The perihypoglossal projection to the superior colliculus in the rhesus monkey

1990 ◽  
Vol 4 (1) ◽  
pp. 29-42 ◽  
Author(s):  
Rosi Hartwich-Young ◽  
Jon S. Nelson ◽  
David L. Sparks

AbstractThe projection of the perihypoglossal (PH) complex to the superior colliculus (SC) in the rhesus monkey was investigated using the retrograde transport of wheat germ agglutinin conjugated to horseradish peroxidase (WGA-HRP). Following physiological identification by electrical stimulation and multiunit recording, small injections of the tracer were placed within the SC of three monkeys. The largest numbers of retrogradely labeled neurons within the PH complex were found in the contralateral nucleus prepositus hypoglossi (NPH), in the laterally adjacent medial vestibular nucleus, and in the ventrally adjacent reticular formation (the nucleus reticularis supragigantocellularis). These labeled neurons are strikingly heterogeneous in size and morphology. The nuclei supragenualis and intercalatus also contain numerous labeled neurons in the 2 cases in which the injections involve the caudal SC. Large numbers of retrogradely labeled neurons as well as anterogradely transported WGA-HRP are observed alo throughout the pontine and medullary reticular formation, including the midline raphe. The PH complex, particularly the NPH, is known to be involved in the coding of eye position and has been hypothesized to be a critical component of the “neural integrator.” Our data demonstrate the existence of a robust projection from the PH complex to the contralateral SC in the rhesus monkey. This projection may serve as the anatomical substrate by which a corollary of eye position could reach the SC. Such a signal is a prerequisite for the computation, at the collicular level, of saccadic motor error signals observed in the SC of rhesus monkeys.

1992 ◽  
Vol 68 (1) ◽  
pp. 319-332 ◽  
Author(s):  
J. L. McFarland ◽  
A. F. Fuchs

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)


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.


1994 ◽  
Vol 72 (6) ◽  
pp. 2754-2770 ◽  
Author(s):  
E. L. Keller ◽  
J. A. Edelman

1. We recorded the spatial and temporal dynamics of saccade-related burst neurons (SRBNs) found in the intermediate layers of the superior colliculus (SC) in the alert, behaving monkey. These burst cells are normally the first neurons recorded during radially directed microelectrode penetrations of the SC after the electrode has left the more dorsally situated visual layers. They have spatially delimited movement fields whose centers describe the well-studied motor map of the SC. They have a rather sharp, saccade-locked burst of activity that peaks just before saccade onset and then declines steeply during the saccade. Many of these cells, when recorded during saccade trials, also have an early, transient visual response and an irregular prelude of presaccadic activity. 2. Because saccadic eye movements normally have very stereotyped durations and velocity trajectories that vary systematically with saccade size, it has been difficult in the past to establish quantitatively whether the activity of SRBNs temporally codes dynamic saccadic control signals, e.g., dynamic motor error or eye velocity, where dynamic motor error is defined as a signal proportional to the instantaneous difference between desired final eye position and the actual eye position during a saccade. It has also not been unequivocally established whether SRBNs participate in an organized spatial shift of ensemble activity in the intermediate layers of the SC during saccadic eye movements. 3. To address these issues, we studied the activity of SRBNs using an interrupted saccade paradigm. Saccades were interrupted with pulsatile electrical stimulation through a microelectrode implanted in the omnipauser region of the brain stem while recordings were made simultaneously from single SRBNs in the SC. 4. Shortly after the beginning of the stimulation (which was electronically triggered at saccade onset), the eyes decelerated rapidly and stopped completely. When the high-frequency (typically 300-400 pulses per second) stimulation was terminated (average duration 12 ms), the eye movement was reinitiated and a resumed saccade was made accurately to the location of the target. 5. When we recorded from SRBNs in the more caudal colliculus, which were active for large saccades, cell discharge was powerfully and rapidly suppressed by the stimulation (average latency = 3.8 ms). Activity in the same cells started again just before the onset of the resumed saccade and continued during this saccade even though it has a much smaller amplitude than would normally be associated with significant discharge for caudal SC cells.(ABSTRACT TRUNCATED AT 400 WORDS)


2000 ◽  
Vol 10 (2) ◽  
pp. 107-117
Author(s):  
DeWana R. Kerr ◽  
Andrew J. Sansom ◽  
Paul F. Smith ◽  
Cynthia L. Darlington

The aim of the present study was to compare in vitro protein expression, protein kinase activity and protein phosphorylation in the medial vestibular nucleus (MVN) and prepositus hypoglossi (PH) from labyrinthine-intact guinea pigs and from guinea pigs at various stages of vestibular compensation following unilateral labyrinthectomy (UL). The ipsilateral (I-MVN) and contralateral (C-MVN) MVN, and the ipsilateral (I-PH) and contralateral (C-PH) PH, were dissected from 3 naive labyrinthine-intact guinea pigs and 55 guinea pigs at 10 hs or 53 hs following a surgical UL or sham operation. Tissue extracts were incubated with [gamma- 33 P]ATP ± Ca 2 + , phorbal 12, 13 dibutyrate and phosphatidylserine or ± Ca 2 + and calmodulin, to enhance protein kinase C (PKC) or calcium calmodulin kinase (CaMK) activity, respectively. Data were analysed as the ratio of activated to basal 33 P incorporation detected by phosphorimaging. There were similar total protein and phosphoprotein profiles in the MVN and PH, as well as both PKC and CaMKII activity, suggesting that the MVN and PH are similar in the way that proteins undergo rapid modification by phosphorylation. During the development of vestibular compensation, a 46 kDa band in C-PH displayed higher PKC-mediated phosphorylation from 10 hs post-UL compared to sham controls. Significantly greater PKC-mediated phosphorylation of proteins of approximately 18, 46 and 75 kDa was observed in C-PH at 10 hs compared to 53 hs post-UL and in most cases the phosphorylation was greater in C-PH than in the C-MVN. These results suggest that between 10 and 53 hs post-UL, PKC-mediated phosphorylation changes mainly in the C-PH rather than the ipsilateral or contralateral MVN.


1975 ◽  
Vol 38 (6) ◽  
pp. 1421-1435 ◽  
Author(s):  
B. W. Peterson ◽  
C. Abzug

In one series of experiments, vestibular neurons that could be activated antidromically by stimulation of the contralateral medial reticular formation were studied with extracellular recording in cats under pentobarbital anesthesia. These neurons were found in all of the four main vestibular nuclei, but were less prevalent in dorsal Deiters' nucleus and in the central region of the superior vestibular nucleus than elsewhere. Regions of the pontine and medullary reticular formation from which neurons in different vestibular nuclei were activated corresponded to the pattern of vestibuloreticular projections described by neuroanatomists. 2. Latencies of antidromic responses to stimulation of the contralateral reticular formation ranged from 0.6 to over 3 ms, indicating a relatively slow transfer of activity from vestibular nuclei to reticular formation.


1996 ◽  
Vol 76 (1) ◽  
pp. 332-352 ◽  
Author(s):  
C. A. Scudder ◽  
A. K. Moschovakis ◽  
A. B. Karabelas ◽  
S. M. Highstein

1. The intra-axonal recording and horseradish peroxidase injection technique together with spontaneous eye movement monitoring has been employed in alert behaving monkeys to study the discharge pattern and axonal projections of mesencephalic saccade-related long-lead burst neurons (LLBNs). 2. Most of the recovered axons (N = 21) belonged to two classes of neurons. The majority (N = 13) were identified as efferents of the superior colliculus and had circumscribed movement fields typical of collicular saccade-related burst neurons. This discharge pattern, their responses to electrical stimulation of one or both superior colliculi, and their morphological appearance identified them as members of the T class of tectal efferent neurons. 3. Axons of these T cells deployed terminal fields within several saccade-related brain stem areas including the nucleus reticularis tegmenti pontis, which projects to the cerebellum; the nucleus reticularis pontis oralis and caudalis, which contains excitatory premotor burst neurons; the nucleus raphe interpositus, which contains omnipause neurons; the nucleus paragigantocellularis, which contains inhibitory premotor burst neurons, as well as other less differentiated parts of the brain stem reticular formation. 4. The other class of LLBNs (N = 4) had their somata in the medullary reticular formation just lateral to the interstitial nucleus of Cajal. They projected primarily to the raphe nuclei, the medullary reticular formation, and the paramedian reticular nucleus. Discharges were of the directional type with up ON directions (N = 3) and down ON directions (N = 1). 5. Other fibers, which project to pontine and medullary oculomotor structures but whose somata were not recovered (N = 4), illustrate that there are also other types of LLBNs that contribute to the generation and control of saccadic eye movements. 6. Our findings complement previous data about the axonal trajectories of T-type superior colliculus efferents. They also demonstrate the existence of LLBNs located in the mesencephalic reticular formation and their target areas in the brain stem. Implications of these findings for current concepts of oculomotor control are discussed.


1992 ◽  
Vol 8 (3) ◽  
pp. 257-276 ◽  
Author(s):  
Paul J. May ◽  
John D. Porter

AbstractThe superior colliculus exerts its most direct influence over orienting movements, and saccades in particular, via its descending projections to the brain stem and spinal cord. However, while there is detailed physiological data concerning the generation of saccade-related activity in the primate superior colliculus, there is relatively little data on the detailed connectivity of this structure in primates. Consequently, retrograde transport techniques were utilized to determine the locations of the cells of origin of these descending pathways in macaque monkeys. Tectal cells that projected to the ipsilateral pontine reticular formation were mainly found in the deep gray layer and occasionally in the intermediate gray layer. Tectal cells that projected to the contralateral pontine reticular formation were predominantly located in the intermediate gray layer. The contralaterally projecting population could be subdivided into two groups. The cells in upper sublamina of the intermediate gray layer project primarily to the saccade-related regions of the paramedian reticular formation. Cells in the lower sublamina project primarily to more lateral regions of the pontine reticular formation and to the spinal cord. We conclude that the primate colliculus is provided with at least three descending output channels, which are likely to differ in their connections and functions. Specifically, it seems likely that the lower portion of the intermediate gray layer may be specialized to subserve combined head and eye orienting movements, while the upper sublamina subserves saccades.


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