scholarly journals Temporal Firing Patterns of Purkinje Cells in the Cerebellar Ventral Paraflocculus During Ocular Following Responses in Monkeys II. Complex Spikes

1998 ◽  
Vol 80 (2) ◽  
pp. 832-848 ◽  
Author(s):  
Yasushi Kobayashi ◽  
Kenji Kawano ◽  
Aya Takemura ◽  
Yuka Inoue ◽  
Toshihiro Kitama ◽  
...  

Kobayashi, Yasushi, Kenji Kawano, Aya Takemura, Yuka Inoue, Toshihiro Kitama, Hiroaki Gomi, and Mitsuo Kawato. Temporal firing patterns of Purkinje cells in cerebellar ventral paraflocculus during ocular following responses in monkeys. II. Complex spikes. J. Neurophysiol. 80: 832–848, 1998. Many theories of cerebellar motor learning propose that complex spikes (CS) provide essential error signals for learning and modulate parallel fiber inputs that generate simple spikes (SS). These theories, however, do not satisfactorily specify what modality is represented by CS or how information is conveyed by the ultra-low CS firing rate (1 Hz). To further examine the function of CS and the relationship between CS and SS in the cerebellum, CS and SS were recorded in the ventral paraflocculus (VPFL) of awake monkeys during ocular following responses (OFR). In addition, a new statistical method using a generalized linear model of firing probability based on a binomial distribution of the spike count was developed for analysis of the ultra-low CS firing rate. The results of the present study showed that the spatial coordinates of CS were aligned with those of SS and the speed-tuning properties of CS and SS were more linear for eye movement than retinal slip velocity, indicating that CS contain a motor component in addition to the sensory component identified in previous studies. The generalized linear model to reproduce firing probability confirmed these results, demonstrating that CS conveyed high-frequency information with its ultra-low firing frequency and conveyed both sensory and motor information. Although the temporal patterns of the CS were similar to those of the SS when the sign was reversed and magnitude was amplified ∼50 times, the velocity/acceleration coefficient ratio of the eye movement model, an aspect of the CS temporal firing profile, was less than that of the SS, suggesting that CS were more sensory in nature than SS. A cross-correlation analysis of SS that are triggered by CS revealed that short-term modulation, that is, the brief pause in SS caused by CS, does not account for the reciprocal modulation of SS and CS. The results also showed that three major aspects of the CS and SS individual cell firing characteristics were negatively correlated on a cell-to-cell basis: the preferred direction of stimulus motion, the mean percent change in firing rate induced by upward stimulus motion, and patterns of temporal firing probability. These results suggest that CS may contribute to long-term interactions between parallel and climbing fiber inputs, such as long-term depression and/or potentiation.

1998 ◽  
Vol 80 (2) ◽  
pp. 818-831 ◽  
Author(s):  
Hiroaki Gomi ◽  
Munetaka Shidara ◽  
Aya Takemura ◽  
Yuka Inoue ◽  
Kenji Kawano ◽  
...  

Gomi, Hiroaki, Munetaka Shidara, Aya Takemura, Yuka Inoue, Kenji Kawano, and Mitsuo Kawato. Temporal firing patterns of Purkinje cells in the cerebellar ventral paraflocculus during ocular following responses in monkeys. I. Simple spikes. J. Neurophysiol. 80: 818–831, 1998. The simple-spike firing frequency of 30 Purkinje cells (P cells) in the ventral paraflocculus (VPFL) of alert monkeys was studied in relation to vertical slow eye movements, termed ocular following response (OFR), induced by large-field visual motions of different velocities and durations. To quantitatively analyze the relationship between eye movement and firing frequency, an inverse dynamics representation of the eye movement was used for reconstructing the temporal waveform of firing. Coefficients of eye-acceleration, velocity, and position, bias, and time lag between firing and eye movement were estimated by least-square error method. In the regression analyses for each stimulus condition, 86% (146/170) of the well-modulated temporal firing patterns taken from those 30 P cells were reconstructed successfully from eye movement. The model with acceleration, velocity, and position terms, which we used, was shown as the best among several potential models by Cp statistics, consistent with t-test of significance of each term. Reliable coefficients were obtained from 75% (109/146) of the well-reconstructed firing patterns of 28 cells among 30. The estimated coefficients were larger (statistically significant) for slow stimuli than for fast stimuli, suggesting changes in sensitivities under different conditions. However, firing patterns of each cell under several different conditions were frequently well reconstructed by an inverse dynamics representation with a single set of coefficients (13 cells among 21). This indicates that the relationships between P cell firing and OFR are roughly linear in those stimulus ranges. The estimated coefficients for acceleration and velocity suggested that the VPFL P cells properly encode the dynamic components of the motor command during vertical OFR. As for the positional component, however, these P cells are correlated with eye movement in the opposite direction. In the regression analysis without positional component, remarkable differences between observed and reconstructed firing patterns were noted especially in the initial phase of the movements, indicating that the negative positional component was not negligible during OFR. Thus we conclude that, during OFR, the VPFL P cells cannot provide the necessary final motor command, and other brain regions, downstream neural structures, or other types of P cells must provide lacking position-dependent motor commands. This finding about the negative correlation with the position is in the opposite sign with previous studies obtained from the fixation and the smooth pursuit movement. From these comparisons, how the VPFL contributes to a part of the final motor command or how other brain regions complement the VPFL is suggested to be different for early and late phases of the movements.


1997 ◽  
Vol 28 ◽  
pp. S195 ◽  
Author(s):  
Kenji Yamamoto ◽  
Yasushi Kobayashi ◽  
Aya Takemura ◽  
Kenji Kawano ◽  
Mitsuo Kawato

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)


1994 ◽  
Vol 72 (2) ◽  
pp. 954-973 ◽  
Author(s):  
S. G. Lisberger ◽  
T. A. Pavelko ◽  
H. M. Bronte-Stewart ◽  
L. S. Stone

1. We made extracellular recordings from Purkinje cells in the flocculus and ventral paraflocculus of awake monkeys before and after motor learning in the vestibuloocular reflex (VOR). Three samples were recorded 1) after miniaturizing spectacles had reduced the gain of the VOR (eye speed divided by head speed) to 0.4; 2) when the gain of the VOR was near 1.0; and 3) after magnifying spectacles had increased the gain of the VOR to 1.6. 2. We studied Purkinje cells that showed stronger modulation of simple-spike firing rate during horizontal than during vertical pursuit. These cells corresponded to the previously identified “horizontal gaze velocity Purkinje cells” or HGVP-cells. During pursuit of smooth target motion with the head stationary, HGVP-cells showed strong modulation of firing rate with increases for ipsiversive eye motion (toward the side of recording). When the monkey canceled his VOR by tracking a target that moved exactly with him during sinusoidal head rotation in the horizontal plane, HGVP-cells again showed strong modulation of firing rate with increases for ipsiversive head motion. 3. The responses of HGVP-cells during pursuit with the head stationary and during cancellation of the VOR reveal separate components of firing rate related to eye and head velocity. We used these two behavioral conditions to test for effects of motor learning on the head and eye velocity components of the simple-spike firing of HGVP-cells. Our data confirm the previous observation that motor learning causes the sensitivity to head velocity to be larger when the gain of the VOR is high and smaller when the gain of the VOR is low. Thus we agree with the previous conclusion that changes in the vestibular sensitivity of HGVP-cells, measured during sinusoidal head motion at low frequencies, are in the wrong direction to cause changes in the gain of the VOR. 4. To determine whether the simple-spike output from the HGVP-cells plays a role in the VOR after motor learning, we recorded simple-spike firing during the VOR evoked by transient, rapid changes in head velocity in darkness. When the gain of the VOR was low, firing rate increased during the VOR evoked by ipsiversive head motion and decreased during the VOR evoked by contraversive head motion. When the gain of the VOR was high, the direction selectivity of the responses was reversed.(ABSTRACT TRUNCATED AT 400 WORDS)


1994 ◽  
Vol 72 (4) ◽  
pp. 2045-2050 ◽  
Author(s):  
R. J. Krauzlis ◽  
S. G. Lisberger

1. We recorded the simple spike firing rate of gaze velocity Purkinje cells (GVP-cells) in the flocculus/ventral paraflocculus of two monkeys during the smooth pursuit eye movements evoked by a target that was initially at rest, started suddenly, moved at a constant velocity, and then stopped. 2. For target motion in the preferred direction, GVP-cells showed a large transient increase in firing rate at the onset of pursuit, a smaller but sustained increase during the maintenance of pursuit, and a smooth return to baseline firing with little undershoot at the offset of pursuit. For target motion in the nonpreferred direction, GVP-cells showed a small decrease in firing rate at the onset of pursuit, a similar sustained decrease during the maintenance of pursuit, but a large transient increase in firing rate at the offset of pursuit before returning to baseline firing. 3. We pooled the data in our sample of horizontal GVP-cells by subtracting the population average of firing rate recorded during pursuit in the nonpreferred direction from the population average recorded during pursuit in the preferred direction. We transformed this net population average by passing it through a model of the brain stem final common pathway and the oculomotor plant. This yielded a signal that closely matched the observed trajectory of eye velocity during pursuit. We conclude that the transient overshoots exhibited in the firing rate of GVP-cells can provide appropriate compensation for the lagging dynamics of the oculomotor plant.


1999 ◽  
Vol 82 (5) ◽  
pp. 2612-2632 ◽  
Author(s):  
Pierre A. Sylvestre ◽  
Kathleen E. Cullen

The mechanics of the eyeball and its surrounding tissues, which together form the oculomotor plant, have been shown to be the same for smooth pursuit and saccadic eye movements. Hence it was postulated that similar signals would be carried by motoneurons during slow and rapid eye movements. In the present study, we directly addressed this proposal by determining which eye movement–based models best describe the discharge dynamics of primate abducens neurons during a variety of eye movement behaviors. We first characterized abducens neuron spike trains, as has been classically done, during fixation and sinusoidal smooth pursuit. We then systematically analyzed the discharge dynamics of abducens neurons during and following saccades, during step-ramp pursuit and during high velocity slow-phase vestibular nystagmus. We found that the commonly utilized first-order description of abducens neuron firing rates (FR = b + kE + rE˙, where FR is firing rate, E and E˙ are eye position and velocity, respectively, and b, k, and r are constants) provided an adequate model of neuronal activity during saccades, smooth pursuit, and slow phase vestibular nystagmus. However, the use of a second-order model, which included an exponentially decaying term or “slide” (FR = b + kE + rE˙ + uË − c[Formula: see text]), notably improved our ability to describe neuronal activity when the eye was moving and also enabled us to model abducens neuron discharges during the postsaccadic interval. We also found that, for a given model, a single set of parameters could not be used to describe neuronal firing rates during both slow and rapid eye movements. Specifically, the eye velocity and position coefficients ( r and k in the above models, respectively) consistently decreased as a function of the mean (and peak) eye velocity that was generated. In contrast, the bias ( b, firing rate when looking straight ahead) invariably increased with eye velocity. Although these trends are likely to reflect, in part, nonlinearities that are intrinsic to the extraocular muscles, we propose that these results can also be explained by considering the time-varying resistance to movement that is generated by the antagonist muscle. We conclude that to create realistic and meaningful models of the neural control of horizontal eye movements, it is essential to consider the activation of the antagonist, as well as agonist motoneuron pools.


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