Characteristics of antidromically identified oculomotor internuclear neurons during vergence and versional eye movements

1994 ◽  
Vol 71 (3) ◽  
pp. 1111-1127 ◽  
Author(s):  
R. A. Clendaniel ◽  
L. E. Mays
Keyword(s):  
Eye Movements ◽  
Medial Rectus ◽  
Oculomotor Nucleus ◽  
Abducens Nucleus ◽  
Unit Recording ◽  
Antidromic Activation ◽  
Reversible Inactivation ◽  
Lidocaine Injection ◽  
Lidocaine Hcl ◽  
Tonic Pattern

1. Previous studies have shown that midbrain near response cells that increase their activity during convergent eye movements project to medial rectus motoneurons, which also increase their activity during convergence. Most neurons in the abducens nucleus decrease their firing rate during convergence, and the source of this vergence signal is unknown. Oculomotor internuclear neurons (OINs) in monkeys project primarily from the medial rectus subdivisions of the oculomotor nucleus to the contralateral abducens nucleus, although there is a smaller ipsilateral projection as well. Because of these anatomic connections, it has been suggested that the OIN input may be responsible for the vergence signal seen on abducens neurons. The behavior of the OINs during eye movements and their synaptic drive are not known. Thus the goal of this study is to determine the behavior of these neurons during conjugate and disjunctive eye movements and to determine if these neurons have an excitatory or inhibitory drive on the abducens neurons. 2. Single-unit recording studies in alert rhesus monkeys were used to characterize the behavior of OINs. Eighteen OINs were identified by antidromic activation and collision testing. The recorded OINs displayed a burst-tonic pattern of activity during adducting saccades, and the majority of these cells displayed an increase in tonic activity with convergent eye movements. 3. Identified OINs were compared with a large sample of non-activated and untested horizontal burst-tonic cells in the medial rectus subdivisions of the oculomotor nucleus. The results indicate that the OINs behave similarly to medial rectus motoneurons during vergence and versional eye movements. None of the OINs displayed vertical eye position sensitivity. 4. Microstimulation of the oculomotor nucleus where both the OINs and medial rectus motoneurons were located resulted in a large adducting twitch of the ipsilateral eye and a smaller abducting twitch of the contralateral eye. The latter effect was presumed to be the result of OIN innervation of the contralateral abducens nucleus. This result suggests that the crossed OIN pathway is predominately, if not entirely, excitatory. 5. Injection of 10% lidocaine HCl into the medial rectus subdivision of the oculomotor nucleus caused a reversible inactivation of the medial rectus motoneurons and OINs. As expected, the inactivation of medial rectus motoneurons resulted in an exophoria and weakness of adduction for the eye ipsilateral to the lidocaine injection. In addition, the lidocaine injection resulted in hypometric and slowed abducting saccades in the eye contralateral to the injection site. This result also suggest that the crossed OIN pathway is excitatory.(ABSTRACT TRUNCATED AT 400 WORDS)

Abducens internuclear neurons carry an inappropriate signal for ocular convergence

1989 ◽  
Vol 62 (1) ◽  
pp. 70-81 ◽  
Author(s):  
P. D. Gamlin ◽  
J. W. Gnadt ◽  
L. E. Mays
Keyword(s):  
Eye Movements ◽  
Action Potentials ◽  
Vestibular Nuclei ◽  
Lateral Rectus ◽  
Medial Rectus ◽  
Medial Longitudinal Fasciculus ◽  
Unit Recording ◽  
Antidromic Activation ◽  
Prepositus Hypoglossi ◽  
Ocular Convergence

1. Single-unit recording studies in alert Rhesus monkeys characterized the vergence signal carried by abducens internuclear neurons. These cells were identified by antidromic activation and the collision of spontaneous with antidromic action potentials. The behavior of abducens internuclear neurons during vergence was compared with that of horizontal burst-tonic fibers in the medial longitudinal fasciculus (MLF) and to that of a large sample of unidentified abducens cells (presumably both motoneurons and internuclear neurons). 2. The results indicate that abducens internuclear neurons and lateral rectus motoneurons behave similarly during vergence eye movements: the majority of both groups of cells decrease their firing rate for convergence eye movements: a minority show no change for vergence. This finding is strongly supported by recordings of horizontal burst-tonic fibers in the MLF, the majority of which decrease their activity significantly for convergence eye movements. 3. These findings indicate that a net inappropriate vergence signal is sent to medial rectus motoneurons via the abducens internuclear pathway. Because medial rectus motoneurons increase their activity appropriately during symmetrical convergence, this inappropriate MLF signal must be overcome by a more potent direct vergence input. 4. Overall, both abducens internuclear neurons and lateral rectus motoneurons decrease their activity for convergence less than would be expected based on their conjugate gain. This implies that some degree of co-contraction of the lateral and medial rectus muscles occurs during convergence eye movements. 5. Some horizontal burst-tonic MLF fibers decrease their activity more for convergence than any recorded abducens neuron. These fibers may arise from cells in the nucleus prepositus hypoglossi or vestibular nuclei.

The vestibuloocular reflex of the adult flatfish. I. Oculomotor organization

1985 ◽  
Vol 54 (4) ◽  
pp. 887-899 ◽  
Author(s):  
W. Graf ◽  
R. Baker
Keyword(s):  
Eye Movements ◽  
Motor Neuron ◽  
Motor Neurons ◽  
Vertical Plane ◽  
Extraocular Muscles ◽  
The Body ◽  
Medial Rectus ◽  
Inferior Rectus ◽  
Abducens Nucleus ◽  
Eye Muscles

The flatfish species constitute a natural paradigm for investigating adaptive changes in the vertebrate central nervous system. During metamorphosis all species of flatfish experience a 90 degree change in orientation between their vestibular and extraocular coordinate axes. As a result, the optic axes of both eyes maintain their orientation with respect to earth horizontal, but the horizontal semicircular canals become oriented vertically. Since the flatfish propels its body with the same swimming movements when referenced to the body as a normal fish, the horizontal canals are exposed to identical accelerations, but in the flatfish these accelerations occur in a vertical plane. The appropriate compensatory eye movements are simultaneous rotations of both eyes forward or backward (i.e., parallel), in contrast to the symmetric eye movements in upright fish (i.e., one eye moves forward, the other backward). Therefore, changes in the extraocular muscle arrangement and/or the neuronal connectivity are required. This study describes the peripheral and central oculomotor organization in the adult winter flounder, Pseudopleuronectes americanus. At the level of the peripheral oculomotor apparatus, the sizes of the horizontal extraocular muscles (lateral and medial rectus) were considerably smaller than those of the vertical eye muscles, as quantified by fiber counts and area measurements of cross sections of individual muscles. However, the spatial orientations and the kinematic characteristics of all six extraocular muscles were not different from those described in comparable lateral-eyed animals. There were no detectable asymmetries between the left and the right eye. Central oculomotor organization was investigated by extracellular horseradish peroxidase injections into individual eye muscles. Commonly described distributions of extraocular motor neurons in the oculomotor, trochlear, and abducens nuclei were found. These motor neuron pools consisted of two contralateral (superior rectus and superior oblique) and four ipsilateral populations (inferior oblique, inferior rectus, medial rectus, and lateral rectus). The labeled cells formed distinct motor neuron populations, which overlapped little. As expected, the numbers of labeled motoneurons differed in horizontal and vertical eye movers. The numerical difference was especially prominent in comparing the abducens nucleus with one of the vertical recti subdivisions. Nevertheless, there was bilateral symmetry between the motoneurons projecting to the left and right eyes.(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)

Effect of Reversible Inactivation of Macaque Lateral Intraparietal Area on Visual and Memory Saccades

1999 ◽  
Vol 81 (4) ◽  
pp. 1827-1838 ◽  
Author(s):  
Chiang-Shan Ray Li ◽  
Pietro Mazzoni ◽  
Richard A. Andersen
Keyword(s):  
Eye Movements ◽  
Sensory Information ◽  
Saccadic Eye Movements ◽  
Direct Role ◽  
Unit Recording ◽  
Reversible Inactivation ◽  
Lateral Intraparietal Area ◽  
Upper Visual Field ◽  
Eye Field ◽  
Parietal Eye

Effect of reversible inactivation of macaque lateral intraparietal area on visual and memory saccades. Previous studies from our laboratory identified a parietal eye field in the primate lateral intraparietal sulcus, the lateral intraparietal area (area LIP). Here we further explore the role of area LIP in processing saccadic eye movements by observing the effects of reversible inactivation of this area. One to 2 μl of muscimol (8 mg/ml) were injected at locations where saccade-related activities were recorded for each lesion experiment. After the muscimol injection we observed in two macaque monkeys consistent effects on both the metrics and dynamics of saccadic eye movements at many injection sites. These effects usually took place within 10–30 min and disappeared after 5–6 h in most cases and certainly when tested the next day. After muscimol injection memory saccades directed toward the contralesional and upper space became hypometric, and in one monkey those to the ipsilesional space were slightly but significantly hypermetric. In some cases, the scatter of the end points of memory saccades was also increased. On the other hand, the metrics of visual saccades remained relatively intact. Latency for both visual and memory saccades toward the contralesional space was increased and in many cases displayed a higher variance after muscimol lesion. At many injection sites we also observed an increase of latency for visual and memory saccades toward the upper space. The peak velocities for memory saccades toward the contralesional space were decreased after muscimol injection. The peak velocities of visual saccades were not significantly different from those of the controls. The duration of saccadic eye movements either to the ipsilesional or contralesional space remained relatively the same for both visual and memory saccades. Overall these results demonstrated that we were able to selectively inactivate area LIP and observe effects on saccadic eye movements. Together with our previous recording studies these results futher support the view that area LIP plays a direct role in processing incoming sensory information to program saccadic eye movements. The results are consistent with our unit recording data and microstimulation studies, which suggest that area LIP represents contralateral space and also has a bias for the upper visual field.

Neural control of vergence eye movements: convergence and divergence neurons in midbrain

1984 ◽  
Vol 51 (5) ◽  
pp. 1091-1108 ◽  
Author(s):  
L. E. Mays
Keyword(s):  
Eye Movements ◽  
Firing Rate ◽  
Neural Control ◽  
Cell Activity ◽  
Mesencephalic Reticular Formation ◽  
Medial Rectus ◽  
Oculomotor Nucleus ◽  
Position Signal ◽  
Binocular Single Vision ◽  
Convergence And Divergence

Animals with binocular single vision use disjunctive (vergence) eye movements to align the two eyes on a visual target. Several lines of evidence suggest that conjugate and vergence eye movement commands are generated independently and combined at the medial rectus motoneurons. If this were true, then a pure vergence eye-position signal should exist. This signal would be proportional to the horizontal angle between the eyes (vergence angle), without regard to the direction of conjugate gaze. The purpose of this experiment was to identify and study neurons that carry a pure vergence signal. Extracellular unit recordings were made from midbrain and pontine sites in monkeys trained to track visual targets moving in the horizontal, vertical, and depth (or target vergence) planes. The most commonly encountered neuron that had a vergence signal was the convergence cell. These units had a firing rate that was linearly proportional to the convergence angle; their activity was unaffected by changes in conjugate gaze. Changes in convergence cell activity preceded the change in vergence angle slightly. Convergence cell activity increased for increased convergence regardless of whether the change was in response to purely accommodative or disparity cues. Divergence cells were found far less frequently. These cells were similar to convergence cells except that they decreased their firing rate for increases in convergence. The activity of divergence cells was unaffected by changes in the direction of conjugate gaze. Both convergence and divergence cells were found, intermixed, in the mesencephalic reticular formation must outside the oculomotor nucleus. Most cells with a vergence signal were found within 1-2 mm of the nucleus. These results support the view that conjugate and vergence signals are generated independently and are combined at the extraocular motoneurons. Convergence cells seem ideally suited to provide the vergence signal required by the nearby medial rectus motoneurons.

Existence in the nucleus incertus of the cat of horizontal-eye-movement-related neurons projecting to the cerebellar flocculus

1995 ◽  
Vol 74 (3) ◽  
pp. 1367-1372 ◽  
Author(s):  
G. Cheron ◽  
S. Saussez ◽  
N. Gerrits ◽  
E. Godaux
Keyword(s):  
Eye Movements ◽  
Eye Movement ◽  
Retrograde Transport ◽  
Great Sensitivity ◽  
Antidromic Activation ◽  
Vertical Movements ◽  
Cerebellar Flocculus ◽  
Nucleus Incertus ◽  
Alert Cats ◽  
Eye Velocity

1. Properties of nucleus incertus (NIC) neurons projecting to the cerebellar flocculus were studied in alert cats by using chronic unit and eye movement recording and antidromic activation. Projection of these neurons onto the flocculus was verified with retrograde transport of horseradish peroxidase after injections in the flocculus. 2. Bipolar stimulation electrodes were implanted into the "middle" zone of each flocculus because this zone is known to be involved in the control of horizontal eye movements. The dorsomedial aspect of the pontine tegmentum was explored with microelectrodes during stimulation of both flocculi. The majority of neurons antidromically activated from the flocculus were found in the caudal part of the NIC. 3. Of the 69 neurons activated from the flocculus, 44 were classified as burst-tonic (BT) neurons; 34 discharged in relation with horizontal movements of the eye, 10 in relation with vertical movements. Of the 14 remaining neurons, 6 were not related to eye movements and 8 were classified as burst neurons. The BT neurons of the NIC displayed a great sensitivity to both horizontal eye position and horizontal eye velocity. 4. This study demonstrates the presence of a new group of horizontal eye movement related BT neurons situated in the NIC. The fact that they project to the horizontal floccular zone emphasizes the importance of the functional specialization of the different Purkinje cell zones.

Lateral spread of neural excitation during microstimulation in intermediate gray layer of cat's superior colliculus

1982 ◽  
Vol 47 (2) ◽  
pp. 167-178 ◽  
Author(s):  
J. T. McIlwain
Keyword(s):  
Eye Movements ◽  
Superior Colliculus ◽  
Lateral Spread ◽  
Discharge Zone ◽  
Antidromic Activation ◽  
Distributed Coding ◽  
Pulse Generators ◽  
Spread Of Excitation ◽  
Train Length ◽  
Stimulus Site

1. Synaptically mediated spread of excitation has been studied during microstimulation in the intermediate gray layer of the superior colliculus of cats anesthetized with ketamine. Antidromic activation was used to identify those neurons sending axons to or through the contralateral pontine reticular formation. 2. Current thresholds were dependent on pulse duration, train length, and distance from the cell to the stimulus site. Stimulation with four cathodal pulses, 0.5 ms in duration, 30 microA in intensity, delivered at 400 Hz, excited cells of the intermediated gray up to 2-3 mm from the stimulus site. The results suggest that at least half the output cells in a region about 3 mm in diameter were driven by this stimulus. 3. The extent of spread in the unanesthetized midpontine-pretrigeminal cat was as great as, or greater than, that in animals anesthetized with ketamine. 4. Quick eye movements were evoked in ketamine-anesthetized cats by 100-ms trains of 0.5-ms pulses delivered at 400 Hz. Current thresholds for eye movements ranged from 15 to 90 microA, with most falling below 25 microA. 5. These results suggest that intracollicular microstimulation, with stimuli commonly used in studies of electrically evoked saccades, is accompanied by widespread synaptic activation of the intermediate gray layer. Since the metrics of electrically evoked saccades seem, nonetheless, to depend primarily on the location of the stimulating electrode, information about amplitude and direction must somehow be encoded in the distribution of neuronal discharge. 6. One possible form of such a distributed coding mechanism is discussed. This model assumes that the spatial densities of cells projecting to vertical and horizontal pulse generators of the saccadic system vary systematically beneath the retinotopic collicular map. Signals to the pulse generators change in magnitude as the collicular discharge zone occupies different positions in the connectional gradients and engages the specific output systems in varying proportion.

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
Keyword(s):  
Eye Movements ◽  
Firing Rate ◽  
Eye Movement ◽  
Vestibular Stimulation ◽  
Medial Rectus ◽  
Eye Position ◽  
Sensory Stimuli ◽  
Time Constants ◽  
Recruitment Threshold ◽  
Eye Blink

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)

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