Inertial representation of angular motion in the vestibular system of rhesus monkeys. II. Otolith-controlled transformation that depends on an intact cerebellar nodulus

1995 ◽  
Vol 73 (5) ◽  
pp. 1729-1751 ◽  
Author(s):  
D. E. Angelaki ◽  
B. J. Hess

1. We recently studied the spatial representation of angular motion signals in rhesus monkeys by examining the orientation of postrotatory vestibuloocular responses during tilt of the head and body relative to gravity after constant-velocity rotation about an earth-vertical axis. We have reported that low-frequency angular motion signals in the vestibuloocular reflex (VOR) of rhesus monkeys are spatially transformed such that they remain invariant relative to gravity. In the present study we examine the properties of these inertial vestibular signals by employing similar stimulation conditions in animals with either selective semicircular canal plugging or selective lesions of cerebellar lobule X (nodulus) and ventral lobule IX (uvula). 2. We studied the spatial organization of postrotatory VOR in two rhesus monkeys that had either the lateral or one of the vertical canal pairs inactivated by plugging. In both monkeys, the spatiotemporal characteristics of postrotatory velocity after rotation in the plane of an intact canal pair and tilting in the plane of the plugged canal pair were indistinguishable from those of intact animals: postrotatory responses after tilts in the plane of the plugged canal pair were strongly damped, whereas an orthogonal response component was generated that rotated the eye velocity vector toward alignment with gravity. Thus otolith information rather than transient semicircular canal inputs that normally coexist during tilts seem to provide the necessary cues for the central transformation of semicircular canal signals. 3. We studied the three-dimensional VOR properties in two animals in which the cerebellar nodulus and ventral uvula were surgically ablated. After these lesions the temporal properties of the horizontal, vertical, and torsional VOR during earth-vertical-axis rotations were differentially affected. For horizontal VOR, the duration of postrotatory nystagmus was prolonged and the responses acquired strongly underdamped (i.e., oscillatory) properties. Similarly, sinusoidal responses were characterized by smaller phase leads after the lesion. For torsional VOR, the duration of postrotatory nystagmus was significantly shorter after the lesions, reaching postlesion values of 3.6 +/- 1.7 (SD) s and 6.4 +/- 1.1 s compared with prelesion values of 22.4 +/- 4.5 and 33.6 +/- 5.3 s for each animal. In addition, large phase leads characterized the torsional VOR during low-frequency sinusoidal stimulation. The dynamic properties of the vertical VOR in the lesioned animals, on the other hand, were indistinguishable from those in controls. 4. The cerebellar lesions affected the spatial organization of the horizontal and vertical/torsional systems in a differential way. Inertial transformation of lateral canal activity was only partially affected.(ABSTRACT TRUNCATED AT 400 WORDS)

1998 ◽  
Vol 79 (2) ◽  
pp. 791-807 ◽  
Author(s):  
Dora E. Angelaki ◽  
Bernhard J. M. Hess

Angelaki, Dora E. and Bernhard J. M. Hess. Visually induced adaptation in three-dimensional organization of primate vestibulo-ocular reflex. J. Neurophysiol. 79: 791–807, 1998. The adaptive plasticity of the spatial organization of the vestibuloocular reflex (VOR) has been investigated in intact and canal-plugged primates using 2-h exposure to conflicting visual (optokinetic, OKN) and vestibular rotational stimuli about mutually orthogonal axes (generating torsional VOR + vertical OKN, torsional VOR + horizontal OKN, vertical VOR + horizontal OKN, and horizontal VOR + vertical OKN). Adaptation protocols with 0.5-Hz (±18°) head movements about either an earth-vertical or an earth-horizontal axis induced orthogonal response components as high as 40–70% of those required for ideal adaptation. Orthogonal response gains were highest at the adapting frequency with phase leads present at lower and phase lags present at higher frequencies. Furthermore, the time course of adaptation, as well as orthogonal response dynamics were similar and relatively independent of the particular visual/vestibular stimulus combination. Low-frequency (0.05 Hz, vestibular stimulus: ±60°; optokinetic stimulus: ±180°) adaptation protocols with head movements about an earth-vertical axis induced smaller orthogonal response components that did not exceed 20–40% of the head velocity stimulus (i.e., ∼10% of that required for ideal adaptation). At the same frequency, adaptation with head movements about an earth-horizontal axis generated large orthogonal responses that reached values as high as 100–120% of head velocity after 2 h of adaptation (i.e., ∼40% of ideal adaptation gains). The particular spatial and temporal response characteristics after low-frequency, earth-horizontal axis adaptation in both intact and canal-plugged animals strongly suggests that the orienting (and perhaps translational) but not inertial (velocity storage) components of the primate otolith-ocular system exhibit spatial adaptability. Due to the particular nested arrangement of the visual and vestibular stimuli, the optic flow pattern exhibited a significant component about the third spatial axis (i.e., orthogonal to the axes of rotation of the head and visual surround) at twice the oscillation frequency. Accordingly, the adapted VOR was characterized consistently by a third response component (orthogonal to both the axes of head and optokinetic drum rotation) at twice the oscillation frequency after earth-horizontal but not after earth-vertical axis 0.05-Hz adaptation. This suggests that the otolith-ocular (but not the semicircular canal-ocular) system can adaptively change its spatial organization at frequencies different from those of the head movement.


1996 ◽  
Vol 75 (6) ◽  
pp. 2405-2424 ◽  
Author(s):  
D. E. Angelaki ◽  
B. J. Hess

1. The dynamic properties of otolith-ocular reflexes elicited by sinusoidal linear acceleration along the three cardinal head axes were studied during off-vertical axis rotations in rhesus monkeys. As the head rotates in space at constant velocity about an off-vertical axis, otolith-ocular reflexes are elicited in response to the sinusoidally varying linear acceleration (gravity) components along the interaural, nasooccipital, or vertical head axis. Because the frequency of these sinusoidal stimuli is proportional to the velocity of rotation, rotation at low and moderately fast speeds allows the study of the mid-and low-frequency dynamics of these otolith-ocular reflexes. 2. Animals were rotated in complete darkness in the yaw, pitch, and roll planes at velocities ranging between 7.4 and 184 degrees/s. Accordingly, otolith-ocular reflexes (manifested as sinusoidal modulations in eye position and/or slow-phase eye velocity) were quantitatively studied for stimulus frequencies ranging between 0.02 and 0.51 Hz. During yaw and roll rotation, torsional, vertical, and horizontal slow-phase eye velocity was sinusoidally modulated as a function of head position. The amplitudes of these responses were symmetric for rotations in opposite directions. In contrast, mainly vertical slow-phase eye velocity was modulated during pitch rotation. This modulation was asymmetric for rotations in opposite direction. 3. Each of these response components in a given rotation plane could be associated with an otolith-ocular response vector whose sensitivity, temporal phase, and spatial orientation were estimated on the basis of the amplitude and phase of sinusoidal modulations during both directions of rotation. Based on this analysis, which was performed either for slow-phase eye velocity alone or for total eye excursion (including both slow and fast eye movements), two distinct response patterns were observed: 1) response vectors with pronounced dynamics and spatial/temporal properties that could be characterized as the low-frequency range of “translational” otolith-ocular reflexes; and 2) response vectors associated with an eye position modulation in phase with head position ("tilt" otolith-ocular reflexes). 4. The responses associated with two otolith-ocular vectors with pronounced dynamics consisted of horizontal eye movements evoked as a function of gravity along the interaural axis and vertical eye movements elicited as a function of gravity along the vertical head axis. Both responses were characterized by a slow-phase eye velocity sensitivity that increased three- to five-fold and large phase changes of approximately 100-180 degrees between 0.02 and 0.51 Hz. These dynamic properties could suggest nontraditional temporal processing in utriculoocular and sacculoocular pathways, possibly involving spatiotemporal otolith-ocular interactions. 5. The two otolith-ocular vectors associated with eye position responses in phase with head position (tilt otolith-ocular reflexes) consisted of torsional eye movements in response to gravity along the interaural axis, and vertical eye movements in response to gravity along the nasooccipital head axis. These otolith-ocular responses did not result from an otolithic effect on slow eye movements alone. Particularly at high frequencies (i.e., high speed rotations), saccades were responsible for most of the modulation of torsional and vertical eye position, which was relatively large (on average +/- 8-10 degrees/g) and remained independent of frequency. Such reflex dynamics can be simulated by a direct coupling of primary otolith afferent inputs to the oculomotor plant. (ABSTRACT TRUNCATED)


2012 ◽  
Vol 108 (5) ◽  
pp. 1511-1520 ◽  
Author(s):  
Richard F. Lewis ◽  
Csilla Haburcakova ◽  
Wangsong Gong ◽  
Faisal Karmali ◽  
Daniel M. Merfeld

To investigate the characteristics of eye movements produced by electrical stimulation of semicircular canal afferents, we studied the spatial and temporal features of eye movements elicited by short-term lateral canal stimulation in two squirrel monkeys with plugged lateral canals, with the head upright or statically tilted in the roll plane. The electrically induced vestibuloocular reflex (eVOR) evoked with the head upright decayed more quickly than the stimulation signal provided by the electrode, demonstrating an absence of the classic velocity storage effect that improves the dynamics of the low-frequency VOR. When stimulation was provided with the head tilted in roll, however, the eVOR decayed more rapidly than when the head was upright, and a cross-coupled vertical response developed that shifted the eye's rotational axis toward alignment with gravity. These results demonstrate that rotational information provided by electrical stimulation of canal afferents interacts with otolith inputs (or other graviceptive cues) in a qualitatively normal manner, a process that is thought to be mediated by the velocity storage network. The observed interaction between the eVOR and graviceptive cues is of critical importance for the development of a functionally useful vestibular prosthesis. Furthermore, the presence of gravity-dependent effects (dumping, spatial orientation) despite an absence of low-frequency augmentation of the eVOR has not been previously described in any experimental preparation.


2000 ◽  
Vol 83 (3) ◽  
pp. 1522-1535 ◽  
Author(s):  
Karin Jaggi-Schwarz ◽  
Hubert Misslisch ◽  
Bernhard J. M. Hess

We examined the three-dimensional (3-D) spatial orientation of postrotatory eye velocity after horizontal off-vertical axis rotations by varying the final body orientation with respect to gravity. Three rhesus monkeys were oriented in one of two positions before the onset of rotation: pitched 24° nose-up or 90° nose-up (supine) relative to the earth-horizontal plane and rotated at ±60°/s around the body-longitudinal axis. After 10 turns, the animals were stopped in 1 of 12 final positions separated by 30°. An empirical analysis of the postrotatory responses showed that the resultant response plane remained space-invariant, i.e., accurately represented the actual head tilt plane at rotation stop. The alignment of the response vector with the spatial vertical was less complete. A complementary analysis, based on a 3-D model that implemented the spatial transformation and dynamic interaction of otolith and lateral semicircular canal signals, confirmed the empirical description of the spatial response. In addition, it allowed an estimation of the low-pass filter time constants in central otolith and semicircular canal pathways as well as the weighting ratio between direct and inertially transformed canal signals in the output. Our results support the hypothesis that the central vestibular system represents head velocity in gravity-centered coordinates by sensory integration of otolith and semicircular canal signals.


1994 ◽  
Vol 72 (1) ◽  
pp. 31-46 ◽  
Author(s):  
J. Van der Steen ◽  
J. I. Simpson ◽  
J. Tan

1. The three -dimensional, binocular eye movements evoked by electrical microstimulation of the cerebellar flocculus of alert, pigmented rabbits were recorded using the scleral search coil technique. The components of these eye movements were obtained in reference to an orthogonal coordinate system consisting of a vertical axis and two horizontal axes at 45 degrees and 135 degrees azimuth. The azimuth coordinate was taken to increase to both sides from the 0 degrees reference in the direction of the nose. 2. Eye movements were evoked most readily by stimulation (0.2 -ms pulses at 200 Hz for 1 s, intensity < or = 20 microA) at loci in the deep granular layer and the white matter. They consisted of slow (5–20 deg/s) movements. The responses were either binocular, with the eye ipsilateral to the stimulated flocculus usually having the larger amplitude, or were monocular, in which case they were restricted to the ipsilateral eye. 3. The evoked responses were classified according to the combination of the largest measured component of rotation for the two eyes and its sense of rotation (clockwise, CW, or counterclockwise, CCW). Seventy -eight percent of the evoked eye movements could be placed in one of two classes. For one of these classes the largest response component was a short -latency abduction of the ipsilateral eye about its vertical axis (19%), whereas for the other class (59%), the largest response component was a short -latency CCW rotation of the ipsilateral (left) eye about its 135 degrees axis. This response was frequently (50%) accompanied by a smaller short -latency CW rotation of the contralateral (right) eye about its 45 degrees axis. 4. The two main classes of three -dimensional eye movements are associated differentially with anatomically distinguishable compartments that are revealed by acetylcholinesterase histochemistry. Of the five anatomically distinguishable compartments in the floccular white matter, three are predominant. The middle of these three compartments is associated with the vertical axis class of movements, whereas the two adjacent compartments are associated with the 135 degrees class of eye movements. The eye movement relation of the other two, smaller compartments, was not determined. 5. The spatial orientation of the rotation axes of the two main classes of evoked eye movements closely corresponds to that of the preferred axes of the visual climbing fiber input to the flocculus. This suggests that both are organized in a similar coordinate system.(ABSTRACT TRUNCATED AT 400 WORDS)


1995 ◽  
Vol 73 (4) ◽  
pp. 1716-1720 ◽  
Author(s):  
D. E. Angelaki ◽  
B. J. Hess

1. During rotations that dynamically activate utricular and saccular primary afferents, the otolith system centrally detects the velocity and direction of rotation of the head in space. This property is experimentally manifested as a steady-state compensatory nystagmus during constant velocity off-vertical axis rotations. The computational, physiological, and anatomic details of this response remain presently unknown. Here we report that surgical inactivation of the cerebellar nodulus and ventral uvula abolished the ability of the otolith system to generate steady-state nystagmus during constant velocity rotation and to improve the dynamics of the vestibuloocular reflex (VOR) during low-frequency sinusoidal oscillations about off-vertical axes in rhesus monkeys. These results suggest that the cerebellar nodulus and/or ventral uvula comprise part of the neural substrate that is involved in these computations.


2003 ◽  
Vol 90 (2) ◽  
pp. 622-630 ◽  
Author(s):  
Marousa Pavlou ◽  
Nicole Wijnberg ◽  
Mary E. Faldon ◽  
Adolfo M. Bronstein

The subjective visual vertical (SVV) is usually considered a measure of otolith function. Herewith we investigate the influence of semicircular canal (SCC) stimulation on the SVV by rotating normal subjects in yaw about an earth-vertical axis, with velocity steps of ± 90°/s, for 60 s. SVV was assessed by setting an illuminated line to perceived earth vertical in darkness, during a per- and postrotary period. Four head positions were tested: upright, 30° backward (chin up) or forward, and ∼40° forward from upright. During head upright/backward conditions, a significant SVV tilt ( P < 0.01) in the direction opposite to rotation was found that reversed during postrotary responses. The rotationally induced SVV tilt had a time constant of decay of ∼30 s. Rotation with the head 30° forward did not affect SVV, whereas the 40° forward tilt caused a direction reversal of SVV responses compared with head upright/backward. Spearman correlation values (Rho) between individual SCC efficiencies in different head positions and mean SVV tilts were 0.79 for posterior, 0.34 for anterior, and – 0.80 for horizontal SCCs. Three-dimensional video-oculography showed that SVV and torsional eye position measurements were highly correlated (0.83) and in the direction opposite to the slow phase torsional vestibuloocular reflex. In conclusion: 1) during yaw axis rotation without reorientation of the head with respect to gravity, the SVV is influenced by SCC stimulation; 2) this effect is mediated by the vertical SCCs, particularly the posterior SCCs; 3) rotationally induced SVV changes are due to torsional ocular tilt; 4) SVV and ocular tilts occur in the “anticompensatory,” fast phase direction of the torsional nystagmus; and 5) clinically, abnormal SVV tilts cannot be considered a specific indication of otolith system dysfunction.


Materials ◽  
2020 ◽  
Vol 13 (17) ◽  
pp. 3812 ◽  
Author(s):  
Heng Jiang ◽  
Mangong Zhang ◽  
Yu Liu ◽  
Dongliang Pei ◽  
Meng Chen ◽  
...  

Elastic metamaterials have promising applications in wave control and vibration isolation, due to their extraordinary characteristics, e.g., negative Poisson ratio, band gaps, effective negative mass density and effective negative modulus. How to develop new functional metamaterials using a special structure has always been a hot topic in this field. In this study, a three-dimensional (3D) star structure is designed to construct metamaterials with both negative static and dynamic properties. The results show that the 3D star structure formed a wide band gap at lower frequency and had a negative Poisson’s ratio. Different from conventional acoustic metamaterials, the main physical mechanism behind the low-frequency band gap of the 3D star structure is the resonance mode formed by the bending deformation of each rib plate, which made it easier to achieve effective isolation of low-frequency elastic waves with a low mass density. In addition, many structural parameters of the 3D star structure can be modulated to effectively adjust the band gap frequency by changing the angle between the concave nodes and aspect ratio. This study provides a new way to design the 3D acoustic metamaterials and develop the lightweight vibration isolation devices.


1996 ◽  
Vol 75 (6) ◽  
pp. 2425-2440 ◽  
Author(s):  
D. E. Angelaki ◽  
B. J. Hess

1. The dynamic contribution of otolith signals to three-dimensional angular vestibuloocular reflex (VOR) was studied during off-vertical axis rotations in rhesus monkeys. In an attempt to separate response components to head velocity from those to head position relative to gravity during low-frequency sinusoidal oscillations, large oscillation amplitudes were chosen such that peak-to-peak head displacements exceeded 360 degrees. Because the waveforms of head position and velocity differed in shape and frequency content, the particular head position and angular velocity sensitivity of otolith-ocular responses could be independently assessed. 2. During both constant velocity rotation and low-frequency sinusoidal oscillations, the otolith system generated two different types of oculomotor responses: 1) modulation of three-dimensional eye position and/or eye velocity as a function of head position relative to gravity, as presented in the preceding paper, and 2) slow-phase eye velocity as a function of head angular velocity. These two types of otolith-ocular responses have been analyzed separately. In this paper we focus on the angular velocity responses of the otolith system. 3. During constant velocity off-vertical axis rotations, a steady-state nystagmus was elicited that was maintained throughout rotation. During low-frequency sinusoidal off-vertical axis oscillations, dynamic otolith stimulation resulted primarily in a reduction of phase leads that characterize low-frequency VOR during earth-vertical axis rotations. Both of these effects are the result of an internally generated head angular velocity signal of otolithic origin that is coupled through a low-pass filter to the VOR. No change in either VOR gain or phase was observed at stimulus frequencies larger than 0.1 Hz. 4. The dynamic otolith contribution to low-frequency angular VOR exhibited three-dimensional response characteristics with some quantitative differences in the different response components. For horizontal VOR, the amplitude of the steady-state slow-phase velocity during constant velocity rotation and the reduction of phase leads during sinusoidal oscillation were relatively independent of tilt angle (for angles larger than approximately 10 degrees). For vertical and torsional VOR, the amplitude of steady-state slow-phase eye velocity during constant velocity rotation increased, and the phase leads during sinusoidal oscillation decreased with increasing tilt angle. The largest steady-state response amplitudes and smallest phase leads were observed during vertical/torsional VOR about an earth-horizontal axis. 5. The dynamic range of otolith-borne head angular velocity information in the VOR was limited to velocities up to approximately 110 degrees/s. Higher head velocities resulted in saturation and a decrease in the amplitude of the steady-state response components during constant velocity rotation and in increased phase leads during sinusoidal oscillations. 6. The response characteristics of otolith-borne angular VORs were also studied in animals after selective semicircular canal inactivation. Otolith angular VORs exhibited clear low-pass filtered properties with a corner frequency of approximately 0.05-0.1 Hz. Vectorial summation of canal VOR alone (elicited during earth-vertical axis rotations) and otolith VOR alone (elicited during off-vertical axis oscillations after semicircular canal inactivation) could not predict VOR gain and phase during off-vertical axis rotations in intact animals. This suggests a more complex interaction of semicircular canal and otolith signals. 7. The results of this study show that the primate low-frequency enhancement of VOR dynamics during off-vertical axis rotation is independent of a simultaneous activation of the vertical and torsional “tilt” otolith-ocular reflexes that have been characterized in the preceding paper. (ABSTRACT TRUNCATED)


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