Anatomy and Physiology of the Primate Interstitial Nucleus of Cajal. II. Discharge Pattern of Single Efferent Fibers

1998 ◽  
Vol 80 (6) ◽  
pp. 3100-3111 ◽  
Author(s):  
Y. Dalezios ◽  
C. A. Scudder ◽  
S. M. Highstein ◽  
A. K. Moschovakis
Keyword(s):  
Smooth Pursuit ◽  
Discharge Pattern ◽  
Eye Position ◽  
Interstitial Nucleus Of Cajal ◽  
Anatomy And Physiology ◽  
Saccade Size ◽  
Saccade Velocity ◽  
Behaving Monkeys ◽  
Eye Velocity ◽  
Vertical Up

Dalezios, Y., C. A. Scudder, S. M. Highstein, and A. K. Moschovakis. Anatomy and physiology of the primate interstitial nucleus of Cajal. II. Discharge pattern of single efferent fibers. J. Neurophysiol. 80: 3100–3111, 1998. Single efferent fibers of the interstitial nucleus of Cajal (NIC) were characterized physiologically and injected with biocytin in alert behaving monkeys. Quantitative analysis demonstrated that their discharge encodes a constellation of oculomotor variables. Tonic and phasic signals were related to vertical (up or down) eye position and saccades, respectively. Depending on how they encoded eye position, saccade velocity, saccade size, saccade duration, and smooth-pursuit eye velocity, fibers were characterized as regular or irregular, bi- or unidirectionally modulated, more or less sensitive, and reliable or unreliable. Further, fibers that did not burst for saccades (tonic) and fibers the eye-position and saccade-related signals of which increased in the same (in-phase) or in the opposite (anti-phase) directions were encountered. A continuum of discharge properties was the rule. We conclude that NIC efferent fibers send a combination of eye-position, saccade-, and smooth-pursuit-related signals, mixed in proportions that differ for different fibers, to targets of the vertical neural integrator such as extraocular motoneurons.

Discharge Characteristics of Vestibular Saccade Neurons in Alert Monkeys

1998 ◽  
Vol 79 (2) ◽  
pp. 835-847 ◽  
Author(s):  
Chris R. S. Kaneko ◽  
Kikuro Fukushima
Keyword(s):  
Smooth Pursuit ◽  
Discharge Rate ◽  
Vestibular Stimulation ◽  
Eye Position ◽  
Interstitial Nucleus Of Cajal ◽  
Discharge Characteristics ◽  
Vestibular Ocular Reflex ◽  
Saccade Size ◽  
Saccade Velocity ◽  
Vertical Saccade

Kaneko, Chris R. S. and Kikuro Fukushima. Discharge characteristics of vestibular saccade neurons in alert monkeys. J. Neurophysiol. 79: 835–847, 1998. We previously described a class of neurons, located in and around the interstitial nucleus of Cajal of the cat, that discharged during vestibular stimulation and before saccades. We called these neurons vestibular saccade neurons (VSNs). In the present study, we characterized similar neurons in the monkey. These neurons discharged before vertical saccades and during vertical vestibular stimulation as well as vertical smooth pursuit. Like cat VSNs, the discharge metrics of these VSNs were poorly related to saccade metrics and showed only occasional, weak sensitivity to eye position. They discharged most intensely (on-direction) for movements that were either upward or downward, and their on-directions were consistent during pitch and pursuit but not for eye position. For saccades, the correlation coefficient of number of spikes and vertical saccade size varied from 0.08 to 0.90 with a mean of ∼0.6. The average sensitivity (i.e., slope) of the number of spikes and vertical saccade size linear regression was 0.3 ± 0.2 spike/deg. Average correlations between peak discharge rate and peak saccade velocity and between burst duration and saccade duration were 0.5 and 0.4; sensitivities were 0.2 ± 0.2 spike per s per deg/s and 0.6 ± 0.5 ms/ms, respectively. Average vestibular sensitivities during 0.5 Hz, ±10° sinusoidal pitch while the animals suppressed their vestibular ocular reflex were 0.97 spike/s per deg/s for up VSNs and 0.66 spike/s per deg/s for down VSNs. The average static position sensitivity for the population of 39 VSNs tested was 0.55 spike/s per deg. The average gain for VSNs tested during 0.5 Hz, ±10° sinusoidal smooth pursuit tracking was 1.4 spike/s per deg/s. As we could not identify analogous neurons in the region of the monkey ponto-medullary junction, we conclude that horizontal on-direction VSNs do not exist in the monkey. We discuss a possible functional role for VSNs and similar neurons described in previous studies and conclude that these neurons are most likely involved with the process of neural integration (in a mathematical sense) of velocity-coded inputs from a variety of oculomotor subsystems and are not a pivotal element in saccade generation.

Activity of Mesencephalic Vertical Burst Neurons During Saccades and Smooth Pursuit

2000 ◽  
Vol 83 (4) ◽  
pp. 2080-2092 ◽  
Author(s):  
M. Missal ◽  
S. de Brouwer ◽  
P. Lefèvre ◽  
E. Olivier
Keyword(s):  
Vertical Velocity ◽  
Smooth Pursuit ◽  
Medial Longitudinal Fasciculus ◽  
Eye Position ◽  
Interstitial Nucleus Of Cajal ◽  
Burst Neurons ◽  
Preferred Direction ◽  
Saccade Onset ◽  
Vertical Saccades ◽  
Eye Velocity

The activity of vertical burst neurons (BNs) was recorded in the rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF-BNs) and in the interstitial nucleus of Cajal (NIC-BNs) in head-restrained cats while performing saccades or smooth pursuit. BNs emitted a high-frequency burst of action potentials before and during vertical saccades. On average, these bursts led saccade onset by 14 ± 4 ms (mean ± SD, n = 23), and this value was in the range of latencies (∼5–15 ms) of medium-lead burst neurons (MLBNs). All NIC-BNs ( n = 15) had a downward preferred direction, whereas riMLF-BNs showed either a downward ( n = 3) or an upward ( n = 5) preferred direction. We found significant correlations between saccade and burst parameters in all BNs: vertical amplitude was correlated with the number of spikes, maximum vertical velocity with maximum of the spike density, and saccade duration with burst duration. A correlation was also found between instantaneous vertical velocity and neuronal activity during saccades. During fixation, all riMLF-BNs and ∼50% of NIC-BNs (7/15) were silent. Among NIC-BNs active during fixation (8/15), only two cells had an activity correlated with the eye position in the orbit. During smooth pursuit, most riMLF-BNs were silent (7/8), but all NIC-BNs showed an activity that was significantly correlated with the eye velocity. This activity was unaltered during temporary disappearance of the visual target, demonstrating that it was not visual in origin. For a given neuron, its on-direction during smooth pursuit and saccades remained identical. The activity of NIC-BNs during both saccades and smooth pursuit can be described by a nonlinear exponential function using the velocity of the eye as independent variable. We suggest that riMLF-BNs, which were not active during smooth pursuit, are vertical MLBNs responsible for the generation of vertical saccades. Because NIC-BNs discharged during both saccades and pursuit, they cannot be regarded as MLBNs as usually defined. NIC-BNs could, however, be the site of convergence of both the saccadic and smooth pursuit signals at the premotoneuronal level. Alternatively, NIC-BNs could participate in the integration of eye velocity to eye position signals and represent input neurons to a common integrator.

Neuronal Responses Related to Smooth Pursuit Eye Movements in the Periarcuate Cortical Area of Monkeys

1998 ◽  
Vol 80 (1) ◽  
pp. 28-47 ◽  
Author(s):  
Masaki Tanaka ◽  
Kikuro Fukushima
Keyword(s):  
Eye Movements ◽  
Smooth Pursuit ◽  
Cortical Area ◽  
Eye Position ◽  
Smooth Pursuit Eye Movements ◽  
Neuronal Responses ◽  
Stationary Target ◽  
Pursuit Eye Movements ◽  
Preferred Direction ◽  
Eye Velocity

Tanaka, Masaki and Kikuro Fukushima. Neuronal responses related to smooth pursuit eye movements in the periarcuate cortical area of monkeys. J. Neurophysiol. 80: 28–47, 1998. To examine how the periarcuate area is involved in the control of smooth pursuit eye movements, we recorded 177 single neurons while monkeys pursued a moving target in the dark. The majority (52%, 92/177) of task-related neurons responded to pursuit but had little or no response to saccades. Histological reconstructions showed that these neurons were located mainly in the posterior bank of the arcuate sulcus near the sulcal spur. Twenty-seven percent (48/177) changed their activity at the onset of saccades. Of these, 36 (75%) showed presaccadic burst activity with strong preference for contraversive saccades. Eighteen (10%, 18/177) were classified as eye-position–related neurons, and 11% (19/177) were related to other aspects of the stimuli or response. Among the 92 neurons that responded to pursuit, 85 (92%) were strongly directional with uniformly distributed preferred directions. Further analyses were performed in these directionally sensitive pursuit-related neurons. For 59 neurons that showed distinct changes in activity around the initiation of pursuit, the median latency from target motion was 96 ms and that preceding pursuit was −12 ms, indicating that these neuron can influence the initiation of pursuit. We tested some neurons by briefly extinguishing the tracking target ( n = 39) or controlling its movement with the eye position signal ( n = 24). The distribution of the change in pursuit-related activity was similar to previous data for the dorsomedial part of the medial superior temporal neurons ( Newsome et al. 1988) , indicating that pursuit-related neurons in the periarcuate area also carry extraretinal signals. For 22 neurons, we examined the responses when the animals reversed pursuit direction to distinguish the effects of eye acceleration in the preferred direction from oppositely directed eye velocity. Almost all neurons discharged before eye velocity reached zero, however, only nine neurons discharged before the eyes were accelerated in the preferred direction. The delay in neuronal responses relative to the onset of eye acceleration in these trials might be caused by suppression from oppositely directed pursuit velocity. The results suggest that the periarcuate neurons do not participate in the earliest stage of eye acceleration during the change in pursuit direction, although most of them may participate in the early stages of pursuit initiation in the ordinary step-ramp pursuit trials. Some neurons changed their activity when the animals fixated a stationary target, and this activity could be distinguished easily from the strong pursuit-related responses. Our results suggest that the periarcuate pursuit area carries extraretinal signals and affects the premotor circuitry for smooth pursuit.

Discharge patterns in nucleus prepositus hypoglossi and adjacent medial vestibular nucleus during horizontal eye movement in behaving macaques

1992 ◽  
Vol 68 (1) ◽  
pp. 319-332 ◽  
Author(s):  
J. L. McFarland ◽  
A. F. Fuchs
Keyword(s):  
Eye Movements ◽  
Eye Movement ◽  
Smooth Pursuit ◽  
Vestibular Nucleus ◽  
Medial Vestibular Nucleus ◽  
Eye Position ◽  
Head Velocity ◽  
Firing Rates ◽  
Prepositus Hypoglossi ◽  
Eye Velocity

1. Monkeys were trained to perform a variety of horizontal eye tracking tasks designed to reveal possible eye movement and vestibular sensitivities of neurons in the medulla. To test eye movement sensitivity, we required stationary monkeys to track a small spot that moved horizontally. To test vestibular sensitivity, we rotated the monkeys about a vertical axis and required them to fixate a target rotating with them to suppress the vestibuloocular reflex (VOR). 2. All of the 100 units described in our study were recorded from regions of the medulla that were prominently labeled after injections of horseradish peroxidase into the abducens nucleus. These regions include the nucleus prepositus hypoglossi (NPH), the medial vestibular nucleus (MVN), and their common border (the “marginal zone”). We report here the activities of three different types of neurons recorded in these regions. 3. Two types responded only during eye movements per se. Their firing rates increased with eye position; 86% had ipsilateral “on” directions. Almost three quarters (73%) of these medullary neurons exhibited a burst-tonic discharge pattern that is qualitatively similar to that of abducens motoneurons. There were, however, quantitative differences in that these medullary burst-position neurons were less sensitive to eye position than were abducens motoneurons and often did not pause completely for saccades in the off direction. The burst of medullary burst position neurons preceded the saccade by an average of 7.6 +/- 1.7 (SD) ms and, on average, lasted the duration of the saccade. The number of spikes in the burst was well correlated with saccade size. The second type of eye movement neuron displayed either no discernible burst or an inconsistent one for on-direction saccades and will be referred to as medullary position neurons. Neither the burst-position nor the position neurons responded when the animals suppressed the VOR; hence, they displayed no vestibular sensitivity. 4. The third type of neuron was sensitive to both eye movement and vestibular stimulation. These neurons increased their firing rates during horizontal head rotation and smooth pursuit eye movements in the same direction; most (76%) preferred ipsilateral head and eye movements. Their firing rates were approximately in phase with eye velocity during sinusoidal smooth pursuit and with head velocity during VOR suppression; on average, their eye velocity sensitivity was 50% greater than their vestibular sensitivity. Sixty percent of these eye/head velocity cells were also sensitive to eye position. 5. The NPH/MVN region contains many neurons that could provide an eye position signal to abducens neurons.(ABSTRACT TRUNCATED AT 400 WORDS)

Discharge patterns and recruitment order of identified motoneurons and internuclear neurons in the monkey abducens nucleus

1988 ◽  
Vol 60 (6) ◽  
pp. 1874-1895 ◽  
Author(s):  
A. F. Fuchs ◽  
C. A. Scudder ◽  
C. R. Kaneko
Keyword(s):  
Firing Rate ◽  
Smooth Pursuit ◽  
Action Potentials ◽  
Medial Rectus ◽  
Eye Position ◽  
Oculomotor Nucleus ◽  
Abducens Nucleus ◽  
Position Sensitivity ◽  
Discharge Patterns ◽  
Eye Velocity

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)

Firing behavior of brain stem neurons during voluntary cancellation of the horizontal vestibuloocular reflex. II. Eye movement related neurons

1993 ◽  
Vol 70 (2) ◽  
pp. 844-856 ◽  
Author(s):  
K. E. Cullen ◽  
C. Chen-Huang ◽  
R. A. McCrea
Keyword(s):  
Eye Movements ◽  
Firing Rate ◽  
Smooth Pursuit ◽  
Vestibular Nucleus ◽  
Medial Vestibular Nucleus ◽  
Eye Position ◽  
Smooth Pursuit Eye Movements ◽  
Stationary Target ◽  
Pursuit Eye Movements ◽  
Eye Velocity

1. The single-unit activity of neurons in the vestibular nucleus, the prepositus nucleus, and the abducens nucleus, whose activity was primarily related to horizontal eye movements, was recorded in alert squirrel monkeys that were trained to track a small visual target by generating smooth pursuit eye movements and to cancel their horizontal vestibuloocular reflex (VOR) by fixating a head stationary target. 2. The spiking behavior of each cell was recorded during 1) spontaneous eye movements, 2) horizontal smooth pursuit of a target that was moved sinusoidally +/- 20 degrees/s at 0.5 Hz, 3) horizontal VOR evoked by 0.5-Hz sinusoidal turntable rotations +/- 40 degrees/s (VORs), and 4) voluntary cancellation of the VOR by fixation of a head-stationary target during 0.5-Hz sinusoidal turntable rotation at +/- 40 degrees/s (VORCs). The responses of most (28/42) of the units were recorded during unpredictable 100-ms steps in head acceleration (400 degrees/s2) that were generated while the monkey was fixating a target light. The acceleration steps were generated either when the monkey was stationary or when the turntable was already rotating (VORt trials), and the monkey was canceling its VOR (VORCt trials). 3. The firing behavior of all 12 of the abducens neurons recorded was closely related to horizontal eye position and eye velocity during all of the behavioral paradigms used, although there was a small but significant increase in the eye position sensitivity of many of these units when the eye was moving (smooth pursuit) versus when the eye was stationary (fixation). 4. Many neurons in the prepositus nucleus and the medial vestibular nucleus (n = 15) were similar to abducens neurons, in that their firing rate was related primarily to horizontal eye position and eye velocity, regardless of the behavioral paradigm used. These cells were, on average, more sensitive to eye position and smooth pursuit eye velocity than were abducens neurons. 5. The firing rate of 15 other neurons in the prepositus and medial vestibular nucleus was related primarily to horizontal smooth pursuit eye movements. The tonic firing rate of all of these smooth pursuit (SP) cells was related to horizontal eye position, and the majority generated bursts of spikes during saccades in all directions but their off direction. Six of the SP neurons fired in phase with ipsilateral eye movements, whereas the remaining nine were sensitive to eye movements in the opposite direction.(ABSTRACT TRUNCATED AT 400 WORDS)

Smooth-Pursuit Eye-Movement-Related Neuronal Activity in Macaque Nucleus Reticularis Tegmenti Pontis

2003 ◽  
Vol 89 (4) ◽  
pp. 2146-2158 ◽  
Author(s):  
David A. Suzuki ◽  
Tetsuto Yamada ◽  
Robert D. Yee
Keyword(s):  
Eye Movements ◽  
Smooth Pursuit ◽  
Response Amplitude ◽  
Eye Position ◽  
Smooth Pursuit Eye Movements ◽  
Average Sensitivity ◽  
Nucleus Reticularis Tegmenti Pontis ◽  
Pursuit Eye Movements ◽  
Nucleus Reticularis ◽  
Eye Velocity

Neuronal responses that were observed during smooth-pursuit eye movements were recorded from cells in rostral portions of the nucleus reticularis tegmenti pontis (rNRTP). The responses were categorized as smooth-pursuit eye velocity (78%) or eye acceleration (22%). A separate population of rNRTP cells encoded static eye position. The sensitivity to pursuit eye velocity averaged 0.81 spikes/s per °/s, whereas the average sensitivity to pursuit eye acceleration was 0.20 spikes/s per °/s2. Of the eye-velocity cells with horizontal preferences for pursuit responses, 56% were optimally responsive to contraversive smooth-pursuit eye movements and 44% preferred ipsiversive pursuit. For cells with vertical pursuit preferences, 61% preferred upward pursuit and 39% preferred downward pursuit. The direction selectivity was broad with 50% of the maximal response amplitude observed for directions of smooth pursuit up to ±85° away from the optimal direction. The activities of some rNRTP cells were linearly related to eye position with an average sensitivity of 2.1 spikes/s per deg. In some cells, the magnitude of the response during smooth-pursuit eye movements was affected by the position of the eyes even though these cells did not encode eye position. On average, pursuit centered to one side of screen center elicited a response that was 73% of the response amplitude obtained with tracking centered at screen center. For pursuit centered on the opposite side, the average response was 127% of the response obtained at screen center. The results provide a neuronal rationale for the slow, pursuit-like eye movements evoked with rNRTP microstimulation and for the deficits in smooth-pursuit eye movements observed with ibotenic acid injection into rNRTP. More globally, the results support the notion of a frontal and supplementary eye field-rNRTP-cerebellum pathway involved with controlling smooth-pursuit eye movements.

Eye Movement Deficits Following Ibotenic Acid Lesions of the Nucleus Prepositus Hypoglossi in Monkeys II. Pursuit, Vestibular, and Optokinetic Responses

1999 ◽  
Vol 81 (2) ◽  
pp. 668-681 ◽  
Author(s):  
Chris R. S. Kaneko
Keyword(s):  
Eye Movements ◽  
Eye Movement ◽  
Smooth Pursuit ◽  
Ibotenic Acid ◽  
Eye Position ◽  
Neural Integrator ◽  
Nucleus Prepositus Hypoglossi ◽  
Optokinetic Responses ◽  
Prepositus Hypoglossi ◽  
Eye Velocity

Eye movement deficits following ibotenic acid lesions of the nucleus prepositus hypoglossi in monkeys. II. Pursuit, vestibular, and optokinetic responses. The eyes are moved by a combination of neural commands that code eye velocity and eye position. The eye position signal is supposed to be derived from velocity-coded command signals by mathematical integration via a single oculomotor neural integrator. For horizontal eye movements, the neural integrator is thought to reside in the rostral nucleus prepositus hypoglossi (nph) and project directly to the abducens nuclei. In a previous study, permanent, serial ibotenic acid lesions of the nph in three rhesus macaques compromised the neural integrator for fixation but saccades were not affected. In the present study, to determine further whether the nph is the neural substrate for a single oculomotor neural integrator, the effects of those lesions on smooth pursuit, the vestibulo-ocular reflex (VOR), vestibular nystagmus (VN), and optokinetic nystagmus (OKN) are documented. The lesions were correlated with long-lasting deficits in eye movements, indicated most clearly by the animals’ inability to maintain steady gaze in the dark. However, smooth pursuit and sinusoidal VOR in the dark, like the saccades in the previous study, were affected minimally. The gain of horizontal smooth pursuit (eye movement/target movement) decreased slightly (<25%) and phase lead increased slightly for all frequencies (0.3–1.0 Hz, ±10° target tracking), most noticeably for higher frequencies (0.8–0.7 and ∼20° for 1.0-Hz tracking). Vertical smooth pursuit was not affected significantly. Surprisingly, horizontal sinusoidal VOR gain and phase also were not affected significantly. Lesions had complex effects on both VN and OKN. The plateau of per- and postrotatory VN was shortened substantially (∼50%), whereas the initial response and the time constant of decay decreased slightly. The initial OKN response also decreased slightly, and the charging phase was prolonged transiently then recovered to below normal levels like the VN time constant. Maximum steady-state, slow eye velocity of OKN decreased progressively by ∼30% over the course of the lesions. These results support the previous conclusion that the oculomotor neural integrator is not a single neural entity and that the mathematical integrative function for different oculomotor subsystems is most likely distributed among a number of nuclei. They also show that the nph apparently is not involved in integrating smooth pursuit signals and that lesions of the nph can fractionate the VOR and nystagmic responses to adequate stimuli.

scholarly journals The Response of MSTd Neurons to Perturbations in Target Motion During Ongoing Smooth-Pursuit Eye Movements

2010 ◽  
Vol 103 (1) ◽  
pp. 519-530 ◽  
Author(s):  
Seiji Ono ◽  
Lukas Brostek ◽  
Ulrich Nuding ◽  
Stefan Glasauer ◽  
Ulrich Büttner ◽  
...  
Keyword(s):  
Eye Movement ◽  
Smooth Pursuit ◽  
Dynamic Properties ◽  
Receptive Fields ◽  
Gain Control ◽  
Frontal Eye Field ◽  
Cortical Areas ◽  
Target Perturbation ◽  
Behaving Monkeys ◽  
Dynamic Gain

Several regions of the brain are involved in smooth-pursuit eye movement (SPEM) control, including the cortical areas MST (medial superior temporal) and FEF (frontal eye field). It has been shown that the eye-movement responses to a brief perturbation of the visual target during ongoing pursuit increases with higher pursuit velocities. To further investigate the underlying neuronal mechanism of this nonlinear dynamic gain control and the contributions of different cortical areas to it, we recorded from MSTd (dorsal division of the MST area) neurons in behaving monkeys ( Macaca mulatta) during step-ramp SPEM (5–20°/s) with and without superimposed target perturbation (one cycle, 5 Hz, ±10°/s). Smooth-pursuit–related MSTd neurons started to increase their activity on average 127 ms after eye-movement onset. Target perturbation consistently led to larger eye-movement responses and decreasing latencies with increasing ramp velocities, as predicted by dynamic gain control. For 36% of the smooth-pursuit–related MSTd neurons the eye-movement perturbation was accompanied by detectable changes in neuronal activity with a latency of 102 ms, with respect to the eye-movement response. The remaining smooth-pursuit–related MSTd neurons (64%) did not reflect the eye-movement perturbation. For the large majority of cases this finding could be predicted by the dynamic properties of the step-ramp responses. Almost all these MSTd neurons had large visual receptive fields responding to motion in preferred directions opposite to the optimal SPEM stimulus. Based on these findings it is unlikely that MSTd plays a major role for dynamic gain control and initiation of the perturbation response. However, neurons in MSTd could still participate in SPEM maintenance. Due to their visual field properties they could also play a role in other functions such as self-motion perception.

Quantitative Analysis of Abducens Neuron Discharge Dynamics During Saccadic and Slow Eye Movements

1999 ◽  
Vol 82 (5) ◽  
pp. 2612-2632 ◽  
Author(s):  
Pierre A. Sylvestre ◽  
Kathleen E. Cullen
Keyword(s):  
Eye Movements ◽  
Firing Rate ◽  
Eye Movement ◽  
Neuronal Activity ◽  
Smooth Pursuit ◽  
Slow Phase ◽  
Vestibular Nystagmus ◽  
Firing Rates ◽  
Rapid Eye Movements ◽  
Eye Velocity

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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