Biases in the perception of self-motion during whole-body acceleration and deceleration

Tremblay, Luc; Kennedy, Andrew; Paleressompoulle, Dany; Borel, Lilinane; Mouchnino, Laurence; Blouin, Jean

doi:10.3389/fnint.2013.00090

Cited by 10 publications

(11 citation statements)

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“…Gain factors were below 1 (mean ϳ0.7), indicating a general underestimation of translation, which is in line with a general underestimation of distance traveled (Tremblay et al 2013). However, performance was better than previously found with passive sinusoidal translations (Clemens et al 2012), suggesting that the content of vestibular feedback (sinusoidal vs. transient) and task conditions affect updating performance.…”

Section: Discussionmentioning

confidence: 81%

Parallax-sensitive remapping of visual space in occipito-parietal alpha-band activity during whole-body motion

Gutteling

Selen

Medendorp

2015

Journal of Neurophysiology

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Gutteling TP, Selen LP, Medendorp WP. Parallax-sensitive remapping of visual space in occipito-parietal alpha-band activity during whole-body motion. J Neurophysiol 113: 1574 -1584, 2015. First published December 10, 2014 doi:10.1152/jn.00477.2014Despite the constantly changing retinal image due to eye, head, and body movements, we are able to maintain a stable representation of the visual environment. Various studies on retinal image shifts caused by saccades have suggested that occipital and parietal areas correct for these perturbations by a gaze-centered remapping of the neural image. However, such a uniform, rotational, remapping mechanism cannot work during translations when objects shift on the retina in a more complex, depth-dependent fashion due to motion parallax. Here we tested whether the brain's activity patterns show parallax-sensitive remapping of remembered visual space during whole-body motion. Under continuous recording of electroencephalography (EEG), we passively translated human subjects while they had to remember the location of a world-fixed visual target, briefly presented in front of or behind the eyes' fixation point prior to the motion. Using a psychometric approach we assessed the quality of the memory update, which had to be made based on vestibular feedback and other extraretinal motion cues. All subjects showed a variable amount of parallaxsensitive updating errors, i.e., the direction of the errors depended on the depth of the target relative to fixation. The EEG recordings show a neural correlate of this parallax-sensitive remapping in the alphaband power at occipito-parietal electrodes. At parietal electrodes, the strength of these alpha-band modulations correlated significantly with updating performance. These results suggest that alpha-band oscillatory activity reflects the time-varying updating of gaze-centered spatial information during parallax-sensitive remapping during wholebody motion. spatial updating; EEG; alpha power; whole-body motion; remapping WE PERCEIVE THE WORLD as a stable reality, despite the ubiquitous changes in visual input due to our own movements. We do not perceive a visual shift when we make a saccade, even though the image of the world moves briskly on our retinas (Bridgeman and Nardello 1994; Schlag and Schlag-Rey 2002; von Helmholtz 1867). Also, when we walk around, our perception seems not to be disturbed by the even more complex changes in the optic flow on our retinas (see Angelaki and Hess 2005 for review). How does our brain create this percept of visual stability?There is evidence that the brain codes dynamic visual representations of the environment, which are remapped in gaze-centered coordinates when the eyes move. Various cortical and subcortical regions have been implicated in this remapping during saccadic eye movements in both primates (Colby and Goldberg 1999;Duhamel et al. 1992) In geometric terms, when the body translates through space, world-stationary objects move at different speeds and in different directions relative to the ret...

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Section: Discussionmentioning

confidence: 81%

Parallax-sensitive remapping of visual space in occipito-parietal alpha-band activity during whole-body motion

Gutteling

Selen

Medendorp

2015

Journal of Neurophysiology

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“…On the basis of recent evidence that vestibular processing is involved in changing the visuo-spatial perspective and in self-other discrimination, Deroualle and Lopez ( 2014 ) propose a vestibular contribution to several sensorimotor mechanisms that are important for social cognition. Psychological investigations have recently demonstrated how vestibular information may play a role in spatial cognition like mental imagery, bodily self-consciousness and self-motion perception, including its influences on emotional aspects and mood as reported by Mast et al ( 2014 ), Pfeiffer et al ( 2014 ), and Tremblay et al ( 2013 ), with an overview of the higher cognitive processes of self-consciousness. Mast et al ( 2014 ) also reports how vestibular disorders and some psychiatric symptoms may be entangled, completing the review of Gurvich et al ( 2013 ).…”

Section: Spatial Cognition Bodily and Self-motion Perceptionmentioning

confidence: 88%

Editorial: The Vestibular System in Cognitive and Memory Processes in Mammalians

Besnard

Lopez

Brandt

et al. 2015

Front. Integr. Neurosci.

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International audienceIn the nineteenth century Pierre–Jean–Marie Flourens (1825) and Ernst Mach described the vestibular system and its peripheral organs while Robert Barany, rewarded by the Nobel prize in 1914, was the first to investigate vestibular disorders with caloric tests making surgical treatments of the vestibular organ possible. Recently, Graf and Klam (2006) have reminded us that this ancient sensory system appeared more than 500 million years ago. Logically its influence would most likely not be restricted to balance reflexes at the brainstem level; it must have also shaped our brain. The vestibular system is the one sensory organ dedicated to gravity perception, which along with light and oxygen served as a motor of evolution. In the 1950s the groups of Otto–Joachim Grüsser in Germany, Wilder Penfield in Canada, and later the group of Alain Berthoz in France, demonstrated in elegant experiments on awake monkey (Guldin and Grüsser, 1998), epileptic patient (Penfield, 1957), and neurologically-normal human (Lobel et al., 1999) the existence of vestibular projections to the cortex and how they combine with visual and proprioceptive information. An increasing number of researchers, often fervent disciples, have built on these findings to produce a spate of publications that have consolidated the evidence for a sense of verticality and three-dimensional body representations within the vestibular cortical areas. In the 1990s Paul Smith and colleagues examined vestibular processing in the hippocampus and its role in spatial memory. Exploring this topic in the rodent (Smith, 1997), they began to elucidate the secrets and the previously silent functions of the vestibular system. These findings led to increasing clarity about how vestibular degeneration may be related to some aspects of dementia (Previc, 2013), psychiatric diseases (Gurvich et al., 2013), and cognitive impairments in the elderly (Bigelow et al., 2015; Semenov et al., 2015). The research by Marianne Dieterich and Thomas Brandt has examined the bilateral organization of multiple multisensory cortical areas and revealed the vestibular dominance of the non-dominant hemisphere (Dieterich et al., 2003). They addressed the following questions: how is one global percept of motion and orientation in space formed, and does this dominance determine the lateralization of brain function such as handedness (Brandt and Dieterich, 2015)? A vestibular contribution to the most crucial aspects of the human sense of self and self-consciousness has recently been highlighted by neurological and neuroscientific investigations: vestibular signals contribute to the experience that the self is located within the boundaries of the body (Blanke et al., 2004; Lopez et al., 2008) and may even be involved in self-other discrimination and interactions (Lenggenhager and Lopez, 2015).In this Frontiers in Integrative Neuroscience Research Topic initiated by Sidney Simon, twenty-four articles highlight recent discoveries in the field of vestibular cognition, including: (1) Ana...

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“…On the whole, we suggest that the effect of asymmetric rotation on central processing is responsible for the perceptual persistent asymmetry and that the preceding fast rotation is the critical factor responsible for keeping the gain of the slow responses down. When contrasting high and low frequencies are delivered in combination or in sequence, as with the stimulus used here, the perception of higher over lower frequency rotations is favored ( Massot et al 2012 ; Panichi et al 2011 ; Pettorossi et al 2013 ; Tremblay et al 2013 ). This centrally mediated phenomenon due to frequency contrast selectively affects perception of self-motion but not reflex function such as the VOR, and our present results demonstrate that the loss of unilateral peripheral vestibular input preserves this central adaptive property.…”

Section: Discussionmentioning

confidence: 99%

Asymmetric vestibular stimulation reveals persistent disruption of motion perception in unilateral vestibular lesions

Panichi

Faralli

Bruni

et al. 2017

Journal of Neurophysiology

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Self-motion perception was studied in patients with unilateral vestibular lesions (UVL) due to acute vestibular neuritis at 1 wk and 4, 8, and 12 mo after the acute episode. We assessed vestibularly mediated self-motion perception by measuring the error in reproducing the position of a remembered visual target at the end of four cycles of asymmetric whole-body rotation. The oscillatory stimulus consists of a slow (0.09 Hz) and a fast (0.38 Hz) half cycle. A large error was present in UVL patients when the slow half cycle was delivered toward the lesion side, but minimal toward the healthy side. This asymmetry diminished over time, but it remained abnormally large at 12 mo. In contrast, vestibulo-ocular reflex responses showed a large direction-dependent error only initially, then they normalized. Normalization also occurred for conventional reflex vestibular measures (caloric tests, subjective visual vertical, and head shaking nystagmus) and for perceptual function during symmetric rotation. Vestibular-related handicap, measured with the Dizziness Handicap Inventory (DHI) at 12 mo correlated with self-motion perception asymmetry but not with abnormalities in vestibulo-ocular function. We conclude that 1) a persistent self-motion perceptual bias is revealed by asymmetric rotation in UVLs despite vestibulo-ocular function becoming symmetric over time, 2) this dissociation is caused by differential perceptual-reflex adaptation to high- and low-frequency rotations when these are combined as with our asymmetric stimulus, 3) the findings imply differential central compensation for vestibuloperceptual and vestibulo-ocular reflex functions, and 4) self-motion perception disruption may mediate long-term vestibular-related handicap in UVL patients.NEW & NOTEWORTHY A novel vestibular stimulus, combining asymmetric slow and fast sinusoidal half cycles, revealed persistent vestibuloperceptual dysfunction in unilateral vestibular lesion (UVL) patients. The compensation of motion perception after UVL was slower than that of vestibulo-ocular reflex. Perceptual but not vestibulo-ocular reflex deficits correlated with dizziness-related handicap.

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Biases in the perception of self-motion during whole-body acceleration and deceleration

Cited by 10 publications

References 64 publications

Parallax-sensitive remapping of visual space in occipito-parietal alpha-band activity during whole-body motion

Parallax-sensitive remapping of visual space in occipito-parietal alpha-band activity during whole-body motion

Editorial: The Vestibular System in Cognitive and Memory Processes in Mammalians

Asymmetric vestibular stimulation reveals persistent disruption of motion perception in unilateral vestibular lesions

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