scholarly journals Linear acceleration-evoked cardiovascular responses in awake rats

2007 ◽  
Vol 103 (2) ◽  
pp. 646-654 ◽  
Author(s):  
Hong Zhu ◽  
James R. Jordan ◽  
Steven P. G. Hardy ◽  
Beverly Fulcher ◽  
Curtis Childress ◽  
...  

It has been well documented that vestibular-mediated cardiovascular regulation plays an important role in maintaining stable blood pressure (BP) during postural changes. But the underlying neural mechanisms remain to be elucidated. In particular, because the vestibular stimulation employed in previous animal studies activated both semicircular canals and otolith organs, the contributions of the otolith system has not been studied selectively. The goal of the present study was to characterize cardiovascular responses to natural otolith stimulation in awake rats that were subjected to pure linear motion. In any of the four directions tested, transient linear motion produced a short-latency (∼520 ms) increase in mean BP with a peak of 8.27 ± 0.66 mmHg and was followed by a decrease in BP. There was an initial small biphasic response in heart rate (HR) that was followed by a longer duration increase. The short-latency increase in BP was absent in rats that were pentobarbital sodium anesthetized or that were labyrinthectomized bilaterally, but it was unaffected by baroreceptor denervation, indicating that it was of otolith origin. The increase in BP was linear acceleration intensity dependent and was not affected by absence of visual cues. Furthermore, the BP response was attenuated by inactivation of the medial and inferior vestibular nuclei by microinjections of muscimol, indicating that the otolith-driven cardiovascular responses are mediated by the neurons in these areas. These results not only demonstrate the otolith specific influences on the cardiovascular system but also they establish the first rodent model for examining the neural mechanisms underlying the otolith-mediated cardiovascular regulation.

2003 ◽  
Vol 89 (1) ◽  
pp. 390-400 ◽  
Author(s):  
L. H. Zupan ◽  
D. M. Merfeld

Sensory systems often provide ambiguous information. For example, otolith organs measure gravito-inertial force (GIF), the sum of gravitational force and inertial force due to linear acceleration. However, according to Einstein's equivalence principle, a change in gravitational force due to tilt is indistinguishable from a change in inertial force due to translation. Therefore the central nervous system (CNS) must use other sensory cues to distinguish tilt from translation. For example, the CNS might use dynamic visual cues indicating rotation to help determine the orientation of gravity (tilt). This, in turn, might influence the neural processes that estimate linear acceleration, since the CNS might estimate gravity and linear acceleration such that the difference between these estimates matches the measured GIF. Depending on specific sensory information inflow, inaccurate estimates of gravity and linear acceleration can occur. Specifically, we predict that illusory tilt caused by roll optokinetic cues should lead to a horizontal vestibuloocular reflex compensatory for an interaural estimate of linear acceleration, even in the absence of actual linear acceleration. To investigate these predictions, we measured eye movements binocularly using infrared video methods in 17 subjects during and after optokinetic stimulation about the subject's nasooccipital (roll) axis (60°/s, clockwise or counterclockwise). The optokinetic stimulation was applied for 60 s followed by 30 s in darkness. We simultaneously measured subjective roll tilt using a somatosensory bar. Each subject was tested in three different orientations: upright, pitched forward 10°, and pitched backward 10°. Five subjects reported significant subjective roll tilt (>10°) in directions consistent with the direction of the optokinetic stimulation. In addition to torsional optokinetic nystagmus and afternystagmus, we measured a horizontal nystagmus to the right during and following clockwise (CW) stimulation and to the left during and following counterclockwise (CCW) stimulation. These measurements match predictions that subjective tilt in the absence of real tilt should induce a nonzero estimate of interaural linear acceleration and, therefore, a horizontal eye response. Furthermore, as predicted, the horizontal response in the dark was larger for Tilters ( n = 5) than for Non-Tilters ( n= 12).


2004 ◽  
Vol 92 (1) ◽  
pp. 20-35 ◽  
Author(s):  
Dora E. Angelaki

A gaze-stabilization reflex that has been conserved throughout evolution is the rotational vestibuloocular reflex (RVOR), which keeps images stable on the entire retina during head rotation. An ethological newer reflex, the translational or linear VOR (TVOR), provides fast foveal image stabilization during linear motion. Whereas the sensorimotor processing has been extensively studied in the RVOR, much less is currently known about the neural organization of the TVOR. Here we summarize the computational problems faced by the system and the potential solutions that might be used by brain stem and cerebellar neurons participating in the VORs. First and foremost, recent experimental and theoretical evidence has shown that, contrary to popular beliefs, the sensory signals driving the TVOR arise from both the otolith organs and the semicircular canals. Additional unresolved issues include a scaling by both eye position and vergence angle as well as the temporal transformation of linear acceleration signals into eye-position commands. Behavioral differences between the RVOR and TVOR, as well as distinct differences in neuroanatomical and neurophysiological properties, raise multiple functional questions and computational issues, only some of which are readily understood. In this review, we provide a summary of what is known about the functional properties and neural substrates for this oculomotor system and outline some specific hypotheses about how sensory information is centrally processed to create motor commands for the VORs.


2005 ◽  
Vol 98 (2) ◽  
pp. 526-533 ◽  
Author(s):  
R. L. Mori ◽  
L. A. Cotter ◽  
H. E. Arendt ◽  
C. J. Olsheski ◽  
B. J. Yates

The vestibular system participates in cardiovascular regulation during postural changes. In prior studies (Holmes MJ, Cotter LA, Arendt HE, Cas SP, and Yates BJ. Brain Res 938: 62–72, 2002, and Jian BJ, Cotter LA, Emanuel BA, Cass SP, and Yates BJ. J Appl Physiol 86: 1552–1560, 1999), transection of the vestibular nerves resulted in instability in blood pressure during nose-up body tilts, particularly when no visual information reflecting body position in space was available. However, recovery of orthostatic tolerance occurred within 1 wk, presumably because the vestibular nuclei integrate a variety of sensory inputs reflecting body location. The present study tested the hypothesis that lesions of the vestibular nuclei result in persistent cardiovascular deficits during orthostatic challenges. Blood pressure and heart rate were monitored in five conscious cats during nose-up tilts of varying amplitude, both before and after chemical lesions of the vestibular nuclei. Before lesions, blood pressure remained relatively stable during tilts. In all animals, the blood pressure responses to nose-up tilts were altered by damage to the medial and inferior vestibular nuclei; these effects were noted both when animals were tested in the presence and absence of visual feedback. In four of the five animals, the lesions also resulted in augmented heart rate increases from baseline values during 60° nose-up tilts. These effects persisted for longer than 1 wk, but they gradually resolved over time, except in the animal with the worst deficits. These observations suggest that recovery of compensatory cardiovascular responses after loss of vestibular inputs is accomplished at least in part through plastic changes in the vestibular nuclei and the enhancement of the ability of vestibular nucleus neurons to discriminate body position in space by employing nonlabyrinthine signals.


1979 ◽  
Vol 236 (1) ◽  
pp. R75-R82 ◽  
Author(s):  
J. Buggy ◽  
W. E. Hoffman ◽  
M. I. Phillips ◽  
A. E. Fisher ◽  
A. K. Johnson

Injections of hyperosmotic solutions (1- to 5-microliter injections of NaCl or sucrose solutions ranging in osmolarity from 0.34 to 0.90 osmol/l) into the anteroventral third ventricle (AV3V) of rats resulted in short latency drinking antidiuretic, and pressor responses. AV3V injections or infusions of combined angiotensin-hyperosmotic NaCl solution did not result in drinking greater than the sum of drinking to angiotensin and hyperosmotic NaCl separately administered. Differences in water versus saline drinking fluid preferences provided a behavioral dissociation of angiotensin and hyperosmotic sensitive neural mechanisms. Comparison of AV3V and lateral preoptic injection sites provided an additional separation since angiotensin was equally effective at both sites whereas osmotic stimulation was more effective at the AV3V site. AV3V lesions have previously been reported to abolish drinking, antidiuretic, and pressor responses to angiotensin and hyperosmotic stimulation. The data reported here provide additional evidence that angiotensin and hyperosmotic stimuli may both act on tissue surrounding AV3V but suggest that the neural substrates for these stimuli are not identical.


2005 ◽  
Vol 94 (1) ◽  
pp. 199-205 ◽  
Author(s):  
Daniel M. Merfeld ◽  
Sukyung Park ◽  
Claire Gianna-Poulin ◽  
F. Owen Black ◽  
Scott Wood

II. VOR and perceptual responses during combined Tilt&Translation. To compare and contrast the neural mechanisms that contribute to vestibular perception and action, we measured vestibuloocular reflexes (VOR) and perceptions of tilt and translation. We took advantage of the well-known ambiguity that the otolith organs respond to both linear acceleration and tilt with respect to gravity and investigated the mechanisms by which this ambiguity is resolved. A new motion paradigm that combined roll tilt with inter-aural translation (“ Tilt&Translation”) was used; subjects were sinusoidally (0.8 Hz) roll tilted but with their ears above or below the rotation axis. This paradigm provided sinusoidal roll canal cues that were the same across trials while providing otolith cues that varied linearly with ear position relative to the earth-horizontal rotation axis. We found that perceived tilt and translation depended on canal cues, with substantial roll tilt and inter-aural translation perceptions reported even when the otolith organs measured no inter-aural force. These findings match internal model predictions that rotational cues from the canals influence the neural processing of otolith cues. We also found horizontal translational VORs that varied linearly with radius; a minimal response was measured when the otolith organs transduced little or no inter-aural force. Hence, the horizontal translational VOR was dependent on otolith cues but independent of canal cues. These findings match predictions that translational VORs are elicited by simple filtering of otolith signals. We conclude that internal models govern human perception of tilt and translation at 0.8 Hz and that high-pass filtering governs the human translational VOR at this same frequency.


2017 ◽  
Vol 118 (4) ◽  
pp. 2499-2506 ◽  
Author(s):  
A. Pomante ◽  
L. P. J. Selen ◽  
W. P. Medendorp

The vestibular system provides information for spatial orientation. However, this information is ambiguous: because the otoliths sense the gravitoinertial force, they cannot distinguish gravitational and inertial components. As a consequence, prolonged linear acceleration of the head can be interpreted as tilt, referred to as the somatogravic effect. Previous modeling work suggests that the brain disambiguates the otolith signal according to the rules of Bayesian inference, combining noisy canal cues with the a priori assumption that prolonged linear accelerations are unlikely. Within this modeling framework the noise of the vestibular signals affects the dynamic characteristics of the tilt percept during linear whole-body motion. To test this prediction, we devised a novel paradigm to psychometrically characterize the dynamic visual vertical—as a proxy for the tilt percept—during passive sinusoidal linear motion along the interaural axis (0.33 Hz motion frequency, 1.75 m/s2peak acceleration, 80 cm displacement). While subjects ( n=10) kept fixation on a central body-fixed light, a line was briefly flashed (5 ms) at different phases of the motion, the orientation of which had to be judged relative to gravity. Consistent with the model’s prediction, subjects showed a phase-dependent modulation of the dynamic visual vertical, with a subject-specific phase shift with respect to the imposed acceleration signal. The magnitude of this modulation was smaller than predicted, suggesting a contribution of nonvestibular signals to the dynamic visual vertical. Despite their dampening effect, our findings may point to a link between the noise components in the vestibular system and the characteristics of dynamic visual vertical.NEW & NOTEWORTHY A fundamental question in neuroscience is how the brain processes vestibular signals to infer the orientation of the body and objects in space. We show that, under sinusoidal linear motion, systematic error patterns appear in the disambiguation of linear acceleration and spatial orientation. We discuss the dynamics of these illusory percepts in terms of a dynamic Bayesian model that combines uncertainty in the vestibular signals with priors based on the natural statistics of head motion.


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.


2001 ◽  
Vol 85 (4) ◽  
pp. 1648-1660 ◽  
Author(s):  
D. M. Merfeld ◽  
L. H. Zupan ◽  
C. A. Gifford

All linear accelerometers, including the otolith organs, respond equivalently to gravity and linear acceleration. To investigate how the nervous system resolves this ambiguity, we measured perceived roll tilt and reflexive eye movements in humans in the dark using two different centrifugation motion paradigms (fixed radius and variable radius) combined with two different subject orientations (facing-motion and back-to-motion). In the fixed radius trials, the radius at which the subject was seated was held constant while the rotation speed was changed to yield changes in the centrifugal force. In variable radius trials, the rotation speed was held constant while the radius was varied to yield a centrifugal force that nearly duplicated that measured during the fixed radius condition. The total gravito-inertial force (GIF) measured by the otolith organs was nearly identical in the two paradigms; the primary difference was the presence (fixed radius) or absence (variable radius) of yaw rotational cues. We found that the yaw rotational cues had a large statistically significant effect on the time course of perceived tilt, demonstrating that yaw rotational cues contribute substantially to the neural processing of roll tilt. We also found that the orientation of the subject relative to the centripetal acceleration had a dramatic influence on the eye movements measured during fixed radius centrifugation. Specifically, the horizontal vestibuloocular reflex (VOR) measured in our human subjects was always greater when the subject faced the direction of motion than when the subjects had their backs toward the motion during fixed radius rotation. This difference was consistent with the presence of a horizontal translational VOR response induced by the centripetal acceleration. Most importantly, by comparing the perceptual tilt responses to the eye movement responses, we found that the translational VOR component decayed as the subjective tilt indication aligned with the tilt of the GIF. This was true for both the fixed radius and variable radius conditions even though the time course of the responses was significantly different for these two conditions. These findings are consistent with the hypothesis that the nervous system resolves the ambiguous measurements of GIF into neural estimates of gravity and linear acceleration. More generally, these findings are consistent with the hypothesis that the nervous system uses internal models to process and interpret sensory motor cues.


1991 ◽  
Vol 260 (4) ◽  
pp. H1326-H1331 ◽  
Author(s):  
W. T. Talman ◽  
J. M. Colling ◽  
S. C. Robertson

Previous studies have demonstrated the release of glycine from neurotransmitter pools in the region of the nucleus tractus solitarii (NTS) where cardiovascular afferents terminate. Microinjection of glycine into NTS elicits decreases in arterial pressure and heart rate; these effects are also produced by glutamate or acetylcholine. As glycine may act both at the N-methyl-D-aspartate (NMDA)-receptor complex and centrally to release acetylcholine, we have sought to determine whether the cardiovascular responses to exogenous glycine are mediated through glutamatergic or cholinergic mechanisms. Responses to glycine microinjected into the NTS of anesthetized rats were not affected by blockade of the NMDA receptor complex but, like acetylcholine, were blocked by muscarinic receptor blockade. Physostigmine prolonged responses to glycine. Subthreshold doses of glycine, which augmented responses to acetylcholine microinjected into NTS, either decreased or had no effect on glutamate or NMDA. This study supports a role for glycine in cardiovascular regulation by the NTS and suggests that the actions of glycine may be effected, at least in part, through cholinergic mechanisms.


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