Oculometric Assessment of Sensorimotor Impairment Associated with TBI.

PURPOSE: Diffuse tissue damage from impact or blast traumatic brain injury (TBI) degrades information processing throughout the brain, often resulting in impairments in sensorimotor function. We have developed an eye-movement assessment test, consisting of a simple, appropriately randomized, radial tracking task together with a broad set of oculometric measures that can be combined to yield a sensitive overall indicator of sensorimotor functional status. We show here that this multidimensional method can be used to detect and characterize sensorimotor deficits associated with TBI. METHODS: To compare dynamic visuomotor processing of TBI subjects (n = 34) with a separate control population (n = 41), we used the Comprehensive Oculometric Behavioral Response Assessment (COBRA) method (Liston & Stone, J Vision. 14:12, 2014) to quantify 10 performance metrics for each subject. Each TBI subject's set of oculometrics was then combined to compute a single TBI impairment vector whose magnitude we refer to as the impairment index. RESULTS: In our TBI population, several individual oculometrics were significantly degraded, including pursuit latency, initial pursuit acceleration, pursuit gain, catch-up saccade amplitude, proportion smooth tracking, and speed responsiveness. Furthermore, the TBI impairment index discriminated TBI subjects from controls with an 81% probability that increased with self-reported TBI severity; although the 9 subjects self-reporting "little-to-no" residual impairment were statistically indistinguishable from controls (58% probability), the remaining 25 subjects were easily detectable (91% probability). Given the demonstrated link between higher-order visual perception/cognition and eye movements, we interpret the observed TBI-related impairments as degradations in the speed, accuracy, and precision of information processing within cortical circuits supporting higher-order visual processing and sensorimotor control, not just low-level brainstem motor deficits. CONCLUSIONS: We conclude that multidimensional oculometric testing could be used as a sensitive screen for subtle neurological signs of subclinical neurological insults, to quantify functional impairment, to monitor deterioration or recovery, and to evaluate treatment efficacy.

Redundancy reduction explains the expansion of visual direction space around the cardinal axes.

Motion direction discrimination in humans is worse for oblique directions than for the cardinal directions (the oblique effect). For some unknown reason, the human visual system makes systematic errors in the estimation of particular motion directions; a direction displacement near a cardinal axis appears larger than it really is whereas the same displacement near an oblique axis appears to be smaller. Although the perceptual effects are robust and are clearly measurable in smooth pursuit eye movements, all attempts to identify the neural underpinnings for the oblique effect have failed. Here we show that a model of image velocity estimation based on the known properties of neurons in primary visual cortex (V1) and the middle temporal (MT) visual area of the primate brain produces the oblique effect. We also provide an explanation for the unusual asymmetric patterns of inhibition that have been found surrounding MT neurons. These patterns are consistent with a mechanism within the visual system that prevents redundant velocity signals from being passed onto the next motion-integration stage, (dorsal Medial superior temporal, MSTd). We show that model redundancy-reduction mechanisms within the MT-MSTd pathway produce the oblique effect.

Oculometric assessment of dynamic visual processing.

Eye movements are the most frequent (∼3/s), shortest-latency (∼150-250 ms), and biomechanically simplest (one joint, no inertial complexities) voluntary motor behavior in primates, providing a model system to assess sensorimotor disturbances arising from trauma, fatigue, aging, or disease states. We have developed a 15-min behavioral tracking protocol consisting of randomized Rashbass (1961) step-ramp radial target motion to assess several aspects of the behavioral response to visual motion, including pursuit initiation, steady-state tracking, direction tuning, and speed tuning. We show how oculomotor data can be converted into direction- and speed-tuning oculometric functions, with large increases in efficiency over traditional button-press psychophysics. We also show how the latter two can be converted into standard visual psychometric thresholds. To assess our paradigm, we first tested for the psychometric criterion of repeatability, and report that our metrics are reliable across repeated sessions. Second, we tested for the psychometric criterion of validity, and report that our metrics show the anticipated changes as the motion stimulus degrades due to spatiotemporal undersampling. Third, we documented the distribution of these metrics across a population of 41 normal observers to provide a thorough quantitative picture of normal human ocular tracking performance, with practice and expectation effects minimized. Our method computes 10 metrics that quantify various aspects of the eye-movement response during a simple 15-min clinical test, which could be used as a screening or assessment tool for disorders affecting sensorimotor processing, including degenerative retinal disease; developmental, neurological or psychiatric disorders; strokes; and traumatic brain injury.

G-loading and vibration effects on heart and respiration rates.

BACKGROUND: Operational environments expose pilots and astronauts to sustained acceleration (G loading) and whole-body vibration, alone and in combination. Separately, the physiological effects of G loading and vibration have been well studied; both have effects similar to mild exercise. The few studies of combined G loading and vibration have not reported an interaction between these factors on physiological responses. METHODS: We tested the effects of G loading (+1 and +3.8 G(x)) and vibration (0.5 gx at 8, 12, and 16 Hz), alone and in combination, on heart and respiration rate. RESULTS: We observed an effect of G loading on heart rate (average increase of 23 bpm, SD 12) and respiration rate (average increase of 5 breaths per minute, SD 5), an effect of vibration on heart rate, and an interaction on heart rate. With vibration, we observed heart rate increases of 4 bpm (SD: 3) with no increase in respiration rate. In the +1 G(x) condition, the largest heart rate increase occurred during low-frequency (8 Hz) vibration, while at +3.8 G(x), the largest heart rate increase occurred during high-frequency (16 Hz) vibration, demonstrating interaction. DISCUSSION: Consistent with previous reports, our G-loading and vibration effects are similar to mild exercise. In addition, we observed an interaction between G loading and vibration on heart rate, with maximum heart rates occurring at a higher vibration frequency at +3.8 G(x) compared to +1 G(x). The observed interaction demonstrates that G-loading and vibration effects are not independent and can only be properly assessed during combined exposure.

Onset of positional vertigo during exposure to combined G loading and chest-to-spine vibration.

BACKGROUND: Aerospace environments commonly expose pilots to vibration and sustained acceleration, alone and in combination. CASE REPORTS: Of 16 experimental research participants, 3 reported symptoms of vertigo and signs of torsional nystagmus during or shortly following exposure to sustained chest-to-spine (+3.8 Gx) acceleration (G loading) and chest-to-spine (0.5 g(x)) vibration in the 8-16 Hz band. Two of the participants reported intermittent vertigo for up to 2 wk, were diagnosed with benign paroxysmal positional vertigo (BPPV), and were treated successfully with the Epley Maneuver. On a follow-up survey, a third participant reported transient BPPV-like vertigo, which resolved spontaneously. The follow-up survey also prompted participants to self-report other effects following research protocol exposure to vibration and G loading, revealing details about other minor and transient, but more common, effects that resolved within 3 h. DISCUSSION: Our studies indicated a significantly elevated incidence of BPPV following exposure to vibration plus G loading compared to vibration alone that was positively correlated with participant age. One mechanism for the rolling sensation in BPPV involves broken or dislodged otoconia floating within one of the posterior semicircular canals, making the canal gravity-sensitive. Our observations highlight a heretofore unforeseen risk of otolith damage sustained during launch, undetectable in space, potentially contributing to vertigo and perceived tumbling upon re-entry from microgravity.

Saccadic brightness decisions do not use a difference model.

Eye movements are the most frequent (∼3 per second), shortest-latency (∼150-250 ms), and biomechanically simplest (1 joint, no inertial complexities) voluntary motor behavior in primates, providing a model sensorimotor decision-making system. Current computational "difference" models of choice behavior utilize a single decision variable encoding the difference between two alternate signals, often implemented as a log-likelihood ratio. Alternatively, the oculomotor literature describes a "race" mechanism, in which two separate decision variables encoding the two alternate signals race against one another independently. These two models make two qualitatively distinct predictions, which can be tested empirically with a two-alternative forced-choice task. Unlike the race model, a decision variable based upon a differencing operation predicts strong mirror image correlations between response time (RT) and the signal strengths of the selected and unselected stimuli (because differencing creates equal and opposite correlations). In a saccadic brightness discrimination task, we observed positive correlations between response rate (1/RT) and the strength of both the selected and unselected stimulus, a simple qualitative prediction of race models that applies to any 2AFC task but which is fundamentally at odds with the most basic prediction of any difference model. Our data are, however, qualitatively consistent with a mechanism in which two competing motor plans co-exist and their two corresponding neural decision variables race to a threshold to drive the saccadic decision.

Rethinking human visual attention: spatial cueing effects and optimality of decisions by honeybees, monkeys and humans.

Visual attention is commonly studied by using visuo-spatial cues indicating probable locations of a target and assessing the effect of the validity of the cue on perceptual performance and its neural correlates. Here, we adapt a cueing task to measure spatial cueing effects on the decisions of honeybees and compare their behavior to that of humans and monkeys in a similarly structured two-alternative forced-choice perceptual task. Unlike the typical cueing paradigm in which the stimulus strength remains unchanged within a block of trials, for the monkey and human studies we randomized the contrast of the signal to simulate more real world conditions in which the organism is uncertain about the strength of the signal. A Bayesian ideal observer that weights sensory evidence from cued and uncued locations based on the cue validity to maximize overall performance is used as a benchmark of comparison against the three animals and other suboptimal models: probability matching, ignore the cue, always follow the cue, and an additive bias/single decision threshold model. We find that the cueing effect is pervasive across all three species but is smaller in size than that shown by the Bayesian ideal observer. Humans show a larger cueing effect than monkeys and bees show the smallest effect. The cueing effect and overall performance of the honeybees allows rejection of the models in which the bees are ignoring the cue, following the cue and disregarding stimuli to be discriminated, or adopting a probability matching strategy. Stimulus strength uncertainty also reduces the theoretically predicted variation in cueing effect with stimulus strength of an optimal Bayesian observer and diminishes the size of the cueing effect when stimulus strength is low. A more biologically plausible model that includes an additive bias to the sensory response from the cued location, although not mathematically equivalent to the optimal observer for the case stimulus strength uncertainty, can approximate the benefits of the more computationally complex optimal Bayesian model. We discuss the implications of our findings on the field's common conceptualization of covert visual attention in the cueing task and what aspects, if any, might be unique to humans.

Effects of prior information and reward on oculomotor and perceptual choices.

Expectations about the environment influence motor behavior. In simple tasks, for example, prior knowledge about which stimulus event will likely occur or which response will likely be rewarded induces a tendency to take the favored action (i.e., a motor or response bias), especially when sensory information is sparse or ambiguous. Models of choice behavior account for this bias by weighting decision alternatives unequally, either at an early sensory-input stage or at a downstream motor-output stage. These two alternatives can be distinguished empirically; the former predicts an altered percept that correlates with motor bias, the latter predicts no perceptual effect. By varying the prior probability of target or reward location, we induced biased oculomotor responses in a brightness selection task with human subjects. We found that the induced motor bias was correlated with an amplification of both the sensory signals and internal noise underlying brightness perception, without a systematic change in perceived overall brightness. We also found that the magnitude of the sensory amplification was correlated with the amount of noise in the brightness percept, consistent with a multiplicative weighting factor located downstream from the limiting internal sensory noise. Our data demonstrate that prior knowledge (about target location or reward) shapes visual signals for perception and action in parallel but does not improve the quality (i.e., signal-to-noise ratio) of sensory processing.