Neural control of vergence eye movements: activity of abducens and oculomotor neurons

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.

2019 ◽  
Author(s):  
Christian Brysch ◽  
Claire Leyden ◽  
Aristides B. Arrenberg

AbstractBackgroundThe oculomotor integrator (OI) in the vertebrate hindbrain transforms eye velocity input into persistent position coding output, which plays a crucial role in retinal image stability. For a mechanistic understanding of the integrator function and eye position control, knowledge about the tuning of the OI and other oculomotor nuclei is needed. Zebrafish are increasingly used to study integrator function and sensorimotor circuits, yet the precise neuronal tuning to motor variables remains uncharacterized.ResultsHere, we recorded cellular calcium signals while evoking monocular and binocular optokinetic eye movements at different slow-phase eye velocities. Our analysis reveals the anatomical distributions of motoneurons and internuclear neurons in the nucleus abducens as well as those of oculomotor neurons in caudally adjacent hindbrain volumes. Each neuron is tuned to eye position and/or velocity to variable extents and is only activated after surpassing particular eye position and velocity thresholds. While the abducens (rhombomeres 5/6) mainly codes for eye position, in rhombomeres 7/8 a velocity-to-position coding gradient exists along the rostro-caudal axis, which likely corresponds to the velocity and position storage mechanisms. Position encoding neurons are recruited at eye position thresholds distributed across the behavioral dynamic range, while velocity encoding neurons have more centered firing thresholds for velocity. In the abducens, neurons coding exclusively for one eye intermingle with neurons coding for both eyes. Many of these binocular neurons are preferentially active during conjugate eye movements, which represents a functional diversification in the final common motor pathway.ConclusionsWe localized and functionally characterized the repertoire of oculomotor neurons in the zebrafish hindbrain. Our findings provide evidence for a mixed but task-specific binocular code and suggest that generation of persistent activity is organized along the rostro-caudal axis in the hindbrain.


2001 ◽  
Vol 86 (4) ◽  
pp. 1546-1554 ◽  
Author(s):  
S. Glasauer ◽  
M. Dieterich ◽  
Th. Brandt

To find an explanation of the mechanisms of central positional nystagmus in neurological patients with posterior fossa lesions, we developed a three-dimensional (3-D) mathematical model to simulate head position-dependent changes in eye position control relative to gravity. This required a model implementation of saccadic burst generation, of the neural velocity to eye position integrator, which includes the experimentally demonstrated leakage in the torsional component, and of otolith-dependent neural control of Listing's plane. The validity of the model was first tested by simulating saccadic eye movements in different head positions. Then the model was used to simulate central positional nystagmus in off-vertical head positions. The model simulated lesions of assumed otolith inputs to the burst generator or the neural integrator, both of which resulted in different types of torsional-vertical nystagmus that only occurred during head tilt in roll plane. The model data qualitatively fit clinical observations of central positional nystagmus. Quantitative comparison with patient data were not possible, since no 3-D analyses of eye movements in various head positions have been reported in the literature on patients with positional nystagmus. The present model, prompted by an open clinical question, proposes a new hypothesis about the generation of pathological nystagmus and about neural control of Listing's plane.


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)


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)


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 64 (2) ◽  
pp. 413-422 ◽  
Author(s):  
J. M. Delgado-Garcia ◽  
C. Evinger ◽  
M. Escudero ◽  
R. Baker

1. The activity of both accessory abducens (Acc Abd) and abducens (Abd) motoneurons (Mns) was recorded in the alert cat during eye retraction and rotational eye movements. Cats were fitted with two scleral coils, one measured rotational eye movements directly and the other retraction by distinguishing the translational component. 2. Acc Abd and Abd Mns were identified following antidromic activation from electrical stimulation of the ipsilateral VIth nerve. 3. In response to corneal air puffs, bursts of spikes were produced in all (n = 30) Acc Abd Mns. The burst began 7.2 +/- 1.2 (SD) ms after onset of the air puff and 8.9 +/- 1.9 ms before eye retraction. 4. Acc Abd Mns were silent throughout all types of rotational eye movements, and tonic activity was not observed during intervals without air-puff stimulation. 5. In contrast, all (n = 50) identified Abd Mns exhibited a burst and/or pause in activity preceding and during horizontal saccades as well as a tonic activity proportional to eye position. 6. Only 10% of Abd Mns fired a weak burst of spikes in response to air-puff stimulation. 7. We conclude that Acc Abd Mns are exclusively involved in eye retraction in the cat and that only a few Abd Mns have an eye-retraction signal added to their eye position and velocity signals. Thus any rotational eye-movement response described in retractor bulbi muscle must result from innervation by Mns located in the Abd and/or the oculomotor nuclei. 8. The organization of the prenuclear circuitry and species variation are discussed in view of the nictiating membrane extension response measured in associative learning.


2019 ◽  
Vol 121 (5) ◽  
pp. 1865-1878 ◽  
Author(s):  
A. M. Pastor ◽  
P. M. Calvo ◽  
R. R. de la Cruz ◽  
R. Baker ◽  
H. Straka

Computational capability and connectivity are key elements for understanding how central vestibular neurons contribute to gaze-stabilizing eye movements during self-motion. In the well-characterized and segmentally distributed hindbrain oculomotor network of goldfish, we determined afferent and efferent connections along with discharge patterns of descending octaval nucleus (DO) neurons during different eye motions. Based on activity correlated with horizontal eye and head movements, DO neurons were categorized into two complementary groups that either increased discharge during both contraversive (type II) eye (e) and ipsiversive (type I) head (h) movements (eIIhI) or vice versa (eIhII). Matching time courses of slow-phase eye velocity and corresponding firing rates during prolonged visual and head rotation suggested direct causality in generating extraocular motor commands. The axons of the dominant eIIhI subgroup projected either ipsi- or contralaterally and terminated in the abducens nucleus, Area II, and Area I with additional recurrent collaterals of ipsilaterally projecting neurons within the parent nucleus. Distinct feedforward commissural pathways between bilateral DO neurons likely contribute to the generation of eye velocity signals in eIhII cells. The shared contribution of DO and Area II neurons to eye velocity storage likely represents an ancestral condition in goldfish that is clearly at variance with the task separation between mammalian medial vestibular and prepositus hypoglossi neurons. This difference in signal processing between fish and mammals might correlate with a larger repertoire of visuo-vestibular-driven eye movements in the latter species that potentially required a shift in sensitivity and connectivity within the hindbrain-cerebello-oculomotor network. NEW & NOTEWORTHY We describe the structure and function of neurons within the goldfish descending octaval nucleus. Our findings indicate that eye and head velocity signals are processed by vestibular and Area II velocity storage integrator circuitries whereas the velocity-to-position Area I neural integrator generates eye position solely. This ancestral condition differs from that of mammals, in which vestibular neurons generally lack eye position signals that are processed and stored within the nucleus prepositus hypoglossi.


BMC Biology ◽  
2019 ◽  
Vol 17 (1) ◽  
Author(s):  
Christian Brysch ◽  
Claire Leyden ◽  
Aristides B. Arrenberg

Abstract Background The oculomotor integrator (OI) in the vertebrate hindbrain transforms eye velocity input into persistent position coding output, which plays a crucial role in retinal image stability. For a mechanistic understanding of the integrator function and eye position control, knowledge about the tuning of the OI and other oculomotor nuclei is needed. Zebrafish are increasingly used to study integrator function and sensorimotor circuits, yet the precise neuronal tuning to motor variables remains uncharacterized. Results Here, we recorded cellular calcium signals while evoking monocular and binocular optokinetic eye movements at different slow-phase eye velocities. Our analysis reveals the anatomical distributions of motoneurons and internuclear neurons in the nucleus abducens as well as those of oculomotor neurons in caudally adjacent hindbrain volumes. Each neuron is tuned to eye position and/or velocity to variable extents and is only activated after surpassing particular eye position and velocity thresholds. While the abducens (rhombomeres 5/6) mainly codes for eye position, in rhombomeres 7/8, a velocity-to-position coding gradient exists along the rostro-caudal axis, which likely corresponds to the oculomotor structures storing velocity and position, and is in agreement with a feedforward mechanism of persistent activity generation. Position encoding neurons are recruited at eye position thresholds distributed across the behaviourally relevant dynamic range, while velocity-encoding neurons have more centred firing thresholds for velocity. In the abducens, neurons coding exclusively for one eye intermingle with neurons coding for both eyes. Many of these binocular neurons are preferentially active during conjugate eye movements and less active during monocular eye movements. This differential recruitment during monocular versus conjugate tasks represents a functional diversification in the final common motor pathway. Conclusions We localized and functionally characterized the repertoire of oculomotor neurons in the zebrafish hindbrain. Our findings provide evidence for a mixed but task-specific binocular code and suggest that generation of persistent activity is organized along the rostro-caudal axis in the hindbrain.


2003 ◽  
Vol 90 (2) ◽  
pp. 739-754 ◽  
Author(s):  
Pierre A. Sylvestre ◽  
Julia T. L. Choi ◽  
Kathleen E. Cullen

Burst-tonic (BT) neurons in the prepositus hypoglossi and adjacent medial vestibular nuclei are important elements of the neural integrator for horizontal eye movements. While the metrics of their discharges have been studied during conjugate saccades (where the eyes rotate with similar dynamics), their role during disjunctive saccades (where the eyes rotate with markedly different dynamics to account for differences in depths between saccadic targets) remains completely unexplored. In this report, we provide the first detailed quantification of the discharge dynamics of BT neurons during conjugate saccades, disjunctive saccades, and disjunctive fixation. We show that these neurons carry both significant eye position and eye velocity-related signals during conjugate saccades as well as smaller, yet important, “slide” and eye acceleration terms. Further, we demonstrate that a majority of BT neurons, during disjunctive fixation and disjunctive saccades, preferentially encode the position and the velocity of a single eye; only few BT neurons equally encode the movements of both eyes (i.e., have conjugate sensitivities). We argue that BT neurons in the nucleus prepositus hypoglossi/medial vestibular nucleus play an important role in the generation of unequal eye movements during disjunctive saccades, and carry appropriate information to shape the saccadic discharges of the abducens nucleus neurons to which they project.


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)


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