Excitatory input from interneurons in the abducens nucleus to medial rectus motoneurons mediating conjugate horizontal nystagmus in the cat

1. Motoneurons innervating the cat retractor bulbi muscle have been identified by retrograde axonal transport of horseradish peroxidase (HRP). Following injections of the four slips of the retractor bulbi muscle, labeled motoneurons were found in the abducens nucleus overlapping the distribution of lateral rectus motoneurons and in the oculomotor nucleus partially overlapping the distribution of medial rectus motoneurons. Retractor bulbi motoneurons also were found in the accessory abducens nucleus situated ventral and lateral to the abducens nucleus. 2. Retractor bulbi motoneurons varied considerably in shape and size, but in all instances contained similar cytoplasmic organelles. Quantitative analyses of mean soma diameter indicated that the average size of retractor bulbi motoneurons was larger than the average size of lateral rectus and medial rectus motoneurons. 3. Retractor bulbi motoneurons in the accessory abducens nucleus were identified electrophysically and stained by intracellular injection of HRP. Neuronal reconstructions demonstrated a dorsomedial axonal trajectory directed toward the abducens nucleus and elongated dendritic fields oriented in a dorsomedial-ventrolateral axis. Another major dendritic extension was directed toward the magnocellular division of the spinal trigeminal nucleus, a major source of excitatory input to these motoneurons. 4. Quantitative analyses of synaptic density indicated that the somata of retractor bulbi motoneurons were contacted by significantly fewer synaptic endings than the somata of motoneurons in the abducens nucleus. Retractor bulbi motoneurons in the abducens nucleus exhibited variations in synaptic density that were similar to the densities on lateral rectus motoneurons. 5. Given the morphological differences in location, size, and somadendritic extent between motoneurons in the accessory abducens, abducens and oculomotor nuclei, it is suggested that such features reflect functional differences between the motoneurons with respect to fiber composition of the muscles they innervate, and subsequently to the role each muscle plays in eye movement. 6. Since the morphological features of retractor bulbi motoneurons in the accessory abducens nucleus are quite different from those in either the abducens or oculomotor nuclei, it appears that each motoneuronal population may perform unique oculomotor functions.

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

Journal of Neurophysiology ◽

10.1152/jn.1985.54.4.887 ◽

1985 ◽

Vol 54 (4) ◽

pp. 887-899 ◽

Cited By ~ 25

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)

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

Journal of Neurophysiology ◽

10.1152/jn.1994.71.3.1111 ◽

1994 ◽

Vol 71 (3) ◽

pp. 1111-1127 ◽

Cited By ~ 31

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)

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

Journal of Neurophysiology ◽

10.1152/jn.1988.60.6.1874 ◽

1988 ◽

Vol 60 (6) ◽

pp. 1874-1895 ◽

Cited By ~ 130

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)

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Excitatory termination of abducens internuclear neurons on medial rectus motoneurons: relationship to syndrome of internuclear ophthalmoplegia

Journal of Neurophysiology ◽

10.1152/jn.1978.41.6.1647 ◽

1978 ◽

Vol 41 (6) ◽

pp. 1647-1661 ◽

Cited By ~ 105

Author(s):

S. M. Highstein ◽

R. Baker

Keyword(s):

Brain Stem ◽

Nerve Stimulation ◽

Physiological Activity ◽

Vestibular Nerve ◽

Medial Rectus ◽

Medial Longitudinal Fasciculus ◽

Internuclear Ophthalmoplegia ◽

Field Potentials ◽

Abducens Nucleus ◽

Stimulation Of

1. Field potentials and intracellular records were obtained from the medial rectus subdivision of the IIIrd nucleus in anesthetized cats following electrical stimulation of the abducens nuclei, vestibular nerves, pontomedullary brain stem, and the medial longitudinal fasciculi (MLF). 2. Stimulation of the contralateral abducens nucleus produced unique field potentials in the medial rectus subdivision. They consisted of an early sharp transient volley followed by a slower postsynaptic negativity. 3. Monosynaptic EPSPs were evoked in medial rectus motoneurons following contralateral abducens nucleus stimulation. The EPSP amplitudes were graded when the stimulus intensity was increased from threshold to supramaximal. EPSPs produced by contralateral abducens nucleus stimulation were larger in amplitude than those produced by ipsilateral vestibular nerve stimulation. The current-voltage relationship and reversal potentials for Vi- and abducens-evoked EPSPs were similar and indicated an overlapping location of excitatory synaptic terminals on medial rectus motoneurons. 4. Secondary vestibular axons activated monosynaptically by ipsilateral vestibular nerve stimulation were not recruited by abducens nucleus stimulation. 5. Ipsilateral MLF stimulation produced EPSPs with similar profiles as those observed following abducens nucleus stimulation; however, stimulation of the contralateral MLF at comparable stimulus intensities did not produce any changes in transmembrane potential. 6. When higher intensity stimuli were applied to the contralateral MLF, the synaptic potentials recorded in the medial rectus were occluded by those produced by weaker stimulation applied to the ipsilateral MLF. This suggests that the potentials resulting from stronger contralateral stimulation were due to current spread to the ipsilateral MLF. 7. While recording in the medial rectus subdivision, various sites in the ponto-medullary brain stem were explored with a stimulating electrode. Analysis of evoked field potentials suggested that the ascending internuclear axons were contained only in the MLF ipsilateral to the medial rectus. Acute brain stem lesions confirmed this suggestion. 8. Chronic lesions were placed in the brain stem to isolate the abducens nucleus from either extrinsic fibers of passage or axon collaterals. Acute electrophysiological experiments in these chronic animals corroborated the suggestion that the medial rectus pathway originated from within the abducens nucleus. 9. We conclude that axons from the internuclear neurons of the abducens nucleus exit from the nucleus medially, cross the midline, ascend in the opposite MLF, and terminate monosynaptically on medial rectus motoneurons. 10. we believe that the syndrome of internuclear ophthalmoplegia associated clinically with lesions of the medial longitudinal fasciculus could be due to the absence of ascending physiological activity from internuclear neurons of the abducens nucleus.

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