Roll tilt self-motion direction discrimination training: First evidence for perceptual learning.

Perceptual learning, the ability to improve the sensitivity of sensory perception through training, has been shown to exist in all sensory systems but the vestibular system. A previous study found no improvement of passive self-motion thresholds in the dark after intense direction discrimination training of either yaw rotations (stimulating semicircular canals) or y-translation (stimulating otoliths). The goal of the present study was to investigate whether perceptual learning of self-motion in the dark would occur when there is a simultaneous otolith and semicircular canal input, as is the case with roll tilt motion stimuli. Blindfolded subjects (n = 10) trained on a direction discrimination task with 0.2-Hz roll tilt motion stimuli (9 h of training, 1,800 trials). Before and after training, motion thresholds were measured in the dark for the trained motion and for three transfer conditions. We found that roll tilt sensitivity in the 0.2-Hz roll tilt condition was increased (i.e., thresholds decreased) after training but not for controls who were not exposed to training. This is the first demonstration of perceptual learning of passive self-motion direction discrimination in the dark. The results have potential therapeutic relevance as 0.2-Hz roll thresholds have been associated with poor performance on a clinical balance test that has been linked to more than a fivefold increase in falls.

Motion perception during variable-radius swing motion in darkness.

Using a variable-radius roll swing motion paradigm, we examined the influence of interaural (y-axis) and dorsoventral (z-axis) force modulation on perceived tilt and translation by measuring perception of horizontal translation, roll tilt, and distance from center of rotation (radius) at 0.45 and 0.8 Hz using standard magnitude estimation techniques (primarily verbal reports) in darkness. Results show that motion perception was significantly influenced by both y- and z-axis forces. During constant radius trials, subjects' perceptions of tilt and translation were generally almost veridical. By selectively pairing radius (1.22 and 0.38 m) and frequency (0.45 and 0.8 Hz, respectively), the y-axis acceleration could be tailored in opposition to gravity so that the combined y-axis gravitoinertial force (GIF) variation at the subject's ears was reduced to approximately 0.035 m/s(2) - in effect, the y-axis GIF was "nulled" below putative perceptual threshold levels. With y-axis force nulling, subjects overestimated their tilt angle and underestimated their horizontal translation and radius. For some y-axis nulling trials, a radial linear acceleration at twice the tilt frequency (0.25 m/s(2) at 0.9 Hz, 0.13 m/s(2) at 1.6 Hz) was simultaneously applied to reduce the z-axis force variations caused by centripetal acceleration and by changes in the z-axis component of gravity during tilt. For other trials, the phase of this radial linear acceleration was altered to double the magnitude of the z-axis force variations. z-axis force nulling further increased the perceived tilt angle and further decreased perceived horizontal translation and radius relative to the y-axis nulling trials, while z-axis force doubling had the opposite effect. Subject reports were remarkably geometrically consistent; an observer model-based analysis suggests that perception was influenced by knowledge of swing geometry.

An internal model of head kinematics predicts the influence of head orientation on reflexive eye movements.

Our sense of self-motion and self-orientation results from combining information from different sources. We hypothesize that the central nervous system (CNS) uses internal models of the laws of physics to merge cues provided by different sensory systems. Different models that include internal models have been proposed; we focus herein on that referred to as the sensory weighting model. For simplicity, we isolate the portion of the sensory weighting model that estimates head angular velocity: it includes an inverse internal model of head kinematics and an 'idiotropic' vector aligned with the main body axis. Following a post-rotatory tilt in the dark, which is a rapid tilt following a constant-velocity rotation about an earth-vertical axis, the inverse internal model is applied to conflicting vestibular signals. Consequently, the CNS computes an inaccurate estimate of head angular velocity that shifts toward alignment with an estimate of gravity. Since reflexive eye movements known as vestibulo-ocular reflexes (VOR) compensate for this estimate of head angular velocity, the model predicts that the VOR rotation axis shifts toward alignment with this estimate of gravity and that the VOR time constant depends on final head orientation. These predictions are consistent with experimental data.

Reproduction of ON-center and OFF-center self-rotations.

In self-rotation reproduction tasks, subjects appear to estimate the displacement angle and then reproduce this angle without necessarily replicating the entire temporal velocity profile. In contrast, subjects appear to reproduce the entire temporal velocity profile during linear motion stimulating the otoliths. To investigate what happens during combined rotation and translation, we investigated in darkness the central processing of vestibular cues during eccentric rotation. Controlling a centrifuge with a joystick, nine healthy subjects were asked to reproduce the angle of the previously imposed rotation. Rotations were either ON-center, or 50 cm OFF-center with inter-aural centripetal acceleration. Rotation duration was either variable (proportional to the traveled angle), or constant. We examined whether the stimulation of the otoliths during OFF-center rotation changes self-rotation reproduction, and whether rotation duration is processed differently by the nervous system with and without otolith stimulation. As postulated, the subjects indeed reproduced more closely the stimulus velocity profile when OFF-center. But the primary result is that the additional supra-threshold linear acceleration cues, measured by the otoliths, did not improve performance. More specifically, to our surprise, the ability to reproduce rotation angle degraded slightly in the presence of additional information from the otolith organs, with the linear acceleration cues appearing to interfere with the reproduction of movement duration.

Neural processing of gravito-inertial cues in humans. IV. Influence of visual rotational cues during roll optokinetic stimuli.

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 degrees /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 degrees, and pitched backward 10 degrees. Five subjects reported significant subjective roll tilt (>10 degrees ) in directions consistent with the direction of the optokinetic stimulation. In addition to torsional optokinetic nystagmus and after nystagmus, 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).

Using sensory weighting to model the influence of canal, otolith and visual cues on spatial orientation and eye movements.

The sensory weighting model is a general model of sensory integration that consists of three processing layers. First, each sensor provides the central nervous system (CNS) with information regarding a specific physical variable. Due to sensor dynamics, this measure is only reliable for the frequency range over which the sensor is accurate. Therefore, we hypothesize that the CNS improves on the reliability of the individual sensor outside this frequency range by using information from other sensors, a process referred to as "frequency completion." Frequency completion uses internal models of sensory dynamics. This "improved" sensory signal is designated as the "sensory estimate" of the physical variable. Second, before being combined, information with different physical meanings is first transformed into a common representation; sensory estimates are converted to intermediate estimates. This conversion uses internal models of body dynamics and physical relationships. Third, several sensory systems may provide information about the same physical variable (e.g., semicircular canals and vision both measure self-rotation). Therefore, we hypothesize that the "central estimate" of a physical variable is computed as a weighted sum of all available intermediate estimates of this physical variable, a process referred to as "multicue weighted averaging." The resulting central estimate is fed back to the first two layers. The sensory weighting model is applied to three-dimensional (3D) visual-vestibular interactions and their associated eye movements and perceptual responses. The model inputs are 3D angular and translational stimuli. The sensory inputs are the 3D sensory signals coming from the semicircular canals, otolith organs, and the visual system. The angular and translational components of visual movement are assumed to be available as separate stimuli measured by the visual system using retinal slip and image deformation. In addition, both tonic ("regular") and phasic ("irregular") otolithic afferents are implemented. Whereas neither tonic nor phasic otolithic afferents distinguish gravity from linear acceleration, the model uses tonic afferents to estimate gravity and phasic afferents to estimate linear acceleration. The model outputs are the internal estimates of physical motion variables and 3D slow-phase eye movements. The model also includes a smooth pursuit module. The model matches eye responses and perceptual effects measured during various motion paradigms in darkness (e.g., centered and eccentric yaw rotation about an earth-vertical axis, yaw rotation about an earth-horizontal axis) and with visual cues (e.g., stabilized visual stimulation or optokinetic stimulation).

Neural processing of gravitoinertial cues in humans. III. Modeling tilt and translation responses.

All linear accelerometers measure gravitoinertial force, which is the sum of gravitational force (tilt) and inertial force due to linear acceleration (translation). Neural strategies must exist to elicit tilt and translation responses from this ambiguous cue. To investigate these neural processes, we developed a model of human responses and simulated a number of motion paradigms used to investigate this tilt/translation ambiguity. In this model, the separation of GIF into neural estimates of gravity and linear acceleration is accomplished via an internal model made up of three principal components: 1) the influence of rotational cues (e.g., semicircular canals) on the neural representation of gravity, 2) the resolution of gravitoinertial force into neural representations of gravity and linear acceleration, and 3) the neural representation of the dynamics of the semicircular canals. By combining these simple hypotheses within the internal model framework, the model mimics human responses to a number of different paradigms, ranging from simple paradigms, like roll tilt, to complex paradigms, like postrotational tilt and centrifugation. It is important to note that the exact same mechanisms can explain responses induced by simple movements as well as by more complex paradigms; no additional elements or hypotheses are needed to match the data obtained during more complex paradigms. Therefore these modeled response characteristics are consistent with available data and with the hypothesis that the nervous system uses internal models to estimate tilt and translation in the presence of ambiguous sensory cues.

Vestibular prostheses: the engineering and biomedical issues.

Currently available data demonstrate the need for balance prostheses. Recent technological and biomedical advances now make it feasible to produce miniaturized sensors, signal processors, electric stimulators, and stimulating electrodes that are roughly analogous to a cochlear implant but which provide information about self motion, instead of sound. Many areas require work before balance prostheses become a reality. Some of these include: the development of a motion sensor array, the conversion of the sensed motion into physiologically meaningful information, the delivery of the transformed information to the CNS, the training of vestibular deficient individuals to use the prosthesis, and developing methods to evaluate the efficacy of the device. In this "white paper", we consider these issues in the context of prototype baseline prosthetic devices.

Vestibular discrimination of gravity and translational acceleration.

According to Einstein's equivalence principle, linear accelerations experienced during translational motion are physically indistinguishable from changes in orientation relative to gravity experienced during tilting movements. Nevertheless, despite these ambiguous sensory cues provided by the primary otolith afferents, perceptual and motor responses discriminate between gravity and translational acceleration. There is growing evidence to suggest that the brain resolves this ambiguity primarily by combining signals from multiple sensors, the semicircular canals being a main extra otolith contributor. Here, we summarize the experimental evidence in support of the canal influences on the neural processing of otolith cues, provide specific experimental results in rhesus monkeys, and discuss and compare previously proposed models that combine otolith and semicircular-canal signals in order to provide neural estimates of gravity and linear acceleration.

Neural processing of gravito-inertial cues in humans. II. Influence of the semicircular canals during eccentric rotation.

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.

Neural processing of gravito-inertial cues in humans. I. Influence of the semicircular canals following post-rotatory tilt.

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 degrees in darkness to one of eight different evenly spaced final orientations, a so-called "dumping" protocol. Three speeds (200, 100, and 50 degrees /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 degrees /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.

Prototype neural semicircular canal prosthesis using patterned electrical stimulation.

The design of a prototype semicircular canal prosthesis is presented along with preliminary results. This device measures angular velocity of the head (+/-500 degrees/s) using a piezoelectric vibrating gyroscope. With a digital filter this velocity is filtered to match the dynamic characteristics of the semicircular canals, which are the physiological rotation sensors of the vestibular system. This digitally filtered signal is used to modulate the pulse rate of electrical stimulation. The pulse rate is varied between 50 and 250 Hz via a sigmoidal lookup table relating pulse rate to angular velocity; the steady-state rate is 150 Hz. A current source utilizes these timing pulses to deliver charge balanced, cathodic-first, biphasic, current pulses to the nerves innervating the semicircular canal via platinum electrodes. Power is supplied via lithium batteries. dc/dc converters are used to generate regulated +/-5 V supplies from the batteries. All of the components are contained in a small, lightweight, Nylon box measuring roughly 43 mm x 31 mm x 25 mm, which can be mounted on the top of an animal's head. This device has been tested in guinea pigs having surgically implanted platinum electrodes, and the results show that the prosthesis can provide a rotational cue to the nervous system.

Low-frequency otolith and semicircular canal interactions after canal inactivation.

During sustained constant velocity and low-frequency off-vertical axis rotations (OVAR), otolith signals contribute significantly to slow-phase eye velocity. The adaptive plasticity of these responses was investigated here after semicircular canal plugging. Inactivation of semicircular canals results in a highly compromised and deficient vestibulo-ocular reflex (VOR). Based on the VOR enhancement hypothesis, one could expect an adaptive increase of otolith-borne angular velocity signals due to combined otolith/canal inputs after inactivation of the semicircular canals. Contrary to expectations, however, the steady-state slow-phase velocity during constant velocity OVAR decreased in amplitude over time. A similar progressive decrease in VOR gain was also observed during low-frequency off-vertical axis oscillations. This response deterioration was present in animals with either lateral or vertical semicircular canals inactivated and was limited to the plane(s) of the plugged canals. The results are consistent with the idea that the low-frequency otolith signals do not simply enhance VOR responses. Rather, the nervous system appears to correlate vestibular sensory information from the otoliths and the semicircular canals to generate an integral response to head motion.

Effects of static orientation upon human optokinetic afternystagmus.

"Normal" human subjects were placed in a series of 5 static orientations with respect to gravity and were asked to view an optokinetic display moving at a constant angular velocity. The axis of rotation coincided with the subject's rostro-caudal axis and produced horizontal optokinetic nystagmus and afternystagmus. Wall (1) previously reported that these optokinetic afternystagmus responses were not well characterized by parametric fits to slow component velocity. The response for nose-up, however, was larger than for nose-down. This suggested that the horizontal eye movements measured during optokinetic stimulation might include an induced linear VOR component as presented in the body of this paper. To investigate this hypothesis, another analysis of these data has been made using cumulative slow component eye position. Some subjects' responses had reversals in afternystagmus direction. These reversals were "filled in" by a zero slow component velocity. This method of analysis gives a much more consistent result across subjects and shows that, on average, responses from the nose-down horizontal (prone) orientation are greatly reduced (p < 0.05) compared to other horizontal and vertical orientations. Average responses are compared to responses predicted by a model previously used to predict successfully the responses to post-rotatory nystagmus after earth horizontal axis rotation. Ten of 11 subjects had larger responses in their supine than their prone orientation. Application of horizontal axis optokinetic afternystagmus for clinical otolith function testing, and implications for altered gravity experiments are discussed.

Humans use internal models to estimate gravity and linear acceleration.

Because sensory systems often provide ambiguous information, neural processes must exist to resolve these ambiguities. It is likely that similar neural processes are used by different sensory systems. For example, many tasks require neural processing to distinguish linear acceleration from gravity, but Einstein's equivalence principle states that all linear accelerometers must measure both linear acceleration and gravity. Here we investigate whether the brain uses internal models, defined as neural systems that mimic physical principles, to help estimate linear acceleration and gravity. Internal models may be used in motor contro, sensorimotor integration and sensory processing, but direct experimental evidence for such models is limited. To determine how humans process ambiguous gravity and linear acceleration cues, subjects were tilted after being rotated at a constant velocity about an Earth-vertical axis. We show that the eye movements evoked by this post-rotational tilt include a response component that compensates for the estimated linear acceleration even when no actual linear acceleration occurs. These measured responses are consistent with our internal model predictions that the nervous system can develop a non-zero estimate of linear acceleration even when no true linear acceleration is present.

Clinical use of three-dimensional video measurements of eye movements.

Noninvasive measurements of three-dimensional eye position can be accurately achieved with video methods. A case study showing the potential clinical benefit of these enhanced measurements is presented along with some thoughts about technological advances, essential for clinical application, that are likely to occur in the next several years.

Effect of spaceflight on ability to sense and control roll tilt: human neurovestibular studies on SLS-2.

To measure adaptive changes in the ability to sense tilt after spaceflight, we measured the ability of four astronauts to control roll tilt in the presence of a pseudorandom motion disturbance before and after a 14-day Spacelab mission. The subjects were tested 1) in the dark, 2) with an independent sum-of-sines visual display, and 3) by using a control condition in which the visual cues confirmed the motion cues (counterrotating). The two subjects tested on the landing day exhibited significant decrements (P < 0.05) in their ability to control roll tilt in the dark, whereas no significant performance decrements were observed in the control condition. The absence of changes in the control condition suggests that changes in the neuromuscular component of the task and postflight fatigue were not major factors contributing to the observed performance decrement in the dark. These findings indicate an adaptive change in the way the nervous system interprets tilt cues. Readaptation of all responses appeared to be rapid, with a return to preflight values within 1-2 days after landing.

Perceptual responses to linear acceleration after spaceflight: human neurovestibular studies on SLS-2.

Perceptual responses of four astronauts were measured before and after a 14-day Spacelab Life Sciences-2 mission during interaural (y-axis) and rostrocaudal (z-axis) linear acceleration to measure adaptive changes in perceptual responses to inertial cues. In one test, subjects used a joystick to null a pseudorandom velocity disturbance. Postflight, two of three subjects showed a significantly enhanced ability to null linear self-motion in the y-axis and z-axis orientations. In another test, the subjects used a joystick to indicate their direction of motion during a series of low-acceleration steps. The postflight responses of three of the four subjects showed a significant increase in the response latency for both y-axis and z-axis orientations. In a third test, subjects were asked to track a stationary but unseen target with their eyes while they translated linearly in the dark. No significant changes were observed in the postflight responses. The observed changes, when present, may be due to a reinterpretation of inertial cues that are functionally adaptive for the microgravity environment but are not optimal for responses on Earth.

The dynamic contributions of the otolith organs to human ocular torsion.

We measured human ocular torsion (OT) monocularly (using video) and binocularly (using search coils) while sinusoidally accelerating (0.7 g) five human subjects along an earth-horizontal axis at five frequencies (0.35, 0.4, 0.5, 0.75, and 1.0 Hz). The compensatory nature of OT was investigated by changing the relative orientation of the dynamic (linear acceleration) and static (gravitational) cues. Four subject orientations were investigated: (1) Y-upright-acceleration along the interaural (y) axis while upright; (2) Y-supine-acceleration along the y-axis while supine; (3) Z-RED-acceleration along the dorsoventral (z) axis with right ear down; (4) Z-supine-acceleration along the z-axis while supine. Linear acceleration in the Y-upright, Y-supine and Z-RED orientations elicited conjugate OT. The smaller response in the Z-supine orientation appeared disconjugate. The amplitude of the response decreased and the phase lag increased with increasing frequency for each orientation. This frequency dependence does not match the frequency response of the regular or irregular afferent otolith neurons; therefore the response dynamics cannot be explained by simple peripheral mechanisms. The Y-upright responses were larger than the Y-supine responses (P < 0.05). This difference indicates that OT must be more complicated than a simple low-pass filtered response to interaural shear force, since the dynamic shear force along the interaural axis was identical in these two orientations. The Y-supine responses were, in turn, larger than the Z-RED responses (P < 0.01). Interestingly, the vector sum of the Y-supine responses plus Z-RED responses was not significantly different (P = 0.99) from the Y-upright responses. This suggests that, in this frequency range, the conjugate OT response during Y-upright stimulation might be composed of two components: (1) a response to shear force along the y-axis (as in Y-supine stimulation), and (2) a response to roll tilt of gravitoinertial force (as in Z-RED stimulation).