Effects of Ibotenic Acid Lesions of Nucleus Prepositus Hypoglossi on Optokinetic and Vestibular Eye Movements in the Alert, Trained Monkey

1992 ◽  
Vol 656 (1 Sensing and C) ◽  
pp. 408-427 ◽  
Author(s):  
CHRIS R. S. KANEKO
Keyword(s):  
Eye Movements ◽  
Ibotenic Acid ◽  
Nucleus Prepositus Hypoglossi ◽  
Prepositus Hypoglossi

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

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

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

Eye Movement Deficits After Ibotenic Acid Lesions of the Nucleus Prepositus Hypoglossi in Monkeys. I. Saccades and Fixation

1997 ◽  
Vol 78 (4) ◽  
pp. 1753-1768 ◽  
Author(s):  
Chris R. S. Kaneko
Keyword(s):  
Eye Movement ◽  
Rhesus Macaques ◽  
Ibotenic Acid ◽  
Feedback Signal ◽  
Neural Integrator ◽  
Nucleus Prepositus Hypoglossi ◽  
System A ◽  
Classical Models ◽  
Prepositus Hypoglossi ◽  
Made In

Kaneko, Chris R. S. Eye movement deficits after ibotenic acid lesions of the nucleus prepositus hypoglossi in monkeys. I. Saccades and fixation. J. Neurophysiol. 78: 1753–1768, 1997. It has been suggested that the function of the nucleus prepositus hypoglossi (nph) is the mathematical integration of velocity-coded signals to produce position-coded commands that drive abducens motoneurons and generate horizontal eye movements. In early models of the saccadic system, a single integrator provided not only the signal that maintained steady gaze after a saccade but also an efference copy of eye position, which provided a feedback signal to control the dynamics of the saccade. In this study, permanent, serial ibotenic acid lesions were made in the nph of three rhesus macaques, and their effects were studied while the alert monkeys performed a visual tracking task. Localized damage to the nph was confirmed in both Nissl and immunohistochemically stained material. The lesions clearly were correlated with long-lasting deficits in eye movement. The animals' ability to fixate in the dark was compromised quickly and uniformly so that saccades to peripheral locations were followed by postsaccadic centripetal drift. The time constant of the drift decreased to approximately one-tenth of its normal values but remained 10 times longer than that attributable to the mechanics of the eye. In contrast, saccades were affected minimally. The results are more consistent with models of the neural saccade generator that use separate feedback and position integrators than with the classical models, which use a single multipurpose element. Likewise, the data contradict models that rely on feedback from the nph. In addition, they show that the oculomotor neural integrator is not a single neural entity but is most likely distributed among a number of nuclei.

Discharge Dynamics of Oculomotor Neural Integrator Neurons During Conjugate and Disjunctive Saccades and Fixation

2003 ◽  
Vol 90 (2) ◽  
pp. 739-754 ◽  
Author(s):  
Pierre A. Sylvestre ◽  
Julia T. L. Choi ◽  
Kathleen E. Cullen
Keyword(s):  
Eye Movements ◽  
Vestibular Nucleus ◽  
Vestibular Nuclei ◽  
Medial Vestibular Nucleus ◽  
Eye Position ◽  
Neural Integrator ◽  
Abducens Nucleus ◽  
Nucleus Prepositus Hypoglossi ◽  
Prepositus Hypoglossi ◽  
Eye Velocity

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.

Smooth-Pursuit Eye-Movement Deficits With Chemical Lesions in Macaque Nucleus Reticularis Tegmenti Pontis

1999 ◽  
Vol 82 (3) ◽  
pp. 1178-1186 ◽  
Author(s):  
David A. Suzuki ◽  
Tetsuto Yamada ◽  
Rebecca Hoedema ◽  
Robert D. Yee
Keyword(s):  
Eye Movements ◽  
Smooth Pursuit ◽  
Ibotenic Acid ◽  
Frontal Eye Field ◽  
Smooth Pursuit Eye Movements ◽  
Pontine Nucleus ◽  
Nucleus Reticularis Tegmenti Pontis ◽  
Pursuit Eye Movements ◽  
Nucleus Reticularis ◽  
Dorsolateral Pontine Nucleus

Anatomic and neuronal recordings suggest that the nucleus reticularis tegmenti pontis (NRTP) of macaques may be a major pontine component of a cortico-ponto-cerebellar pathway that subserves the control of smooth-pursuit eye movements. The existence of such a pathway was implicated by the lack of permanent pursuit impairment after bilateral lesions in the dorsolateral pontine nucleus. To provide more direct evidence that NRTP is involved with regulating smooth-pursuit eye movements, chemical lesions were made in macaque NRTP by injecting either lidocaine or ibotenic acid. Injection sites first were identified by the recording of smooth-pursuit-related modulations in neuronal activity. The resulting lesions caused significant deficits in both the maintenance and the initiation of smooth-pursuit eye movements. After lesion formation, the gain of constant-velocity, maintained smooth-pursuit eye movements decreased, on the average, by 44%. Recovery of the ability to maintain smooth-pursuit eye movements occurred over ∼3 days when maintained pursuit gains attained normal values. The step-ramp, “Rashbass” task was used to investigate the effects of the lesions on the initiation of smooth-pursuit eye movements. Eye accelerations averaged over the initial 80 ms of pursuit initiation were determined and found to be decremented, on the average, by 48% after the administration of ibotenic acid. Impairments in the initiation and maintenance of smooth-pursuit eye movements were directional in nature. Upward pursuit seemed to be the most vulnerable and was impaired in all cases independent of lesioning agent and type of pursuit investigated. Downward smooth pursuit seemed more resistant to the effects of chemical lesions in NRTP. Impairments in horizontal tracking were observed with examples of deficits in ipsilaterally and contralaterally directed pursuit. The results provide behavioral support for the physiologically and anatomic-based conclusion that NRTP is a component of a cortico-ponto-cerebellar circuit that presumably involves the pursuit area of the frontal eye field (FEF) and projects to ocular motor-related areas of the cerebellum. This FEF-NRTP-cerebellum path would parallel a middle and medial superior temporal cerebral cortical area-dorsolateral pontine nucleus-cerebellum pathway also known to be involved with regulating smooth-pursuit eye movements.

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

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

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

Pursuit and optokinetic deficits following chemical lesions of cortical areas MT and MST

1988 ◽  
Vol 60 (3) ◽  
pp. 940-965 ◽  
Author(s):  
M. R. Dursteler ◽  
R. H. Wurtz
Keyword(s):  
Eye Movements ◽  
Visual Field ◽  
Visual Motion ◽  
Ibotenic Acid ◽  
Motion Processing ◽  
Temporal Area ◽  
Target Speed ◽  
Pursuit Eye Movements ◽  
Medial Superior Temporal ◽  
Visual Motion Processing

1. Previous experiments have shown that punctate chemical lesions within the middle temporal area (MT) of the superior temporal sulcus (STS) produce deficits in the initiation and maintenance of pursuit eye movements (10, 34). The present experiments were designed to test the effect of such chemical lesions in an area within the STS to which MT projects, the medial superior temporal area (MST). 2. We injected ibotenic acid into localized regions of MST, and we observed two deficits in pursuit eye movements, a retinotopic deficit and a directional deficit. 3. The retinotopic deficit in pursuit initiation was characterized by the monkey's inability to match eye speed to target speed or to adjust the amplitude of the saccade made to acquire the target to compensate for target motion. This deficit was related to the initiation of pursuit to targets moving in any direction in the visual field contralateral to the side of the brain with the lesion. This deficit was similar to the deficit we found following damage to extrafoveal MT except that the affected area of the visual field frequently extended throughout the entire contralateral visual field tested. 4. The directional deficit in pursuit maintenance was characterized by a failure to match eye speed to target speed once the fovea had been brought near the moving target. This deficit occurred only when the target was moving toward the side of the lesion, regardless of whether the target began to move in the ipsilateral or contralateral visual field. There was no deficit in the amplitude of saccades made to acquire the target, or in the amplitude of the catch-up saccades made to compensate for the slowed pursuit. The directional deficit is similar to the one we described previously following chemical lesions of the foveal representation in the STS. 5. Retinotopic deficits resulted from any of our injections in MST. Directional deficits resulted from lesions limited to subregions within MST, particularly lesions that invaded the floor of the STS and the posterior bank of the STS just lateral to MT. Extensive damage to the densely myelinated area of the anterior bank or to the posterior parietal area on the dorsal lip of the anterior bank produced minimal directional deficits. 6. We conclude that damage to visual motion processing in MST underlies the retinotopic pursuit deficit just as it does in MT. MST appears to be a sequential step in visual motion processing that occurs before all of the visual motion information is transmitted to the brainstem areas related to pursuit.(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.

scholarly journals Vestibular Imbalance Associated With a Lesion in the Nucleus Prepositus Hypoglossi Area

2004 ◽  
Vol 61 (9) ◽  
pp. 1440 ◽  
Author(s):  
Sang Won Seo ◽  
Ha Young Shin ◽  
Seo Hyun Kim ◽  
Sang Won Han ◽  
Kyung Yul Lee ◽  
...  
Keyword(s):  
Nucleus Prepositus Hypoglossi ◽  
Prepositus Hypoglossi
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