input units (including 13 p-GC), and 8 P-cells showed cyclic responses during sinusoidal movements of a visual pattern. One class of MF units (57%) responded only to the direction, whereas the others responded to both the direction and retinal-slip velocity. Both CF and P-cell units responded to sinusoidal retinal-slip velocity. Of 67 input units, 23 showed cyclic modulation in firing during sinusoidal eye movements in the horizontal plane. Nineteen were burst-tonic and four were tonic units. They also showed position sensitivity. The phase of the cyclic responses tended to lag behind the eye velocity during low-frequency trackings. Of 237 P-cells, 163 (68.8%) discharged with saccades (burst P-cells), 42 (17.7%) paused with saccades (pause P-cells), and 32 (13.5%) discharged with saccades in one direction and paused in the other (burst-pause P-cells). Position sensitivity was found in 38 P-cells; 12 were burst, 5 were pause, and 10 were burst-pause P-cells. Eleven did not respond with saccades.(ABSTRACT TRUNCATED AT 400 WORDS)


1990 ◽  
Vol 63 (4) ◽  
pp. 902-917 ◽  
Author(s):  
Y. Iwamoto ◽  
T. Kitama ◽  
K. Yoshida

1. The firing characteristics and projection patterns of secondary vestibular nucleus neurons involved in the vertical vestibuloocular pathways were investigated in alert cats. Single-unit recordings were made in the medial longitudinal fasciculus (MLF) near the trochlear nucleus from axons that were monosynaptically activated after electrical stimulation of the vestibular nerve. In a total of 253 identified secondary neurons, 225 discharged in relation to vertical eye movements; 189 of these increased their firing rate for downward eye movements and 36 for upward movements. The activity of the remaining 28 axons was not related to eye movements when the head was still. 2. Virtually all of the secondary neurons with downward on-direction displayed tonic activity that was primarily related to steady eye position during fixation (DPV neurons). The slope of the relationship between firing rate and vertical eye position ranged from 1.2 to 9.1 (spikes/s)/deg with a mean of 3.2 (spikes/s)/deg. The regularity of firing was quantified by calculating the coefficient of variation (CV) of interspike intervals. A comparison of the CV in the population units indicated that DPV neurons could be classified as either regular or irregular neurons. There was a tendency for regular neurons to have higher firing rates and higher correlation coefficients for the rate-position relationships than irregular neurons. 3. During pitch rotation in the light, all the DPV neurons tested increased their firing rate with upward head rotation. Both the phase and the amplitude of the response indicated that DPV neurons discharged not only in relation to eye position but also in relation to head velocity, suggesting that they received monosynaptic input from the posterior semicircular canal. The gain and phase lag of the response relative to head velocity were measured at 0.5 Hz. The range of the gain was 1.1-5.1 (spikes/s)/(deg/s), and that of the phase lag was 18.3-62.4 degrees. There was a tendency for irregular DPV neurons to have a larger gain and smaller phase lag than regular DPV neurons. 4. Ascending and descending projection pathways were determined for 147 DPV axons. Of these, 69 ascended in the contralateral MLF with respect to their soma (crossed-DPV axons), and 78 in the ipsilateral MLF (uncrossed-DPV axons), as revealed by their monosynaptic activation from the contralateral or ipsilateral vestibular nerve. Stimulation of the caudal MLF at the level of the obex evoked direct responses caused by antidromic activation of descending collaterals in approximately 70% (49/69) of the crossed-DPV axons.(ABSTRACT TRUNCATED AT 400 WORDS)


2011 ◽  
Vol 105 (2) ◽  
pp. 896-909 ◽  
Author(s):  
Owen Debowy ◽  
Robert Baker

Monocular organization of the goldfish horizontal neural integrator was studied during spontaneous scanning saccadic and fixation behaviors. Analysis of neuronal firing rates revealed a population of ipsilateral (37%), conjugate (59%), and contralateral (4%) eye position neurons. When monocular optokinetic stimuli were employed to maximize disjunctive horizontal eye movements, the sampled population changed to 57, 39, and 4%. Monocular eye tracking could be elicited at different gain and phase with the integrator time constant independently modified for each eye by either centripetal (leak) or centrifugal (instability) drifting visual stimuli. Acute midline separation between the hindbrain oculomotor integrators did not affect either monocularity or time constant tuning, corroborating that left and right eye positions are independently encoded within each integrator. Together these findings suggest that the “ipsilateral” and “conjugate/contralateral” integrator neurons primarily target abducens motoneurons and internuclear neurons, respectively. The commissural pathway is proposed to select the conjugate/contralateral eye position neurons and act as a feedfoward inhibition affecting null eye position, oculomotor range, and saccade pattern.


1994 ◽  
Vol 72 (2) ◽  
pp. 909-927 ◽  
Author(s):  
S. G. Lisberger ◽  
T. A. Pavelko ◽  
D. M. Broussard

1. We have identified a group of brain stem cells called “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 strong modulation during 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 infection 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.(ABSTRACT TRUNCATED AT 250 WORDS)


1984 ◽  
Vol 52 (4) ◽  
pp. 743-761 ◽  
Author(s):  
L. E. Mays ◽  
J. D. Porter

Single<unit recordings were made from neurons with horizontal eye position sensitivity in the oculomotor and abducens nuclei in alert monkeys. The animals were trained to perform a visual tracking task that resulted in conjugate eye movements or symmetrical vergence movements. Scatterplots were obtained for unit firing rate as a function of the position of the ipsilateral eye for both types of movement. The slopes of the linear regression line were computed for conjugate (kc) and vergence movements (kv). Previous recording studies implied that kv should be equal to kc for most, if not all, abducens and oculomotor neurons. Other lines of evidence suggested that kv should be zero for a substantial proportion of abducens neurons. In the abducens nucleus, we found some cells for which kv matched kc, and a few cells with a kv value of zero. However, the majority of abducens units had vergence signals that were neither equal to zero nor to their conjugate signals. Overall, kv/kc was 0.62, and the correlation between kv and kc was not significantly different from zero. Similarly, in the oculomotor nucleus, kv was significantly different from kc for a majority of the cells. A few units had kv values less than or equal to zero, whereas other cells had very high kv values. Overall, the kv/kc for oculomotor units was nearly unity (0.94), and the correlation between kv and kc was 0.31. These results confirm previous reports that most neurons in the abducens and oculomotor nuclei with a horizontal eye position sensitivity carry both conjugate and vergence eye movement signals. We do not find that the relative magnitudes of these signals are closely matched for most neurons. It is more likely that vergence and conjugate signals are matched globally, for an entire nucleus, rather than for individual motoneurons. This view is consistent with the hypothesis that conjugate and vergence signals are generated independently and combined for the first time at the motoneurons. Our results also imply that some motoneurons play a more important role than others in either vergence or conjugate movements.


1996 ◽  
Vol 76 (3) ◽  
pp. 1759-1774 ◽  
Author(s):  
G. Cheron ◽  
M. Escudero ◽  
E. Godaux

1. The aim of this study was to characterize the signals transmitted by neurons of the medial vestibular nucleus (MVN) to the middle zone of the flocculus in alert cats. 2. Bipolar stimulating electrodes were implanted into the middle zone of each flocculus, because this zone is known to be involved in the control of horizontal eye movements. Correct implantation of the stimulating electrodes was ensured by 1) recording of Purkinje cells whose activity was related to horizontal eye movements and 2) elicitation of slow abduction of the ipsilateral eye upon electrical stimulation. 3. The rostral two-thirds of the MVN were investigated by microelectrodes during stimulation of both flocculi. Antidromically activated neurons were found only in the central part of the explored area. Forty-four units were activated from the contralateral, eight from the ipsilateral flocculus. Neurons could never be activated from both flocculi. 4. Neurons included in this study were MVN neurons that had 1) to be antidromically activated from one flocculus and 2) to modulate their firing rate during the horizontal vestibuloocular reflex (VOR) elicited by sinusoidal stimulation (0.1 Hz; 10, 20, 30 or 40 degrees). The 39 neurons matching both criteria were classified in 2 groups: 22 neurons changed their firing rate during spontaneous horizontal eye movements (EM-neurons), 17 modulated their activity only during head rotation and were labeled vestibular-only neurons (VO-neurons). 5. Sufficient data were obtained from 13 EM-neurons to allow a quantitative analysis. Among those, 12 were activated from the contralateral and 1 from the ipsilateral flocculus. Their sensitivity to horizontal eye position during intersaccadic fixation was 3.54 +/- 2.75 (SD) spikes.s-1/deg. Eight EM-neurons behaved as type I neurons, five as type II neurons. During the slow phases of the VOR, all of these neurons combined some head-velocity sensitivity (1.50 +/- 0.43 spikes.s-1/deg.s-1) with some horizontal eye-position sensitivity (3.61 +/- 2.45 spikes.s-1/deg). Additionally, seven of these neurons presented a sensitivity to eye velocity (1.34 +/- 0.55 spikes.s-1/deg.s-1). The phase difference between the modulation of firing rate and eye position varied substantially between neurons. The observed phase lead with respect to eye position ranged from 2 to 110 degrees (41.9 +/- 31.8 degrees). 6. Sufficient data were obtained from 10 VO-neurons to allow a quantitative analysis. Among those, nine were activated from the contralateral and one from the ipsilateral flocculus. All of these neurons behaved as type I neurons. The sensitivity to head velocity was 1.64 +/- 1.07 spikes.s-1/deg.s-1. The phase lead of the modulation of spike activity with respect to head velocity ranged from 4.5 to 30.5 degrees (16.4 +/- 8.9 degrees). 7. We conclude that the MVN provides the horizontal zone of the flocculus (with a strong contralateral preference) with information about head velocity (through VO-neurons and EM-neurons) and about eye velocity and position (through EM-neurons).


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