The nucleus prepositus predominantly outputs eye movement-related information during passive and active self-motion

2013 ◽  
Vol 109 (7) ◽  
pp. 1900-1911 ◽  
Author(s):  
Alexis Dale ◽  
Kathleen E. Cullen

Maintaining a constant representation of our heading as we move through the world requires the accurate estimate of spatial orientation. As one turns (or is turned) toward a new heading, signals from the semicircular canals are relayed through the vestibular system to higher-order centers that encode head direction. To date, there is no direct electrophysiological evidence confirming the first relay point of head-motion signals from the vestibular nuclei, but previous anatomical and lesion studies have identified the nucleus prepositus as a likely candidate. Whereas burst-tonic neurons encode only eye-movement signals during head-fixed eye motion and passive vestibular stimulation, these neurons have not been studied during self-generated movements. Here, we specifically address whether burst-tonic neurons encode head motion during active behaviors. Single-unit responses were recorded from the nucleus prepositus of rhesus monkeys and compared for head-restrained and active conditions with comparable eye velocities. We found that neurons consistently encoded eye position and velocity across conditions but did not exhibit significant sensitivity to head position or velocity. Additionally, response sensitivities varied as a function of eye velocity, similar to abducens motoneurons and consistent with their role in gaze control and stabilization. Thus our results demonstrate that the primate nucleus prepositus chiefly encodes eye movement even during active head-movement behaviors, a finding inconsistent with the proposal that this nucleus makes a direct contribution to head-direction cell tuning. Given its ascending projections, however, we speculate that this eye-movement information is integrated with other inputs in establishing higher-order spatial representations.

2004 ◽  
Vol 96 (6) ◽  
pp. 2301-2316 ◽  
Author(s):  
Richard C. Fitzpatrick ◽  
Brian L. Day

Galvanic vestibular stimulation (GVS) is a simple, safe, and specific way to elicit vestibular reflexes. Yet, despite a long history, it has only recently found popularity as a research tool and is rarely used clinically. The obstacle to advancing and exploiting GVS is that we cannot interpret the evoked responses with certainty because we do not understand how the stimulus acts as an input to the system. This paper examines the electrophysiology and anatomy of the vestibular organs and the effects of GVS on human balance control and develops a model that explains the observed balance responses. These responses are large and highly organized over all body segments and adapt to postural and balance requirements. To achieve this, neurons in the vestibular nuclei receive convergent signals from all vestibular receptors and somatosensory and cortical inputs. GVS sway responses are affected by other sources of information about balance but can appear as the sum of otolithic and semicircular canal responses. Electrophysiological studies showing similar activation of primary afferents from the otolith organs and canals and their convergence in the vestibular nuclei support this. On the basis of the morphology of the cristae and the alignment of the semicircular canals in the skull, rotational vectors calculated for every mode of GVS agree with the observed sway. However, vector summation of signals from all utricular afferents does not explain the observed sway. Thus we propose the hypothesis that the otolithic component of the balance response originates from only the pars medialis of the utricular macula.


2018 ◽  
Vol 119 (1) ◽  
pp. 73-83 ◽  
Author(s):  
Shawn D. Newlands ◽  
Ben Abbatematteo ◽  
Min Wei ◽  
Laurel H. Carney ◽  
Hongge Luan

Roughly half of all vestibular nucleus neurons without eye movement sensitivity respond to both angular rotation and linear acceleration. Linear acceleration signals arise from otolith organs, and rotation signals arise from semicircular canals. In the vestibular nerve, these signals are carried by different afferents. Vestibular nucleus neurons represent the first point of convergence for these distinct sensory signals. This study systematically evaluated how rotational and translational signals interact in single neurons in the vestibular nuclei: multisensory integration at the first opportunity for convergence between these two independent vestibular sensory signals. Single-unit recordings were made from the vestibular nuclei of awake macaques during yaw rotation, translation in the horizontal plane, and combinations of rotation and translation at different frequencies. The overall response magnitude of the combined translation and rotation was generally less than the sum of the magnitudes in responses to the stimuli applied independently. However, we found that under conditions in which the peaks of the rotational and translational responses were coincident these signals were approximately additive. With presentation of rotation and translation at different frequencies, rotation was attenuated more than translation, regardless of which was at a higher frequency. These data suggest a nonlinear interaction between these two sensory modalities in the vestibular nuclei, in which coincident peak responses are proportionally stronger than other, off-peak interactions. These results are similar to those reported for other forms of multisensory integration, such as audio-visual integration in the superior colliculus. NEW & NOTEWORTHY This is the first study to systematically explore the interaction of rotational and translational signals in the vestibular nuclei through independent manipulation. The results of this study demonstrate nonlinear integration leading to maximum response amplitude when the timing and direction of peak rotational and translational responses are coincident.


2005 ◽  
Vol 94 (4) ◽  
pp. 2391-2402 ◽  
Author(s):  
Stefano Ramat ◽  
Dominik Straumann ◽  
David S. Zee

We investigated the influence of cognitive factors on the early response of the interaural translational vestibuloocular reflex (tVOR) in six normal subjects. Variables were prior knowledge of direction of head motion and the position of the fixation target relative to the head [head-fixed (HF) or space-fixed (SF)]. A manually driven device provided a step-like head translation (∼35 mm distance, peak acceleration, 0.6–1.3 g). Subjects looked at the SF or HF target located 15 cm in front of their heads in otherwise complete darkness. The testing paradigms were: random interleaving of SF and HF targets with unknown direction of head movement, known target location with random head direction (SFR or HFR), and known target location with known head direction (SFP or HFP). Timing was always unpredictable. A “gain” of the slow phase was calculated with respect to ideal performance (maintained fixation of the SF target, recorded/ideal eye velocity computed at time of peak head velocity). At such times, there were no significant differences in gain between HF and SF trials in the random condition; the average gain was ∼36% of ideal. On the other hand, responses in the SFR and HFR conditions differed as early as 20 ms after the head began moving. Average gain was higher (0.43 ± 0.11 vs. 0.34 ± 0.14; means ± SD, P < 0.05) for each subject in the SFR than the HFR condition. For SFP and HFP, the responses differed from the onset of head motion. Average slow-phase gain was higher (0.49 ± 0.12 vs. 0.31 ± 0.12, P < 0.02) for each subject in SFP than in HFP. The timing of corrective saccades during the tVOR was also influenced by cognitive factors. Visual error signals seemed to be more important for triggering saccades in HF trials, whereas preprogramming, probably based on labyrinthine information, seemed to be more important in SF trials. Simulations showed that the changes in slow-phase gain with cognition could be reproduced with simple parametric adjustments of the gain of activity from otolith afferents and suggest that higher-level cognitive control of the VOR could occur as early as the synapse of peripheral afferents on neurons in the vestibular nuclei, either directly from higher level centers or via the cerebellum. In sum, the tVOR—both in its slow-phase response and the saccadic corrections—is subject to “higher-level” cognitive influences including knowledge of where the line of sight must point during head motion and the impending direction of head motion.


2000 ◽  
Vol 83 (1) ◽  
pp. 630-637 ◽  
Author(s):  
Kathleen E. Cullen ◽  
Henrietta L. Galiana ◽  
Pierre A. Sylvestre

Burst neurons (BNs) in the paramedian pontine reticular formation provide the primary input to the extraocular motoneurons (MNs) during head-restrained saccades and combined eye-head gaze shifts. Prior studies have shown that BNs carry eye movement–related signals during saccades and carry head as well as eye movement–related signals during gaze shifts. Therefore MNs receive signals related to head motion during gaze shifts, yet they solely drive eye motion. Here we addressed whether the relationship between MN firing rates and eye movements is influenced by the additional premotor signals present during gaze shifts. Neurons in the abducens nucleus of monkeys were first studied during saccades made with the head stationary. We then recorded from the same neurons during voluntary combined eye-head gaze shifts. We conclude that the activity of MNs, in contrast to that of BNs, is related to eye motion by the same dynamic relationship during head-restrained saccades and head-unrestrained gaze shifts. In addition, we show that a standard metric-based analysis [i.e., counting the number of spikes (NOS) in a burst] yields misleading results when applied to the same data set. We argue that this latter approach fails because it does not properly consider the system's dynamics or the strong interactions between eye and head motion.


1984 ◽  
Vol 52 (4) ◽  
pp. 724-742 ◽  
Author(s):  
M. C. Chubb ◽  
A. F. Fuchs ◽  
C. A. Scudder

To elucidate how information is processed in the vestibuloocular reflex (VOR) pathways subserving vertical eye movements, extracellular single-unit recordings were obtained from the vestibular nuclei of alert monkeys trained to track a visual target with their eyes while undergoing sinusoidal pitch oscillations (0.2-1.0 Hz). Units with activity related to vertical vestibular stimulation and/or eye movements were classified as either vestibular units (n = 53), vestibular plus eye-position units (n = 30), pursuit units (n = 10), or miscellaneous units (n = 5), which had various combinations of head- and eye-movement sensitivities. Vestibular units discharged in relation to head rotation, but not to smooth eye movements. On average, these units fired approximately in phase with head velocity; however, a broad range of phase shifts was observed. The activities of 8% of the vestibular units were related to saccades. Vestibular plus eye-position units fired in relation to head velocity and eye position and, in addition, usually to eye velocity. Their discharge rates increased for eye and head movements in opposite directions. During combined head and eye movements, the modulation in unit activity was not significantly different from the sum of the modulations during each alone. For saccades, the unit firing rate either decreased to zero or was unaffected. Pursuit units discharged in relation to eye position, eye velocity, or both, but not to head movements alone. For saccades, unit activity usually either paused or was unaffected. The eye-movement-related activities of the vestibular plus eye-position and pursuit units were not significantly different. A quantitative comparison of their firing patterns suggests that vestibular, vestibular plus eye-position, and pursuit neurons in the vestibular nucleus could provide mossy fiber inputs to the flocculus. In addition, the vertical vestibular plus eye-position neurons have discharge patterns similar to those of fibers recorded rostrally in the medial longitudinal fasciculus. Therefore, our data support the view that vertical vestibular plus eye-position neurons are interneurons of the VOR.


1988 ◽  
Vol 60 (5) ◽  
pp. 1753-1764 ◽  
Author(s):  
J. Kasper ◽  
R. H. Schor ◽  
V. J. Wilson

1. We have studied, in decerebrate cats, the responses of neurons in the lateral and descending vestibular nuclei to whole-body rotations in vertical planes that activated vertical semicircular canal and utricular receptors. Some neurons were identified as vestibulospinal by antidromic stimulation with floating electrodes placed in C4. 2. The direction of tilt that caused maximal excitation (response vector orientation) of each neuron was determined. Neuron dynamics were then studied with sinusoidal stimuli closely aligned with the response vector orientation, in the range 0.02-1 Hz. A few cells, for which we could not identify a response vector, probably had spatial-temporal convergence. 3. On the basis of dynamics, neurons were classified as receiving their input primarily from vertical semicircular canals, primarily from the otolith organs, or from canal+otolith convergence. 4. Response vector orientations of canal-driven neurons were often near +45 degrees or -45 degrees with respect to the transverse (roll) plane, suggesting these neurons received excitatory input from the ipsilateral anterior or posterior canal, respectively. Some neurons had canal-related dynamics but vector orientations near roll, presumably because they received convergent input from the ipsilateral anterior and posterior canals. Few neurons had their vectors near pitch. 5. In the lateral vestibular nucleus, neurons with otolith organ input (pure otolith or otolith+canal) tended to have vector orientations closer to roll than to pitch. In the descending nucleus the responses were evenly divided between the roll and pitch quadrants. 6. We conclude that most of our neurons have dynamics and response vector orientations that make them good candidates to participate in vestibulospinal reflexes acting on the limbs, but not those acting on the neck.


1997 ◽  
Vol 273 (2) ◽  
pp. R615-R622 ◽  
Author(s):  
V. A. Convertino ◽  
F. H. Previc ◽  
D. A. Ludwig ◽  
E. J. Engelken

Twelve healthy men underwent measurement of their carotid-cardiac baroreflex response during varying conditions of vestibulo-oculomotor stimulation to test the hypothesis that vestibular and/or oculomotor stimulation associated with head movements in the yaw plane inhibit baroreflex control of heart rate. We assessed the carotid-cardiac baroreflex response by plotting R-R intervals (in milliseconds) at each of eight neck pressure steps with their respective carotid distending pressures (in millimeters mercury). Baroreflex sensitivity was measured under four experimental conditions: 1) sinusoidal whole body yaw rotation of the subject in the dark without visual fixation (combined vestibular-oculomotor stimulation); 2) yaw oscillation of the subject while tracking a small head-fixed light moving with the subject (vestibular stimulation without eye movements); 3) subject stationary while fixating on a small light oscillating in yaw at the same frequency, peak acceleration, and velocity as the chair (eye movements without vestibular stimulation); and 4) subject stationary in the dark (no eye or head motion). Head motion alone reduced baseline baroreflex responsiveness by 30% from 3.8 +/- 0.5 to 2.6 +/- 0.5 ms/mmHg. Eye motion alone also reduced the baroreflex response by 13% (0.5 ms/mmHg) to 3.3 +/- 0.5 ms/mmHg. During head motion, the effect of eye motion was negligible (2.7 +/- 0.4 ms/mmHg). These results suggest that vestibular stimulation associated with head movements in yaw inhibits vagally mediated baroreflex control of heart rate, whereas oculomotor stimulation is less of a factor and only in the absence of vestibular stimulation.


2007 ◽  
Vol 120 (2) ◽  
pp. 120-124 ◽  
Author(s):  
Fu-rong MA ◽  
Jun-xiu LIU ◽  
Xue-pei LI ◽  
Jian-jun MAO ◽  
Qun-dan ZHANG ◽  
...  

Author(s):  
Behrouz Tavakol ◽  
Guillaume Froehlicher ◽  
Douglas P. Holmes ◽  
Howard A. Stone

Lubrication theory is broadly applicable to the flow characterization of thin fluid films and the motion of particles near surfaces. We offer an extension to lubrication theory by starting with Stokes equations and considering higher-order terms in a systematic perturbation expansion to describe the fluid flow in a channel with features of a modest aspect ratio. Experimental results qualitatively confirm the higher-order analytical solutions, while numerical results are in very good agreement with the higher-order analytical results. We show that the extended lubrication theory is a robust tool for an accurate estimate of pressure drop in channels with shape changes on the order of the channel height, accounting for both smooth and sharp changes in geometry.


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