Convergent synaptic inputs from the caudal fastigial nucleus and the superior colliculus onto pontine and pontomedullary reticulospinal neurons

2014 ◽  
Vol 111 (4) ◽  
pp. 849-867 ◽  
Author(s):  
Mayu Takahashi ◽  
Yuriko Sugiuchi ◽  
Yoshikazu Shinoda
Keyword(s):  
Superior Colliculus ◽  
Head Movements ◽  
Fastigial Nucleus ◽  
Cervical Cord ◽  
Abducens Nucleus ◽  
Reticulospinal Neurons ◽  
Nucleus Reticularis ◽  
Caudal Portion ◽  
Reticular Neurons ◽  
Monosynaptic Excitation

The caudal fastigial nucleus (FN) is known to be related to the control of eye movements and projects mainly to the contralateral reticular nuclei where excitatory and inhibitory burst neurons for saccades exist [the caudal portion of the nucleus reticularis pontis caudalis (NRPc), and the rostral portion of the nucleus reticularis gigantocellularis (NRG) respectively]. However, the exact reticular neurons targeted by caudal fastigioreticular cells remain unknown. We tried to determine the target reticular neurons of the caudal FN and superior colliculus (SC) by recording intracellular potentials from neurons in the NRPc and NRG of anesthetized cats. Neurons in the rostral NRG received bilateral, monosynaptic excitation from the caudal FNs, with contralateral predominance. They also received strong monosynaptic excitation from the rostral and caudal contralateral SC, and disynaptic excitation from the rostral ipsilateral SC. These reticular neurons with caudal fastigial monosynaptic excitation were not activated antidromically from the contralateral abducens nucleus, but most of them were reticulospinal neurons (RSNs) that were activated antidromically from the cervical cord. RSNs in the caudal NRPc received very weak monosynaptic excitation from only the contralateral caudal FN, and received either monosynaptic excitation only from the contralateral caudal SC, or monosynaptic and disynaptic excitation from the contralateral caudal and ipsilateral rostral SC, respectively. These results suggest that the caudal FN helps to control also head movements via RSNs targeted by the SC, and these RSNs with SC topographic input play different functional roles in head movements.

Anatomy and physiology of saccadic long-lead burst neurons recorded in the alert squirrel monkey. II. Pontine neurons

1996 ◽  
Vol 76 (1) ◽  
pp. 353-370 ◽  
Author(s):  
C. A. Scudder ◽  
A. K. Moschovakis ◽  
A. B. Karabelas ◽  
S. M. Highstein
Keyword(s):  
Superior Colliculus ◽  
Brain Stem ◽  
Reticular Formation ◽  
Reticulospinal Neurons ◽  
Burst Neurons ◽  
Nucleus Reticularis ◽  
Discharge Patterns ◽  
The Brain ◽  
Saccade Generation

1. The discharge patterns and axonal projections of saccadic long-lead burst neurons (LLBNs) with somata in the pontine reticular formation were studied in alert squirrel monkeys with the use of the method of intraaxonal recording and horseradish peroxidase injection. 2. The largest population of stained neurons were afferents to the cerebellum. They originated in the dorsomedial nucleus reticularis tegmenti pontis (NRTP) including its dorsal cell group (N = 5), the preabducens intrafascicular nucleus (N = 5), and the raphe pontis (N = 1). Axons of all neurons coursed under NRTP and entered brachium pontis without having synapsed in the brain stem. Three axons sent collaterals to the floccular lobe, but other more distant targets of these and the other cerebellar afferents could not be determined. Movement fields of these neurons were intermediate between vectorial and directional types. 3. Four neurons had their somata in nucleus reticularis pontis oralis and terminations in the brain stem reticular formation. Each neuron was different, but all terminated in the region containing excitatory burst neurons, and most terminated in the region containing inhibitory burst neurons. Other targets include nucleus reticularis pontis oralis and caudalis, NRTP, raphe interpositus, and the spinal cord. Discharge patterns included both vectorial and directional types. 4. Two reticulospinal neurons had large multipolar somata either just rostral or ventral to the abducens nucleus. These neurons also projected to the medullary reticular formation, caudal nucleus prepositus hypoglossi, and dorsal and ventral paramedian reticular nucleus. 5. The functional implications of the connections of these LLBNs and those reported in the companion paper are extensively discussed. The fact that the efferents of the superior colliculus target the regions containing medium-lead saccadic burst neurons confirms the role of the colliculus in saccade generation. However, the finding that many other neurons project to these regions and the finding that superior colliculus efferents project more heavily to areas containing reticulospinal neurons argue for a diminished role of the superior colliculus in saccade generation but an augmented role in head movement control.

Neck Muscle Responses to Stimulation of Monkey Superior Colliculus. II. Gaze Shift Initiation and Volitional Head Movements

2002 ◽  
Vol 88 (4) ◽  
pp. 2000-2018 ◽  
Author(s):  
Brian D. Corneil ◽  
Etienne Olivier ◽  
Douglas P. Munoz
Keyword(s):  
Superior Colliculus ◽  
Neck Muscles ◽  
Head Movements ◽  
Emg Activity ◽  
Neck Muscle ◽  
Gaze Shift ◽  
Antagonist Muscles ◽  
Agonist And Antagonist ◽  
Agonist And Antagonist Muscles ◽  
Stimulation Of

We report neck muscle activity and head movements evoked by electrical stimulation of the superior colliculus (SC) in head-unrestrained monkeys. Recording neck electromyography (EMG) circumvents complications arising from the head's inertia and the kinetics of muscle force generation and allows precise assessment of the neuromuscular drive to the head plant. This study served two main purposes. First, we sought to test the predictions made in the companion paper of a parallel drive from the SC onto neck muscles. Low-current, long-duration stimulation evoked both neck EMG responses and head movements either without or prior to gaze shifts, testifying to a SC drive to neck muscles that is independent of gaze-shift initiation. However, gaze-shift initiation was linked to a transient additional EMG response and head acceleration, confirming the presence of a SC drive to neck muscles that is dependent on gaze-shift initiation. We forward a conceptual neural architecture and suggest that this parallel drive provides the oculomotor system with the flexibility to orient the eyes and head independently or together, depending on the behavioral context. Second, we compared the EMG responses evoked by SC stimulation to those that accompanied volitional head movements. We found characteristic features in the underlying pattern of evoked neck EMG that were not observed during volitional head movements in spite of the seemingly natural kinematics of evoked head movements. These features included reciprocal patterning of EMG activity on the agonist and antagonist muscles during stimulation, a poststimulation increase in the activity of antagonist muscles, and synchronously evoked responses on agonist and antagonist muscles regardless of initial horizontal head position. These results demonstrate that the electrically evoked SC drive to the head cannot be considered as a neural replicate of the SC drive during volitional head movements and place important new constraints on the interpretation of electrically evoked head movements.

Head-Unrestrained Gaze Shifts After Muscimol Injection in the Caudal Fastigial Nucleus of the Monkey

2007 ◽  
Vol 98 (6) ◽  
pp. 3269-3283 ◽  
Author(s):  
Julie Quinet ◽  
Laurent Goffart
Keyword(s):  
Feedback Control ◽  
Head Movement ◽  
Peak Velocity ◽  
Head Movements ◽  
Fastigial Nucleus ◽  
Gaze Shifts ◽  
Movement Accuracy ◽  
Central Target ◽  
Target Eccentricity ◽  
Vertical Gaze

The effects of unilateral cFN inactivation on horizontal and vertical gaze shifts generated from a central target toward peripheral ones were tested in two head unrestrained monkeys. After muscimol injection, the eye component was hypermetric during ipsilesional gaze shifts, hypometric during contralesional ones and deviated toward the injected side during vertical gaze shifts. The ipsilesional gaze hypermetria increased with target eccentricity until ∼24° after which it diminished and became smaller than the hypermetria of the eye component. Contrary to eye saccades, the amplitude and peak velocity of which were enhanced, the amplitude and peak velocity of head movements were reduced during ipsilesional gaze shifts. These changes in head movement were not correlated with those affecting the eye saccades. Head movements were also delayed relative to the onset of eye saccades. The alterations in head movement and the faster eye saccades likely explained the reduced head contribution to the amplitude of ipsilesional gaze shifts. The contralesional gaze hypometria increased with target eccentricity and was associated with uncorrelated reductions in eye and head peak velocities. When compared with control movements of similar amplitude, contralesional eye saccades had lower peak velocity and longer duration. This slowing likely accounted for the increase in head contribution to the amplitude of contralesional gaze shifts. These data suggest different pathways for the fastigial control of eye and head components during gaze shifts. Saccade dysmetria was not compensated by appropriate changes in head contribution, raising the issue of the feedback control of movement accuracy during combined eye-head gaze shifts.

scholarly journals Matching the Oculomotor Drive During Head-Restrained and Head-Unrestrained Gaze Shifts in Monkey

2010 ◽  
Vol 104 (2) ◽  
pp. 811-828 ◽  
Author(s):  
Bernard P. Bechara ◽  
Neeraj J. Gandhi
Keyword(s):  
Mean Squared Error ◽  
Vestibular Nuclei ◽  
Cell Types ◽  
Head Movements ◽  
Abducens Nucleus ◽  
Gaze Shifts ◽  
Gaze Shift ◽  
Head Velocity ◽  
Burst Neurons ◽  
Eye Velocity

High-frequency burst neurons in the pons provide the eye velocity command (equivalently, the primary oculomotor drive) to the abducens nucleus for generation of the horizontal component of both head-restrained (HR) and head-unrestrained (HU) gaze shifts. We sought to characterize how gaze and its eye-in-head component differ when an “identical” oculomotor drive is used to produce HR and HU movements. To address this objective, the activities of pontine burst neurons were recorded during horizontal HR and HU gaze shifts. The burst profile recorded on each HU trial was compared with the burst waveform of every HR trial obtained for the same neuron. The oculomotor drive was assumed to be comparable for the pair yielding the lowest root-mean-squared error. For matched pairs of HR and HU trials, the peak eye-in-head velocity was substantially smaller in the HU condition, and the reduction was usually greater than the peak head velocity of the HU trial. A time-varying attenuation index, defined as the difference in HR and HU eye velocity waveforms divided by head velocity [α = ( Ḣhr − Ėhu)/ Ḣ] was computed. The index was variable at the onset of the gaze shift, but it settled at values several times greater than 1. The index then decreased gradually during the movement and stabilized at 1 around the end of gaze shift. These results imply that substantial attenuation in eye velocity occurs, at least partially, downstream of the burst neurons. We speculate on the potential roles of burst-tonic neurons in the neural integrator and various cell types in the vestibular nuclei in mediating the attenuation in eye velocity in the presence of head movements.

Contribution of Head Movement to Gaze Command Coding in Monkey Frontal Cortex and Superior Colliculus

2003 ◽  
Vol 90 (4) ◽  
pp. 2770-2776 ◽  
Author(s):  
Julio C. Martinez-Trujillo ◽  
Eliana M. Klier ◽  
Hongying Wang ◽  
J. Douglas Crawford
Keyword(s):  
Superior Colliculus ◽  
Neural Control ◽  
Significant Contribution ◽  
Head Movements ◽  
Vector Model ◽  
Gaze Control ◽  
Gaze Shift ◽  
Visual Model ◽  
The Gaze ◽  
Supplementary Eye Fields

Most of what we know about the neural control of gaze comes from experiments in head-fixed animals, but several “head-free” studies have suggested that fixing the head dramatically alters the apparent gaze command. We directly investigated this issue by quantitatively comparing head-fixed and head-free gaze trajectories evoked by electrically stimulating 52 sites in the superior colliculus (SC) of two monkeys and 23 sites in the supplementary eye fields (SEF) of two other monkeys. We found that head movements made a significant contribution to gaze shifts evoked from both neural structures. In the majority of the stimulated sites, average gaze amplitude was significantly larger and individual gaze trajectories were significantly less convergent in space with the head free to move. Our results are consistent with the hypothesis that head-fixed stimulation only reveals the oculomotor component of the gaze shift, not the true, planned goal of the movement. One implication of this finding is that when comparing stimulation data against popular gaze control models, freeing the head shifts the apparent coding of gaze away from a “spatial code” toward a simpler visual model in the SC and toward an eye-centered or fixed-vector model representation in the SEF.

Neural Organization of the Pathways From the Superior Colliculus to Trochlear Motoneurons

2007 ◽  
Vol 97 (5) ◽  
pp. 3696-3712 ◽  
Author(s):  
Yoshiko Izawa ◽  
Yuriko Sugiuchi ◽  
Yoshikazu Shinoda
Keyword(s):  
Superior Colliculus ◽  
Interstitial Nucleus Of Cajal ◽  
Saccadic System ◽  
Neural Organization ◽  
Premotor Neurons ◽  
Monosynaptic Inhibition ◽  
Disynaptic Inhibition ◽  
Forel's Field H ◽  
Stimulation Of ◽  
Monosynaptic Excitation

The neural organization of the pathways from the superior colliculus (SC) to trochlear motoneurons was analyzed in anesthetized cats using intracellular recording and transneuronal labeling techniques. Stimulation of the ipsilateral or contralateral SC evoked excitation and inhibition in trochlear motoneurons with latencies of 1.1–2.3 and 1.1–3.8 ms, respectively, suggesting that the earliest components of excitation and inhibition were disynaptic. A midline section between the two SCs revealed that ipsi- and contralateral SC stimulation evoked disynaptic excitation and inhibition in trochlear motoneurons, respectively. Premotor neurons labeled transneuronally after application of wheat germ agglutinin-conjugated horseradish peroxidase into the trochlear nerve were mainly distributed ipsilaterally in the Forel's field H (FFH) and bilaterally in the interstitial nucleus of Cajal (INC). Consequently, we investigated these two likely intermediaries between the SC and trochlear nucleus electrophysiologically. Stimulation of the FFH evoked ipsilateral mono- and disynaptic excitation and contralateral disynaptic inhibition in trochlear motoneurons. Preconditioning stimulation of the ipsilateral SC facilitated FFH-evoked monosynaptic excitation. Stimulation of the INC evoked ipsilateral monosynaptic excitation and inhibition, and contralateral monosynaptic inhibition in trochlear motoneurons. Preconditioning stimulation of the contralateral SC facilitated contralateral INC-evoked monosynaptic inhibition. These results revealed a reciprocal input pattern from the SCs to vertical ocular motoneurons in the saccadic system; trochlear motoneurons received disynaptic excitation from the ipsilateral SC via ipsilateral FFH neurons and disynaptic inhibition from the contralateral SC via contralateral INC neurons. These inhibitory INC neurons were considered to be a counterpart of inhibitory burst neurons in the horizontal saccadic system.

Gaze-related activity of putative inhibitory burst neurons in the head-free cat

1993 ◽  
Vol 70 (6) ◽  
pp. 2678-2683 ◽  
Author(s):  
K. E. Cullen ◽  
D. Guitton ◽  
C. G. Rey ◽  
W. Jiang
Keyword(s):  
The Body ◽  
Head Movements ◽  
Related Activity ◽  
Visual Axis ◽  
Abducens Nucleus ◽  
Gaze Shifts ◽  
Burst Neurons ◽  
The Gaze ◽  
Output Neurons ◽  
The Relationship

1. Previous studies in the cat have demonstrated that output neurons of the superior collicular as well as brain stem omnipause neurons have discharges that are best correlated, not with the trajectory of the eye in the head but, with the trajectory of the visual axis in space (gaze = eye-in-head + head-in-space) during rapid orienting coordinated eye and head movements. In this study, we describe the gaze-related activity of cat premotor “inhibitory burst neurons”(IBNs) identified on the basis of their position relative to the abducens nucleus. 2. The firing behavior of IBNs was studied during 1) saccades made with the head stationary, 2) active orienting combined eye-head gaze shifts, and 3) passive movements of the head on the body. IBN discharges were well correlated with the duration and amplitude of saccades made when the head was stationary. In both head-free paradigms, the behavior of cat IBNs differed from that of previously described primate “saccade bursters”. The duration of their burst was better correlated with gaze than saccade duration, and the total number of spikes in a burst was well correlated with gaze amplitude and generally poorly correlated with saccade amplitude. The behavior of cat IBNs also differed from that of previously described primate “gaze bursters”. The slope of the relationship between the total number of spikes and gaze amplitude observed during head-free gaze shifts was significantly lower than that observed during head-fixed saccades. 3. These studies suggest that cat IBNs do not fit into the categories of gaze-bursters or saccade-bursters that have been described in primate studies.(ABSTRACT TRUNCATED AT 250 WORDS)

Physiological Characterization of Synaptic Inputs to Inhibitory Burst Neurons From the Rostral and Caudal Superior Colliculus

2005 ◽  
Vol 93 (2) ◽  
pp. 697-712 ◽  
Author(s):  
Y. Sugiuchi ◽  
Y. Izawa ◽  
M. Takahashi ◽  
J. Na ◽  
Y. Shinoda
Keyword(s):  
Superior Colliculus ◽  
Abducens Nucleus ◽  
Antidromic Activation ◽  
Synaptic Inputs ◽  
Burst Neurons ◽  
Physiological Characterization ◽  
Monosynaptic Inhibition ◽  
Disynaptic Inhibition ◽  
Stimulation Of

The caudal superior colliculus (SC) contains movement neurons that fire during saccades and the rostral SC contains fixation neurons that fire during visual fixation, suggesting potentially different functions for these 2 regions. To study whether these areas might have different projections, we characterized synaptic inputs from the rostral and caudal SC to inhibitory burst neurons (IBNs) in anesthetized cats. We recorded intracellular potentials from neurons in the IBN region and identified them as IBNs based on their antidromic activation from the contralateral abducens nucleus and short-latency excitation from the contralateral caudal SC and/or single-cell morphology. IBNs received disynaptic inhibition from the ipsilateral caudal SC and disynaptic inhibition from the rostral SC on both sides. Stimulation of the contralateral IBN region evoked monosynaptic inhibition in IBNs, which was enhanced by preconditioning stimulation of the ipsilateral caudal SC. A midline section between the IBN regions eliminated inhibition from the ipsilateral caudal SC, but inhibition from the rostral SC remained unaffected, indicating that the latter inhibition was mediated by inhibitory interneurons other than IBNs. A transverse section of the brain stem rostral to the pause neuron (PN) region eliminated inhibition from the rostral SC, suggesting that this inhibition is mediated by PNs. These results indicate that the most rostral SC inhibits bilateral IBNs, most likely via PNs, and the more caudal SC exerts monosynaptic excitation on contralateral IBNs and antagonistic inhibition on ipsilateral IBNs via contralateral IBNs. The most rostral SC may play roles in maintaining fixation by inhibition of burst neurons and facilitating saccadic initiation by releasing their inhibition.

Sign in / Sign up

Export Citation Format

Share Document