Lesion of the nodulus and ventral uvula abolish steady-state off-vertical axis otolith response

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.

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)


1992 ◽  
Vol 73 (2) ◽  
pp. S121-S131 ◽  
Author(s):  
B. Cohen ◽  
I. Kozlovskaya ◽  
T. Raphan ◽  
D. Solomon ◽  
D. Helwig ◽  
...  

The vestibuloocular reflex (VOR) of two rhesus monkeys was recorded before and after 14 days of spaceflight. The gain (eye velocity/head velocity) of the horizontal VOR, tested 15 and 18 h after landing, was approximately equal to preflight values. The dominant time constant of the animal tested 15 h after landing was equivalent to that before flight. During nystagmus induced by off-vertical axis rotation (OVAR), the latency, rising time constant, steady-state eye velocity, and phase of modulation in eye velocity and eye position with respect to head position were similar in both monkeys before and after flight. There were changes in the amplitude of modulation of horizontal eye velocity during steady-state OVAR and in the ability to discharge stored activity rapidly by tilting during postrotatory nystagmus (tilt dumping) after flight: OVAR modulations were larger, and tilt dumping was lost in the one animal tested on the day of landing and for several days thereafter. If the gain and time constant of the horizontal VOR change in microgravity, they must revert to normal soon after landing. The changes that were observed suggest that adaptation to microgravity had caused alterations in way that the central nervous system processes otolith input.


2000 ◽  
Vol 83 (3) ◽  
pp. 1662-1676 ◽  
Author(s):  
Dora E. Angelaki ◽  
M. Quinn McHenry ◽  
J. David Dickman ◽  
Adrian A. Perachio

The effects of functional, reversible ablation and potential recruitment of the most irregular otolith afferents on the dynamics and sensitivity of the translational vestibuloocular reflexes (trVORs) were investigated in rhesus monkeys trained to fixate near and far targets. Translational motion stimuli consisted of either steady-state lateral and fore-aft sinusoidal oscillations or short-lasting transient lateral head displacements. Short-duration (usually <2 s) anodal (inhibitory) and cathodal (excitatory) currents (50–100 μA) were delivered bilaterally during motion. In the presence of anodal labyrinthine stimulation, trVOR sensitivity and its dependence on viewing distance were significantly decreased. In addition, anodal currents significantly increased phase lags. During transient motion, anodal stimulation resulted in significantly lower initial eye acceleration and more sluggish responses. Cathodal currents tended to have opposite effects. The main characteristics of these results were simulated by a simple model where both regularly and irregularly discharging afferents contribute to the trVORs. Anodal labyrinthine currents also were found to decrease eye velocity during long-duration, constant velocity rotations, although results were generally more variable compared with those during translational motion.


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.


1994 ◽  
Vol 72 (3) ◽  
pp. 1383-1394 ◽  
Author(s):  
A. M. Pastor ◽  
R. R. de la Cruz ◽  
R. Baker

1. The time course of eye velocity responses elicited by head velocity steps was compared in normal, adapted, and cerebellectomized goldfish. Vestibuloocular reflex (VOR) adaptation was induced by combined visual and vestibular stimulation that altered the ratio of eye to head velocity (VOR gain) toward values either higher or lower than the control amplitude. The velocity step consisted of alternating periods of head rotation at a constant velocity of 16 degrees/s zero-to-peak around the vertical axis. 2. The VOR produced by head velocity steps consisted of an early acceleration-related component, the dynamic response, separated from a sustained period of constant velocity, the plateau, by a sag that occurred around 125-150 ms. Latency of the VOR averaged 18 ms for the adducting eye and 20 ms for abducting eye independent of the initial VOR gain. Adapted dynamic VOR responses diverged from the control records at the earliest detectable latency after both high and low VOR gain training. This result demonstrates modification in the shortest latency brain stem VOR pathway, presumably, the three-neuron reflex arc. 3. After acute cerebellectomy the adapted dynamic response was unaltered for approximately 50 ms in the low-gain and 70 ms in the high-gain VOR states. Not less than 30% of the altered velocity was retained throughout the remaining dynamic and sustained component. These results demonstrate that the vestibulocerebellum is not necessary for the maintenance of the earliest adapted eye velocity. Hence brain stem pathways are sufficient for the expression of the modified VOR. 4. Purkinje cells identified by simple and complex spikes were recorded extracellularly in the area of the vestibulocerebellum, where electrical stimulation produced conjugate ipsiversive horizontal eye movements. Independent eye and head velocity sensitivities were determined in response to visual world motion and VOR suppression, respectively. The two signals either added, canceled, or were both present in Purkinje cells throughout the range of eye velocity induced by vertical axis visual-vestibular stimulation. 5. Latency of Purkinje cell discharge to either a vestibular or visual velocity step exhibited means of 43 and 70 ms, respectively.(ABSTRACT TRUNCATED AT 400 WORDS)


2002 ◽  
Vol 87 (2) ◽  
pp. 1159-1164 ◽  
Author(s):  
J. Eric Killian ◽  
James F. Baker

The horizontal vestibuloocular reflex (VOR) of Purkinje cell degeneration ( pcd/pcd) mutant mice, which lack a functional cerebellar cortex, was compared in darkness to that of wild-type animals during constant velocity yaw rotations about an earth-horizontal axis and during sinusoidal yaw rotations about an earth-vertical axis. Both wild-type and pcd/pcd mice showed a compensatory average VOR eye velocity, or bias, during constant velocity horizontal axis rotations, evidence of central neural processing of otolith afferent signals to create a signal proportional to head angular velocity. Eye velocity bias was greater in pcd/pcd mice than in wild-type mice at a low rotational velocity (32°/s), but less at higher velocities (128 and 200°/s). Lesion of the medial nodulus severely attenuated eye velocity bias in two wild-type mice, without attenuating VOR during sinusoidal vertical axis yaw rotations at 0.2 Hz. These results show that while head velocity estimation in mice, as in primates, depends on the cerebellum, pcd/pcd mutant mice develop velocity estimation without a functional cerebellar cortex. We conclude that neural circuits that exclude cerebellar cortex are capable of the signal processing necessary for head angular velocity estimation, but that these circuits are insufficient for normal estimation at high velocities.


2003 ◽  
Vol 13 (4-6) ◽  
pp. 377-393
Author(s):  
Steven T. Moore ◽  
Gilles Clément ◽  
Mingjai Dai ◽  
Theodore Raphan ◽  
David Solomon ◽  
...  

In this paper we review space flight experiments performed by our laboratory. Rhesus monkeys were tested before and after 12 days in orbit on COSMOS flights 2044 (1989) and 2229 (1992–1993). There was a long-lasting decrease in post-flight ocular counter-rolling (70%) and vergence (50%) during off-vertical axis rotation. In one animal, the orientation of optokinetic after-nystagmus shifted by 28° from the spatial vertical towards the body vertical early post-flight. Otolith-ocular and perceptual responses were also studied in four astronauts on the 17-day Neurolab shuttle mission (STS-90) in 1998. Ocular counter-rolling was unchanged in response to 1-g and 0.5-g Gy centrifugation during and after flight and to post-flight static roll tilts relative to pre-flight values. Orientation of the optokinetic nystagmus eye velocity axis to gravito-inertial acceleration (GIA) during centrifugation was also unaltered by exposure to microgravity. Perceptual orientation to the GIA was maintained in-flight, and subjects did not report sensation of translation during constant velocity centrifugation. These studies suggest that percepts and ocular responses to tilt are determined by sensing the body vertical relative to the GIA. The findings also raise the possibility that 'artificial gravity' during the Neurolab flight counteracted adaptation of these otolith-ocular responses.


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)


2000 ◽  
Vol 84 (6) ◽  
pp. 3078-3082 ◽  
Author(s):  
Bernhard J. M. Hess ◽  
Anna Lysakowski ◽  
Lloyd B. Minor ◽  
Dora E. Angelaki

We have previously shown that there is a slowly progressing, frequency-specific recovery of the gain and phase of the horizontal vestibuloocular reflex (VOR) in rhesus monkeys following plugging of the lateral semicircular canals. The adapted VOR response exhibited both dynamic and spatial characteristics that were distinctly different from responses in intact animals. To discriminate between adaptation or recovery of central versus peripheral origin, we have tested the recovered vestibuloocular responses in three rhesus monkeys in which either one or both coplanar pairs of vertical semicircular canals had been plugged previously by occluding the remaining semicircular canals in a second plugging operation. We measured the spatial tuning of the VOR in two or three different mutually orthogonal planes in response to sinusoidal oscillations (1.1 Hz, ±5°, ±35°/s) over a period of 2–3 and 12–14 mo after each operation. Apart from a significant recovery of the torsional/vertical VOR following the first operation we found that these recovered responses were preserved following the second operation, whereas the responses from the newly operated semicircular canals disappeared acutely as expected. In the follow-up period of up to 3 mo after the second operation, responses from the last operated canals showed recovery in two of three animals, whereas the previously recovered responses persisted. The results suggest that VOR recovery following plugging may depend on a regained residual sensitivity of the plugged semicircular canals to angular head acceleration.


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