Human perception of whole body roll-tilt orientation in a hypogravity analog: underestimation and adaptation

Galvan-Garza, Raquel; Clark, Torin K.; Sherwood, David P.; Diaz‐Artiles, Ana; Rosenberg, M. J. F.; Natapoff, Alan; Karmali, Faisal; Oman, Charles M.; Young, Laurence R.

doi:10.1152/jn.00140.2018

Cited by 13 publications

(9 citation statements)

References 49 publications

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“…For any tilt angle, this otolith organ cue is diminished when gravitational forces are reduced. This is supported by our recent work that found that perception of roll tilt is underestimated in a hypogravity analog (Galvan-Garza et al 2018). Likewise, we assume that noise is relatively unchanged, although future studies could investigate whether noise varies with G C by performing the threshold task during centrifugation.…”

Section: Discussionsupporting

confidence: 81%

Human manual control precision depends on vestibular sensory precision and gravitational magnitude

Rosenberg

Galvan-Garza

Clark

et al. 2018

Journal of Neurophysiology

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Precise motion control is critical to human survival on Earth and in space. Motion sensation is inherently imprecise, and the functional implications of this imprecision are not well understood. We studied a “vestibular” manual control task in which subjects attempted to keep themselves upright with a rotational hand controller (i.e., joystick) to null out pseudorandom, roll-tilt motion disturbances of their chair in the dark. Our first objective was to study the relationship between intersubject differences in manual control performance and sensory precision, determined by measuring vestibular perceptual thresholds. Our second objective was to examine the influence of altered gravity on manual control performance. Subjects performed the manual control task while supine during short-radius centrifugation, with roll tilts occurring relative to centripetal accelerations of 0.5, 1.0, and 1.33 GC (1 GC = 9.81 m/s2). Roll-tilt vestibular precision was quantified with roll-tilt vestibular direction-recognition perceptual thresholds, the minimum movement that one can reliably distinguish as leftward vs. rightward. A significant intersubject correlation was found between manual control performance (defined as the standard deviation of chair tilt) and thresholds, consistent with sensory imprecision negatively affecting functional precision. Furthermore, compared with 1.0 GC manual control was more precise in 1.33 GC (−18.3%, P = 0.005) and less precise in 0.5 GC (+39.6%, P < 0.001). The decrement in manual control performance observed in 0.5 GC and in subjects with high thresholds suggests potential risk factors for piloting and locomotion, both on Earth and during human exploration missions to the moon (0.16 G) and Mars (0.38 G). NEW & NOTEWORTHY The functional implications of imprecise motion sensation are not well understood. We found a significant correlation between subjects’ vestibular perceptual thresholds and performance in a manual control task (using a joystick to keep their chair upright), consistent with sensory imprecision negatively affecting functional precision. Furthermore, using an altered-gravity centrifuge configuration, we found that manual control precision was improved in “hypergravity” and degraded in “hypogravity.” These results have potential relevance for postural control, aviation, and spaceflight.

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Section: Discussionsupporting

confidence: 81%

Human manual control precision depends on vestibular sensory precision and gravitational magnitude

Rosenberg

Galvan-Garza

Clark

et al. 2018

Journal of Neurophysiology

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“…To simplify, the HTPG represents gravity perception during head roll‐tilt, whereas the HU‐SVV means gravity perception only when the head is upright. Although the perceptual gain (HTP/HTA) of a head‐roll condition has been reported in a previous study, 27 the HTPG is unique in that it expresses the perceptual gain during multiple left or right head roll‐tilt conditions as a single parameter. The decisive factor in favor of using the HTPG was the linearity between the HTP and HTA during head roll‐tilt at approximately 30° when keeping an upright trunk condition, since in the principal experiment the HTPG was slightly larger than 1, that is, the E‐effect was observed.…”

Section: Discussionmentioning

confidence: 89%

Effect of head roll‐tilt on the subjective visual vertical in healthy participants: Towards better clinical measurement of gravity perception

Wada

Yamanaka

Kitahara

et al. 2020

Laryngoscope Investig Oto

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Objective: Gravity perception is an essential function for spatial orientation and postural stability; however, its assessment is not easy. We evaluated the head-tilt perception gain (HTPG, that is, mean perceptual gain [perceived/actual tilt angle] during left or right head roll-tilt conditions) and head-upright subjective visual vertical (SVV) using a simple method developed by us to investigate the characteristics of gravity perception in healthy participants. Methods: We measured the SVV and head roll-tilt angle during head roll-tilt within ±30 of vertical in the sitting and standing positions while the participant maintained an upright trunk (sitting, 434 participants; standing, 263 participants). We evaluated the head-upright SVV, HTPG, and laterality of the HTPG. Results: We determined the reference ranges of the absolute head-upright SVV (<2.5), HTPG (0.80-1.25), and HTPG laterality (<10%) for the sitting position. The head-upright SVV and HTPG laterality were not influenced by sex or age. However, the HTPG was significantly greater in women than in men and in middle-aged (30-64 years) and elderly (65-88 years) participants than in young participants (18-29 years). The HTPG, but not the head-upright SVV or HTPG laterality, was significantly higher in the standing vs sitting position. Conclusion: The HTPG is a novel parameter of gravity perception involving functions of the peripheral otolith and neck somatosensory systems to the central nervous system. The HTPG in healthy participants is influenced by age and sex in the sitting position and immediately increases after standing to reinforce the righting reflex for unstable posture, which was not seen in the head-upright SVV, previously considered the only parameter.

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“…In each case, the internal magnitude of gravity predicted by the model presumably cannot be directly measured empirically. Instead, perceptions of motion (e.g., tilt perception) can be assessed using psychophysical tasks (Clark et al, 2015b;Clark and Young, 2017;Galvan-Garza et al, 2018), during and following gravity transitions, in order to validate model predictions. Transitions to hyper-gravity (Schone, 1964;Clark et al, 2015a,b) can be performed using human-rated centrifuges.…”

Section: Summary Of Results and Contributionsmentioning

confidence: 99%

“…However, sensory information [e.g., from the otoliths (Fernandez and Goldberg, 1976)] is altered following a gravity transition (Clark et al, 2015b;Galvan-Garza et al, 2018), making the internal models inappropriate (Clark et al, 2015c). This results in misperceptions of orientation (Clement et al, 2007;Clement and Wood, 2012;de Winkel et al, 2012) and large, sustained sensory conflict.…”

Section: Background and Existing Workmentioning

confidence: 99%

COMPASS: Computations for Orientation and Motion Perception in Altered Sensorimotor States

Kravets

Dixon

Ahmed

et al. 2021

Front. Neural Circuits

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Reliable perception of self-motion and orientation requires the central nervous system (CNS) to adapt to changing environments, stimuli, and sensory organ function. The proposed computations required of neural systems for this adaptation process remain conceptual, limiting our understanding and ability to quantitatively predict adaptation and mitigate any resulting impairment prior to completing adaptation. Here, we have implemented a computational model of the internal calculations involved in the orientation perception system’s adaptation to changes in the magnitude of gravity. In summary, we propose that the CNS considers parallel, alternative hypotheses of the parameter of interest (in this case, the CNS’s internal estimate of the magnitude of gravity) and uses the associated sensory conflict signals (i.e., difference between sensory measurements and the expectation of them) to sequentially update the posterior probability of each hypothesis using Bayes rule. Over time, an updated central estimate of the internal magnitude of gravity emerges from the posterior probability distribution, which is then used to process sensory information and produce perceptions of self-motion and orientation. We have implemented these hypotheses in a computational model and performed various simulations to demonstrate quantitative model predictions of adaptation of the orientation perception system to changes in the magnitude of gravity, similar to those experienced by astronauts during space exploration missions. These model predictions serve as quantitative hypotheses to inspire future experimental assessments.

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Human perception of whole body roll-tilt orientation in a hypogravity analog: underestimation and adaptation

Cited by 13 publications

References 49 publications

Human manual control precision depends on vestibular sensory precision and gravitational magnitude

Human manual control precision depends on vestibular sensory precision and gravitational magnitude

Effect of head roll‐tilt on the subjective visual vertical in healthy participants: Towards better clinical measurement of gravity perception

COMPASS: Computations for Orientation and Motion Perception in Altered Sensorimotor States

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