Visual and vestibular perceptual thresholds each demonstrate better precision at specific frequencies and also exhibit optimal integration

Abstract

Karmali F, Lim K, Merfeld DM. Visual and vestibular perceptual thresholds each demonstrate better precision at specific frequencies and also exhibit optimal integration. J Neurophysiol 111: 2393-2403, 2014. First published December 26, 2013 doi:10.1152/jn.00332.2013.-Prior studies show that visual motion perception is more precise than vestibular motion perception, but it is unclear whether this is universal or the result of specific experimental conditions. We compared visual and vestibular motion precision over a broad range of temporal frequencies by measuring thresholds for vestibular (subject motion in the dark), visual (visual scene motion) or visual-vestibular (subject motion in the light) stimuli. Specifically, thresholds were measured for motion frequencies spanning a two-decade physiological range (0.05-5 Hz) using single-cycle sinusoidal acceleration roll tilt trajectories (i.e., distinguishing left-side down from right-side down). We found that, while visual and vestibular thresholds were broadly similar between 0.05 and 5.0 Hz, each cue is significantly more precise than the other at certain frequencies. Specifically, we found that 1) visual and vestibular thresholds were indistinguishable at 0.05 Hz and 2 Hz (i.e., similarly precise); 2) visual thresholds were lower (i.e., vision more precise) than vestibular thresholds between 0.1 Hz and 1 Hz; and 3) visual thresholds were higher (i.e., vision less precise) than vestibular thresholds above 2 Hz. This shows that vestibular perception can be more precise than visual perception at physiologically relevant frequencies. We also found that sensory integration of visual and vestibular information is consistent with static Bayesian optimal integration of visual-vestibular cues. In contrast with most prior work that degraded or altered sensory cues, we demonstrated static optimal integration using natural cues.

Determining thresholds using adaptive procedures and psychometric fits: evaluating efficiency using theory, simulations, and human experiments

“…The study was approved by the local institutional review board and was performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki. Each subject was screened using a detailed, standard vestibular diagnostic clinical exam to confirm the absence of undiagnosed vestibular disorders (Grabherr, Nicoucar, Mast, and Merfeld 2008;Valko, Priesol, Lewis, and Merfeld 2012;Chaudhuri, Karmali et al 2013;Karmali, Lim, and Merfeld 2014). Screening included Hallpike tests, angular vestibuloocular reflex (VOR) evoked via rotation, caloric testing, and posture control measures.…”

“…We attempted to minimize the influence of non-vestibular cues using the same approaches previously used (Grabherr, Nicoucar, Mast, and Merfeld 2008;Valko, Priesol, Lewis, and Merfeld 2012;Chaudhuri, Karmali, and Merfeld 2013;Karmali, Lim, and Merfeld 2014). Briefly, subjects were secured with a five-point harness in a racing-style chair, with their head fixed relative to the chair and platform with a vacuum cushion snugly pressed between two adjustable plates.…”

“…with visual or vestibular stimuli) because of the time required to present relevant dynamic stimuli for each trial. For example, thresholds for single cycles of 0.1 Hz sinusoidal motion which take 10 seconds to present are different for vestibular migraine subjects compared to other subjects (Lewis, Priesol, Nicoucar, Lim, and Merfeld 2011), and it is often informative to measure thresholds at multiple frequencies (Nakayama and Tyler 1981;Benson, Spencer, and Stott 1986;Benson, Hutt, and Brown 1989;Grabherr, Nicoucar, Mast, and Merfeld 2008;Lewis, Priesol, Nicoucar, Lim, and Merfeld 2011;Soyka, Robuffo et al 2011;Valko, Priesol, Lewis, and Merfeld 2012;Haburcakova, Lewis et al 2012;Karmali, Lim et al 2014). …”

Dynamics of individual perceptual decisions

“…Given the dynamic ranges (i.e., frequency ranges) investigated, these measured threshold variations as a function of frequency typically reflect peripheral transduction processes and typically have not told us much about decisionmaking dynamics. With the exception of some vestibular threshold studies (e.g., Benson et al 1986Benson et al , 1989Grabherr et al 2008;Haburcakova et al 2012;Karmali et al 2014;Lewis et al 2011aLewis et al , 2011bLim and Merfeld 2012;Mardirossian et al 2014;Priesol et al 2014;Soyka et al 2011Soyka et al , 2012Valko et al 2012), decision-making studies using signal detection methods have rarely focused on dynamics (e.g., perceptual decisions as a function of frequency, where the frequency is in a range relevant to decision-making as opposed to sensory transduction). As discussed later in this review, such vestibular threshold studies may help inform us about decision-making dynamics because behaviorally relevant stimulus frequencies overlap with frequencies influenced by decision-making dynamics.…”

“…A third study (Lagacé-Nadon et al 2009) tested roll motion (i.e., about the line of sight) using a forced-choice recognition approach for continuous sinusoids between 0.25 and 2 Hz and also reported similar results, with a slope consistent with a high-pass filter up to 1 Hz, with a possible flattening at around 2 Hz. Karmali et al (2014) recently tested visual motion perception using a direction-recognition rather than motion-detection task and single-cycle acceleration motions rather than multiple sinusoidal cycles, over a broad frequency range of 0.05 to 5 Hz. The study also used a "natural" visual scene that included typical objects seen in daily life rather than random dot patterns.…”