scholarly journals Roll Tilt Psychophysics in Rhesus Monkeys During Vestibular and Visual Stimulation

2008 ◽  
Vol 100 (1) ◽  
pp. 140-153 ◽  
Author(s):  
Richard F. Lewis ◽  
Csilla Haburcakova ◽  
Daniel M. Merfeld
Keyword(s):  
Rhesus Monkeys ◽  
Visual Stimulation ◽  
Inertial Force ◽  
Semicircular Canals ◽  
Head Orientation ◽  
Optokinetic Stimulation ◽  
Behavioral Measures ◽  
Visual Vertical ◽  
Fixed Radius ◽  
Roll Tilt

How does the brain calculate the spatial orientation of the head relative to gravity? Psychophysical measurements are critical to investigate this question, but such measurements have been limited to humans. In non-human primates, behavioral measures have focused on vestibular-mediated eye movements, which do not reflect percepts of head orientation. We have therefore developed a method to measure tilt perception in monkeys, derived from the subjective visual vertical (SVV) task. Two rhesus monkeys were trained to align a light bar parallel to gravity and performed this task during roll tilts, centrifugation, and roll optokinetic stimulation. The monkeys accurately aligned the light bar with gravity during static roll tilts but also demonstrated small orientation-dependent misperceptions of the tilt angle analogous to those measured in humans. When the gravito-inertial force (GIF) rotated dynamically in the roll plane, SVV responses remained closely aligned with the GIF during roll tilt of the head (coplanar canal rotational cues present), lagged slightly behind the GIF during variable-radius centrifugation (no canal cues present), and shifted gradually during fixed-radius centrifugation (orthogonal yaw canal cues present). SVV responses also deviated away from the earth-vertical during roll optokinetic stimulation. These results demonstrate that rotational cues derived from the semicircular canals and visual system have prominent effects on psychophysical measurements of roll tilt in rhesus monkeys and therefore suggest that a central synthesis of graviceptive and rotational cues contributes to percepts of head orientation relative to gravity in non-human primates.

Neural Processing of Gravito-Inertial Cues in Humans. IV. Influence of Visual Rotational Cues During Roll Optokinetic Stimuli

2003 ◽  
Vol 89 (1) ◽  
pp. 390-400 ◽  
Author(s):  
L. H. Zupan ◽  
D. M. Merfeld
Keyword(s):  
Visual Cues ◽  
Gravitational Force ◽  
Sensory Information ◽  
Inertial Force ◽  
Linear Acceleration ◽  
Otolith Organs ◽  
Optokinetic Stimulation ◽  
The Difference ◽  
The Right ◽  
Roll Tilt

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).

scholarly journals Gravity dependence of the effect of optokinetic stimulation on the subjective visual vertical

2017 ◽  
Vol 117 (5) ◽  
pp. 1948-1958 ◽  
Author(s):  
Bryan K. Ward ◽  
Christopher J. Bockisch ◽  
Nicoletta Caramia ◽  
Giovanni Bertolini ◽  
Alexander Andrea Tarnutzer
Keyword(s):  
Bayesian Theory ◽  
Roll Angle ◽  
Whole Body ◽  
Optokinetic Stimulation ◽  
Subjective Visual Vertical ◽  
Vestibular Input ◽  
Stimulus Velocity ◽  
Visual Vertical ◽  
Observer Model ◽  
Roll Tilt

Accurate and precise estimates of direction of gravity are essential for spatial orientation. According to Bayesian theory, multisensory vestibular, visual, and proprioceptive input is centrally integrated in a weighted fashion based on the reliability of the component sensory signals. For otolithic input, a decreasing signal-to-noise ratio was demonstrated with increasing roll angle. We hypothesized that the weights of vestibular (otolithic) and extravestibular (visual/proprioceptive) sensors are roll-angle dependent and predicted an increased weight of extravestibular cues with increasing roll angle, potentially following the Bayesian hypothesis. To probe this concept, the subjective visual vertical (SVV) was assessed in different roll positions (≤ ± 120°, steps = 30°, n = 10) with/without presenting an optokinetic stimulus (velocity = ± 60°/s). The optokinetic stimulus biased the SVV toward the direction of stimulus rotation for roll angles ≥ ± 30° ( P < 0.005). Offsets grew from 3.9 ± 1.8° (upright) to 22.1 ± 11.8° (±120° roll tilt, P < 0.001). Trial-to-trial variability increased with roll angle, demonstrating a nonsignificant increase when providing optokinetic stimulation. Variability and optokinetic bias were correlated ( R2 = 0.71, slope = 0.71, 95% confidence interval = 0.57–0.86). An optimal-observer model combining an optokinetic bias with vestibular input reproduced measured errors closely. These findings support the hypothesis of a weighted multisensory integration when estimating direction of gravity with optokinetic stimulation. Visual input was weighted more when vestibular input became less reliable, i.e., at larger roll-tilt angles. However, according to Bayesian theory, the variability of combined cues is always lower than the variability of each source cue. If the observed increase in variability, although nonsignificant, is true, either it must depend on an additional source of variability, added after SVV computation, or it would conflict with the Bayesian hypothesis. NEW & NOTEWORTHY Applying a rotating optokinetic stimulus while recording the subjective visual vertical in different whole body roll angles, we noted the optokinetic-induced bias to correlate with the roll angle. These findings allow the hypothesis that the established optimal weighting of single-sensory cues depending on their reliability to estimate direction of gravity could be extended to a bias caused by visual self-motion stimuli.

Neural Processing of Gravito-Inertial Cues in Humans. I. Influence of the Semicircular Canals Following Post-Rotatory Tilt

2000 ◽  
Vol 84 (4) ◽  
pp. 2001-2015 ◽  
Author(s):  
L. H. Zupan ◽  
R. J. Peterka ◽  
D. M. Merfeld
Keyword(s):  
Eye Movements ◽  
Information Integration ◽  
Constant Velocity ◽  
Gravitational Force ◽  
Inertial Force ◽  
Semicircular Canals ◽  
Linear Acceleration ◽  
Head Orientation ◽  
Otolith Organs ◽  
Sensory Cues

Sensory systems often provide ambiguous information. Integration of various sensory cues is required for the CNS to resolve sensory ambiguity and elicit appropriate responses. The vestibular system includes two types of sensors: the semicircular canals, which measure head rotation, and the otolith organs, which measure gravito-inertial force (GIF), the sum of gravitational force and inertial force due to linear acceleration. According to Einstein's equivalence principle, gravitational force is indistinguishable from inertial force due to linear acceleration. As a consequence, otolith measurements must be supplemented with other sensory information for the CNS to distinguish tilt from translation. The GIF resolution hypothesis states that the CNS estimates gravity and linear acceleration, so that the difference between estimates of gravity and linear acceleration matches the measured GIF. Both otolith and semicircular canal cues influence this estimation of gravity and linear acceleration. The GIF resolution hypothesis predicts that inaccurate estimates of both gravity and linear acceleration can occur due to central interactions of sensory cues. The existence of specific patterns of vestibuloocular reflexes (VOR) related to these inaccurate estimates can be used to test the GIF resolution hypothesis. To investigate this hypothesis, we measured eye movements during two different protocols. In one experiment, eight subjects were rotated at a constant velocity about an earth-vertical axis and then tilted 90° in darkness to one of eight different evenly spaced final orientations, a so-called “dumping” protocol. Three speeds (200, 100, and 50°/s) and two directions, clockwise (CW) and counterclockwise (CCW), of rotation were tested. In another experiment, four subjects were rotated at a constant velocity (200°/s, CW and CCW) about an earth-horizontal axis and stopped in two different final orientations (nose-up and nose-down), a so-called “barbecue” protocol. The GIF resolution hypothesis predicts that post-rotatory horizontal VOR eye movements for both protocols should include an “induced” VOR component, compensatory to an interaural estimate of linear acceleration, even though no true interaural linear acceleration is present. The GIF resolution hypothesis accurately predicted VOR and induced VOR dependence on rotation direction, rotation speed, and head orientation. Alternative hypotheses stating that frequency segregation may discriminate tilt from translation or that the post-rotatory VOR time constant is dependent on head orientation with respect to the GIF direction did not predict the observed VOR for either experimental protocol.

scholarly journals Gravity Dependence of Subjective Visual Vertical Variability

2009 ◽  
Vol 102 (3) ◽  
pp. 1657-1671 ◽  
Author(s):  
A. A. Tarnutzer ◽  
C. Bockisch ◽  
D. Straumann ◽  
I. Olasagasti
Keyword(s):  
Inertial Force ◽  
Semicircular Canals ◽  
The Body ◽  
Otolith Organs ◽  
Subjective Visual Vertical ◽  
Visual Vertical ◽  
Head Roll ◽  
Static Head ◽  
Experimental Findings ◽  
Vertical Variability

The brain integrates sensory input from the otolith organs, the semicircular canals, and the somatosensory and visual systems to determine self-orientation relative to gravity. Only the otoliths directly sense the gravito-inertial force vector and therefore provide the major input for perceiving static head-roll relative to gravity, as measured by the subjective visual vertical (SVV). Intraindividual SVV variability increases with head roll, which suggests that the effectiveness of the otolith signal is roll-angle dependent. We asked whether SVV variability reflects the spatial distribution of the otolithic sensors and the otolith-derived acceleration estimate. Subjects were placed in different roll orientations (0–360°, 15° steps) and asked to align an arrow with perceived vertical. Variability was minimal in upright, increased with head-roll peaking around 120–135°, and decreased to intermediate values at 180°. Otolith-dependent variability was modeled by taking into consideration the nonuniform distribution of the otolith afferents and their nonlinear firing rate. The otolith-derived estimate was combined with an internal bias shifting the estimated gravity-vector toward the body-longitudinal. Assuming an efficient otolith estimator at all roll angles, peak variability of the model matched our data; however, modeled variability in upside-down and upright positions was very similar, which is at odds with our findings. By decreasing the effectiveness of the otolith estimator with increasing roll, simulated variability matched our experimental findings better. We suggest that modulations of SVV precision in the roll plane are related to the properties of the otolith sensors and to central computational mechanisms that are not optimally tuned for roll-angles distant from upright.

Interstitial Nucleus of Cajal Encodes Three-Dimensional Head Orientations in Fick-Like Coordinates

2007 ◽  
Vol 97 (1) ◽  
pp. 604-617 ◽  
Author(s):  
Eliana M. Klier ◽  
Hongying Wang ◽  
J. Douglas Crawford
Keyword(s):  
Coordinate System ◽  
Degrees Of Freedom ◽  
Three Dimensional ◽  
Semicircular Canals ◽  
Head Rotation ◽  
Head Orientation ◽  
Interstitial Nucleus Of Cajal ◽  
The Gaze ◽  
Behavioral Constraints ◽  
The Right

Two central, related questions in motor control are 1) how the brain represents movement directions of various effectors like the eyes and head and 2) how it constrains their redundant degrees of freedom. The interstitial nucleus of Cajal (INC) integrates velocity commands from the gaze control system into position signals for three-dimensional eye and head posture. It has been shown that the right INC encodes clockwise (CW)-up and CW-down eye and head components, whereas the left INC encodes counterclockwise (CCW)-up and CCW-down components, similar to the sensitivity directions of the vertical semicircular canals. For the eyes, these canal-like coordinates align with Listing’s plane (a behavioral strategy limiting torsion about the gaze axis). By analogy, we predicted that the INC also encodes head orientation in canal-like coordinates, but instead, aligned with the coordinate axes for the Fick strategy (which constrains head torsion). Unilateral stimulation (50 μA, 300 Hz, 200 ms) evoked CW head rotations from the right INC and CCW rotations from the left INC, with variable vertical components. The observed axes of head rotation were consistent with a canal-like coordinate system. Moreover, as predicted, these axes remained fixed in the head, rotating with initial head orientation like the horizontal and torsional axes of a Fick coordinate system. This suggests that the head is ordinarily constrained to zero torsion in Fick coordinates by equally activating CW/CCW populations of neurons in the right/left INC. These data support a simple mechanism for controlling head orientation through the alignment of brain stem neural coordinates with natural behavioral constraints.

Responses to Moving Visual Stimuli in Pretectal Neurons of the Small-Spotted Dogfish (Scyliorhinus canicula)

2008 ◽  
Vol 99 (1) ◽  
pp. 200-207 ◽  
Author(s):  
Olivia Andrea Masseck ◽  
Klaus-Peter Hoffmann
Keyword(s):  
Visual Information ◽  
Visual Stimulation ◽  
Semicircular Canals ◽  
Neuronal Responses ◽  
Vertical Movements ◽  
Scyliorhinus Canicula ◽  
Random Dot Patterns ◽  
Pretectal Area ◽  
Corpus Geniculatum Laterale ◽  
Sensitive Direction

Single-unit recordings were performed from a retinorecipient pretectal area (corpus geniculatum laterale) in Scyliorhinus canicula. The function and homology of this nucleus has not been clarified so far. During visual stimulation with a random dot pattern, 45 (35%) neurons were found to be direction selective, 10 (8%) were axis selective (best neuronal responses to rotations in both directions around one particular stimulus axis), and 75 (58%) were movement sensitive. Direction-selective responses were found to the following stimulus directions (in retinal coordinates): temporonasal and nasotemporal horizontal movements, up- and downward vertical movements, and oblique movements. All directions of motion were represented equally by our sample of pretectal neurons. Additionally we tested the responses of 58 of the 130 neurons to random dot patterns rotating around the semicircular canal or body axes to investigate whether direction-selective visual information is mapped into vestibular coordinates in pretectal neurons of this chondrichthyan species. Again all rotational directions were represented equally, which argues against a direct transformation from a retinal to a vestibular reference frame. If a complete transformation had occurred, responses to rotational axes corresponding to the axes of the semicircular canals should have been overrepresented. In conclusion, the recorded direction-selective neurons in the Cgl are plausible detectors for retinal slip created by body rotations in all directions.

Evaluation of the Torsional VOR in Weightlessness

1993 ◽  
Vol 3 (3) ◽  
pp. 207-218
Author(s):  
Andrew H. Clarke ◽  
Winfried Teiwes ◽  
Hans Scherer
Keyword(s):  
Head Movement ◽  
Angular Rate ◽  
Inertial Force ◽  
Semicircular Canals ◽  
Head Rotation ◽  
Video Data ◽  
Microgravity Conditions ◽  
Oculomotor Response ◽  
Roll Axis ◽  
Integrative Processing

The experimental concept and findings from a recent manned orbital spaceflight are described. Together with ongoing terrestrial and parabolic studies, the present experiment is intended to further our knowledge of the sensory integrative processing of information from the semicircular canals and the otolithic receptors, and to quantify the presumed otolithic adaptation to altered gravito-inertial force environments in a more reliable manner than to date. The experiment included measurement of the basic vestibulo-oculomotor response during active head rotation about each of the three orthogonal axes. Priority was given to the recording of ocular torsion, as elicited by head oscillation about the roll axis, and thus due to the concomitant stimulation of the semicircular canals and otolith receptors. Videooculography was employed for the measurement of eye movements; head movement was measured by three orthogonally arranged angular rate sensors and a triaxial linear accelerometer device. All signals were recorded synchronously on a video/data recorder. Preliminary results indicate alterations in the torsional VOR under zero-g conditions, suggesting an adaptive modification of the torsional VOR gain over the course of the 6-day orbital flight. In addition, the inflight test findings yielded discrepancies between intended and performed head movement indicating impairment in sensorimotor coordination under prolonged microgravity conditions.

Neural Processing of Gravito-Inertial Cues in Humans. II. Influence of the Semicircular Canals During Eccentric Rotation

2001 ◽  
Vol 85 (4) ◽  
pp. 1648-1660 ◽  
Author(s):  
D. M. Merfeld ◽  
L. H. Zupan ◽  
C. A. Gifford
Keyword(s):  
Nervous System ◽  
Time Course ◽  
Rotation Speed ◽  
Linear Acceleration ◽  
Otolith Organs ◽  
Centripetal Acceleration ◽  
Variable Radius ◽  
Fixed Radius ◽  
The Subject ◽  
Roll Tilt

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.

Contributions of Single Semicircular Canals to Caloric Nystagmus as Revealed by Canal Plugging in Rhesus Monkeys

1996 ◽  
Vol 116 (4) ◽  
pp. 513-520 ◽  
Author(s):  
Andreas Böhmer ◽  
Dominik Straumann ◽  
Jun-Ichi Suzuki ◽  
Bernhard J. M. Hess ◽  
Volker Henn
Keyword(s):  
Rhesus Monkeys ◽  
Semicircular Canals ◽  
Caloric Nystagmus

Three-Dimensional Organization of Otolith-Ocular Reflexes in Rhesus Monkeys. III. Responses to Translation

1998 ◽  
Vol 80 (2) ◽  
pp. 680-695 ◽  
Author(s):  
Dora E. Angelaki
Keyword(s):  
Frequency Dependence ◽  
Brain Stem ◽  
Rhesus Monkeys ◽  
Three Dimensional ◽  
Head Orientation ◽  
Frequency Range ◽  
Low Frequencies ◽  
Similar Frequency ◽  
Response Sensitivity ◽  
Torsional Response

Angelaki, Dora E. Three-dimensional organization of otolith-ocular reflexes in rhesus monkeys. III. Responses to translation. J. Neurophysiol. 80: 680–695, 1998. The three-dimensional (3-D) properties of the translational vestibulo-ocular reflexes (translational VORs) during lateral and fore-aft oscillations in complete darkness were studied in rhesus monkeys at frequencies between 0.16 and 25 Hz. In addition, constant velocity off-vertical axis rotations extended the frequency range to 0.02 Hz. During lateral motion, horizontal responses were in phase with linear velocity in the frequency range of 2–10 Hz. At both lower and higher frequencies, phase lags were introduced. Torsional response phase changed more than 180° in the tested frequency range such that torsional eye movements, which could be regarded as compensatory to “an apparent roll tilt” at the lowest frequencies, became anticompensatory at all frequencies above ∼1 Hz. These results suggest two functionally different frequency bandwidths for the translational VORs. In the low-frequency spectrum (≪0.5 Hz), horizontal responses compensatory to translation are small and high-pass-filtered whereas torsional response sensitivity is relatively frequency independent. At higher frequencies however, both horizontal and torsional response sensitivity and phase exhibit a similar frequency dependence, suggesting a common role during head translation. During up-down motion, vertical responses were in phase with translational velocity at 3–5 Hz but phase leads progressively increased for lower frequencies (>90° at frequencies <0.2 Hz). No consistent dependence on static head orientation was observed for the vertical response components during up-down motion and the horizontal and torsional response components during lateral translation. The frequency response characteristics of the translational VORs were fitted by “periphery/brain stem” functions that related the linear acceleration input, transduced by primary otolith afferents, to the velocity signals providing the input to the velocity-to-position neural integrator and the oculomotor plant. The lowest-order, best-fit periphery/brain stem model that approximated the frequency dependence of the data consisted of a second order transfer function with two alternating poles (at 0.4 and 7.2 Hz) and zeros (at 0.035 and 3.4 Hz). In addition to clearly differentiator dynamics at low frequencies (less than ∼0.5 Hz), there was no frequency bandwidth where the periphery/brain stem function could be approximated by an integrator, as previously suggested. In this scheme, the oculomotor plant dynamics are assumed to perform the necessary high-frequency integration as required by the reflex. The detailed frequency dependence of the data could only be precisely described by higher order functions with nonminimum phase characteristics that preclude simple filtering of afferent inputs and might be suggestive of distributed spatiotemporal processing of otolith signals in the translational VORs.

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