Discharge characteristics of medial rectus and abducens motoneurons in the goldfish

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)

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)


1995 ◽  
Vol 73 (4) ◽  
pp. 1383-1395 ◽  
Author(s):  
J. S. Stahl ◽  
J. I. Simpson

1. We recorded abducens neurons, identified by electrical stimulation as internuclear neurons or motoneurons, in awake rabbits. The relationship of firing rate to eye movement was determined from responses during stable fixations, sinusoidal rotation in the light (0.05-0.8 Hz), and triangular optokinetic stimulation at 0.1 Hz. 2. All abducens neurons were excited during temporal movement of the ipsilateral eye. Temporal and nasal saccades were associated with bursts or pauses, respectively, in the firing rate. 3. Motoneurons and internuclear neurons are qualitatively indistinguishable. There was no significant quantitative difference between the phase and sensitivity of the two groups for 0.2-Hz sinusoidal rotation in the light. 4. On the basis of the response to stable eye positions, we determined static eye position sensitivity of the abducens neuron pool to be 8.2 +/- 2.5 (SD) spikes.s-1/0, with a static hysteresis of 8.9 spikes/s (1.14 +/- 0.37 degrees). 5. We determined apparent eye position sensitivity (k) and apparent eye velocity sensitivity (r) from the responses to sinusoidal rotation in the light. k increases and r decreases with stimulus frequency, which indicates that the simplest transfer function mediating conversion of abducens nucleus (VI) firing rate to eye position (E) has two poles and one zero. 6. The VI-->E relationship has an "amplitude nonlinearity," manifest as a tendency for k, r, and firing rate phase lead to decrease as eye movement amplitude increases at a fixed frequency. On a percentage basis, phase is less affected than are the sensitivities. The nonlinearity becomes less pronounced for stimulus amplitudes > 2.5 degrees, and consequently a linear model of the VI-->E transformation remains useful, provided that consideration is restricted to the appropriate range of stimulus/response amplitudes. 7. We determined time constants of the linear two-pole, one-zero transfer function from the variation of r/k versus stimulus frequency. The pole time constants were T1 = 3.4 s and T2 = 0.28 s, and the zero time constant (Tz) = 1.6 s. The magnitude of Tz was corroborated by measuring the time constant of the exponential decay in firing rate after step changes in eye position. This transient method yielded a Tz of 1.1 s. 8. The time constants of the VI-->E transfer function are roughly 10 times larger than those reported for the rhesus macaque. The difference is attributable to the reported 10-fold lower stiffness of the rabbit oculomotor plant, which may in turn relate to rabbits postulated lower degree of activation of extraocular muscles at any given position.(ABSTRACT TRUNCATED AT 400 WORDS)


1995 ◽  
Vol 73 (4) ◽  
pp. 1396-1413 ◽  
Author(s):  
J. S. Stahl ◽  
J. I. Simpson

1. We recorded single vestibular nucleus neurons shown by electrical stimulation to receive floccular inhibition [flocculus receiving neurons (FRNs)] and/or to project toward midbrain motoneuronal pools [midbrain projecting neurons (MPNs)] in awake, head-fixed rabbits during compensatory eye movements. Stimuli included head rotation in the light, head rotation in the dark, and rotation of an optokinetic drum about the animal. We employed sinusoidal and triangular position profiles in the 0.05- to 0.8-Hz frequency band. We also examined transient responses to step changes in eye position. 2. We found identified vestibular nucleus cells (i.e., FRN/non-MPNs, FRN/MPNs, and non-FRN/MPNs) in the parvocellular and magnocellular portions of the medial vestibular nucleus, at the rostrocaudal level of the dorsal acoustic stria. 3. All identified vestibular nucleus neurons were excited during ipsilateral (relative to side of recording) head rotation and contralateral eye rotation. 4. The neuronal firing rates could be related to eye position and its time derivatives, and that relationship could be approximated by a two-pole, one-zero linear transfer function. As with abducens neurons, a more detailed approximation requires inclusion of two nonlinearities-a hysteresis and a variable sensitivity term that increases as eye movement amplitude decreases. 5. When the vestibuloocular reflex is suppressed by a conflicting full-field visual stimulus [visual vestibular conflict condition (VVC)], vestibular nucleus neuron modulation is largely suppressed. The remaining modulation is motoric in nature, because it can be related to the residual eye movements. Cells with "sensory vestibular signals," i.e., cells whose modulation during VVC correlates better with head rotation than eye movement, were not encountered. 6. We examined the dependence of firing rate parameters on stimulus modality. All neurons exhibited increased phase lead with respect to abducens nucleus neurons during stimuli involving head rotation. This finding could indicate that vestibular-derived inputs are inhomogeneously distributed on premotor neurons and that the studied premotor population receives a stronger vestibular input than another premotor group, not recorded in the current experiments. 7. FRNs and non-FRNs were similar in their qualitative response to the fast phases, the applicability of the two-pole, one-zero transfer function, hysteresis, and the amplitude nonlinearity. 8. FRNs differed from non-FRNs in having a phase advanced firing rate at all stimulus frequencies during visual and vestibular stimuli. The phase difference suggests that one role of the rabbit flocculus is to regulate phase of the net premotor signal.


1984 ◽  
Vol 52 (4) ◽  
pp. 724-742 ◽  
Author(s):  
M. C. Chubb ◽  
A. F. Fuchs ◽  
C. A. Scudder

To elucidate how information is processed in the vestibuloocular reflex (VOR) pathways subserving vertical eye movements, extracellular single-unit recordings were obtained from the vestibular nuclei of alert monkeys trained to track a visual target with their eyes while undergoing sinusoidal pitch oscillations (0.2-1.0 Hz). Units with activity related to vertical vestibular stimulation and/or eye movements were classified as either vestibular units (n = 53), vestibular plus eye-position units (n = 30), pursuit units (n = 10), or miscellaneous units (n = 5), which had various combinations of head- and eye-movement sensitivities. Vestibular units discharged in relation to head rotation, but not to smooth eye movements. On average, these units fired approximately in phase with head velocity; however, a broad range of phase shifts was observed. The activities of 8% of the vestibular units were related to saccades. Vestibular plus eye-position units fired in relation to head velocity and eye position and, in addition, usually to eye velocity. Their discharge rates increased for eye and head movements in opposite directions. During combined head and eye movements, the modulation in unit activity was not significantly different from the sum of the modulations during each alone. For saccades, the unit firing rate either decreased to zero or was unaffected. Pursuit units discharged in relation to eye position, eye velocity, or both, but not to head movements alone. For saccades, unit activity usually either paused or was unaffected. The eye-movement-related activities of the vestibular plus eye-position and pursuit units were not significantly different. A quantitative comparison of their firing patterns suggests that vestibular, vestibular plus eye-position, and pursuit neurons in the vestibular nucleus could provide mossy fiber inputs to the flocculus. In addition, the vertical vestibular plus eye-position neurons have discharge patterns similar to those of fibers recorded rostrally in the medial longitudinal fasciculus. Therefore, our data support the view that vertical vestibular plus eye-position neurons are interneurons of the VOR.


1976 ◽  
Vol 39 (6) ◽  
pp. 1135-1149 ◽  
Author(s):  
W. M. King ◽  
S. G. Lisberger ◽  
A. F. Fuchs

Extracellular recordings were obtained from 37 histologically identified MLF fibers near the trochlear nucleus in alert monkeys trained to perform a visual tracking task and subjected to adequate horizontal and vertical vestibular stimulation. The behavioral paradigm permitted independent quantitative assessment of a fiber's response to eye or head movements. 2. According to their discharge pattern, almost all MLF fibers were placed in one of two classes: 1) Horizontal burst-tonic fibers (n = 20). During both vestibular and visually evoked eye movements, burst-tonic fibers discharged in strict relation to horizontal eye movements, exhibiting a burst of activity prior to on-direction saccades and steady firing related to horizontal eye position during fixations. 2) Vertical vestibular plus eye-position fibers (n = 14). Vertical fibers discharged in relation to vertical head velocity in the absence of eye movements and in relation to vertical eye position in the absence of head movement, and paused with saccades in any direction. 3. The quantitative similarity of horizontal burst-tonic fiber discharge to that of ipsilateral medial rectus oculomotoneurons suggests that burst-tonic fibers provide the major excitatory synaptic drive to medial rectus motoneurons during conjugate eye movements of vestibular or visual origin. 4. The discharge pattern of vertical vestibular plus eye-position fibers is significantly different from that of oculomotoneurons, suggesting that additional neural processing of vertical fiber information must occur in the mesencephalon. 5. The functional dichotomy of horizontal and vertical MLF fibers and their contrasting discharge patterns provide new evidence for the anatomic and functional separation of horizontal and vertical eye movement mechanisms in the pons and mesencephalon, respectively.


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.


1992 ◽  
Vol 68 (1) ◽  
pp. 319-332 ◽  
Author(s):  
J. L. McFarland ◽  
A. F. Fuchs

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)


1998 ◽  
Vol 79 (3) ◽  
pp. 1461-1480 ◽  
Author(s):  
Markus Lappe ◽  
Martin Pekel ◽  
Klaus-Peter Hoffmann

Lappe, Markus, Martin Pekel, and Klaus-Peter Hoffmann. Optokinetic eye movements elicited by radial optic flow in the macaque monkey. J. Neurophysiol. 79: 1461–1480, 1998. We recorded spontaneous eye movements elicited by radial optic flow in three macaque monkeys using the scleral search coil technique. Computer-generated stimuli simulated forward or backward motion of the monkey with respect to a number of small illuminated dots arranged on a virtual ground plane. We wanted to see whether optokinetic eye movements are induced by radial optic flow stimuli that simulate self-movement, quantify their parameters, and consider their effects on the processing of optic flow. A regular pattern of interchanging fast and slow eye movements with a frequency of 2 Hz was observed. When we shifted the horizontal position of the focus of expansion (FOE) during simulated forward motion (expansional optic flow), median horizontal eye position also shifted in the same direction but only by a smaller amount; for simulated backward motion (contractional optic flow), median eye position shifted in the opposite direction. We relate this to a change in Schlagfeld typically observed in optokinetic nystagmus. Direction and speed of slow phase eye movements were compared with the local flow field motion in gaze direction (the foveal flow). Eye movement direction matched well the foveal motion. Small systematic deviations could be attributed to an integration of the global motion pattern. Eye speed on average did not match foveal stimulus speed, as the median gain was only ∼0.5–0.6. The gain was always lower for expanding than for contracting stimuli. We analyzed the time course of the eye movement immediately after each saccade. We found remarkable differences in the initial development of gain and directional following for expansion and contraction. For expansion, directional following and gain were initially poor and strongly influenced by the ongoing eye movement before the saccade. This was not the case for contraction. These differences also can be linked to properties of the optokinetic system. We conclude that optokinetic eye movements can be elicited by radial optic flow fields simulating self-motion. These eye movements are linked to the parafoveal flow field, i.e., the motion in the direction of gaze. In the retinal projection of the optic flow, such eye movements superimpose retinal slip. This results in complex retinal motion patterns, especially because the gain of the eye movement is small and variable. This observation has special relevance for mechanisms that determine self-motion from retinal flow fields. It is necessary to consider the influence of eye movements in optic flow analysis, but our results suggest that direction and speed of an eye movement should be treated differently.


1999 ◽  
Vol 81 (5) ◽  
pp. 2538-2557 ◽  
Author(s):  
Chiju Chen-Huang ◽  
Robert A. McCrea

Effects of viewing distance on the responses of vestibular neurons to combined angular and linear vestibular stimulation. The firing behavior of 59 horizontal canal–related secondary vestibular neurons was studied in alert squirrel monkeys during the combined angular and linear vestibuloocular reflex (CVOR). The CVOR was evoked by positioning the animal’s head 20 cm in front of, or behind, the axis of rotation during whole body rotation (0.7, 1.9, and 4.0 Hz). The effect of viewing distance was studied by having the monkeys fixate small targets that were either near (10 cm) or far (1.3–1.7 m) from the eyes. Most units (50/59) were sensitive to eye movements and were monosynaptically activated after electrical stimulation of the vestibular nerve (51/56 tested). The responses of eye movement–related units were significantly affected by viewing distance. The viewing distance–related change in response gain of many eye-head-velocity and burst-position units was comparable with the change in eye movement gain. On the other hand, position-vestibular-pause units were approximately half as sensitive to changes in viewing distance as were eye movements. The sensitivity of units to the linear vestibuloocular reflex (LVOR) was estimated by subtraction of angular vestibuloocular reflex (AVOR)–related responses recorded with the head in the center of the axis of rotation from CVOR responses. During far target viewing, unit sensitivity to linear translation was small, but during near target viewing the firing rate of many units was strongly modulated. The LVOR responses and viewing distance–related LVOR responses of most units were nearly in phase with linear head velocity. The signals generated by secondary vestibular units during voluntary cancellation of the AVOR and CVOR were comparable. However, unit sensitivity to linear translation and angular rotation were not well correlated either during far or near target viewing. Unit LVOR responses were also not well correlated with their sensitivity to smooth pursuit eye movements or their sensitivity to viewing distance during the AVOR. On the other hand there was a significant correlation between static eye position sensitivity and sensitivity to viewing distance. We conclude that secondary horizontal canal–related vestibuloocular pathways are an important part of the premotor neural substrate that produces the LVOR. The otolith sensory signals that appear on these pathways have been spatially and temporally transformed to match the angular eye movement commands required to stabilize images at different distances. We suggest that this transformation may be performed by the circuits related to temporal integration of the LVOR.


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)


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