Vestibular System: The Many Facets of a Multimodal Sense

Angelaki, Dora E.; Cullen, Kathleen E.

doi:10.1146/annurev.neuro.31.060407.125555

Cited by 761 publications

(605 citation statements)

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“…These animals show a more or less complete recovery of the lesion-induced static postural deficits over time (Dieringer, 1995;Curthoys, 2000), facilitated by the multimodality of the vestibular system (Angelaki and Cullen, 2008). The recovery is a distributed process (Llinás and Walton, 1979) and involves cellular changes as well as sensory substitutions of the removed vestibular inputs in particular by forelimb proprioceptive signals (Straka et al, 2005).…”

Section: Discussionmentioning

confidence: 99%

Vestibular Asymmetry as the Cause of Idiopathic Scoliosis: A Possible Answer fromXenopus

Lambert¹,

Malinvaud²,

Glaunès

et al. 2009

J. Neurosci.

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Human idiopathic scoliosis is characterized by severe deformations of the spine and skeleton. The occurrence of vestibular-related deficits in these patients is well established but it is unclear whether a vestibular pathology is the common cause for the scoliotic syndrome and the gaze/posture deficits or if the latter behavioral deficits are a consequence of the scoliotic deformations. A possible vestibular origin was tested in the frog Xenopus laevis by unilateral removal of the labyrinthine endorgans at larval stages. After metamorphosis into young adult frogs, X-ray images and three-dimensional reconstructed micro-computer tomographic scans of the skeleton showed deformations similar to those of scoliotic patients. The skeletal distortions consisted of a curvature of the spine in the frontal and sagittal plane, a transverse rotation along the body axis and substantial deformations of all vertebrae. In terrestrial vertebrates, the initial postural syndrome after unilateral labyrinthectomy recovers over time and requires body weight-supporting limb proprioceptive information. In an aquatic environment, however, this information is absent. Hence, the lesion-induced asymmetric activity in descending spinal pathways and the resulting asymmetric muscular tonus persists. As a consequence the mostly cartilaginous skeleton of the frog tadpoles progressively deforms. Lack of limb proprioceptive signals in an aquatic environment is thus the element, which links the Xenopus model with human scoliosis because a comparable situation occurs during gestation in utero. A permanently imbalanced activity in descending locomotor/posture control pathways might be the common origin for the observed structural and behavioral deficits in humans as in the different animal models of scoliosis.

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Section: Discussionmentioning

confidence: 99%

Vestibular Asymmetry as the Cause of Idiopathic Scoliosis: A Possible Answer fromXenopus

Lambert¹,

Malinvaud²,

Glaunès

et al. 2009

J. Neurosci.

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“…Next to motor and proprioceptive signals, spatial perspective taking may also involve the integration of vestibular information, associated with either active or passive motion of the body. For instance, rotating oneself on a desk chair to take the same visual perspective as a colleague results in a stimulation of the semicircular channels and in the spatial updating of our own body position based on visual and vestibular information (Angelaki & Cullen, 2008). Rieser, Guth, & Hill, (1986) have underlined the importance of vestibular information for spatial localization, by showing that blindfolded participants walking a short distance were well able to keep track of their visuo-spatial perspective.…”

Section: Introductionmentioning

confidence: 99%

Imagined own-body transformations during passive self-motion

Elk

Blanke

2013

Psychological Research

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Spatial perspective taking is a crucial social skill that underlies many of our everyday interactions. Previous studies have suggested that spatial perspective taking is an embodied process that involves the integration of both motor and proprioceptive information. Given the importance of vestibular signals for own-body perception, mental own-body imagery, and bodily self-consciousness, in the present study we hypothesized that vestibular stimulation due to passive own-body displacements should also modulate spatial perspective taking. Participants performed an own-body transformation task while being passively rotated in a clockwise or counter-clockwise direction on a human motion platform. A congruency effect was observed, reflected in faster reaction times if the implied mental body rotation direction matched the actual rotation direction of the chair. These findings indicate that vestibular stimulation modulates and facilitates mental perspective taking, thereby highlighting the importance of integrating multisensory bodily information for spatial perspective taking.

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“…Consistently, lesions of vestibular nuclei disrupt angular tuning of head-direction cells 14 and spatial tuning of hippocampal place cells 15 , although lesions of the headdirection cell network, which is thought to provide vestibular input to the hippocampus, do not substantially alter hippocampal spatial selectivity 16 . Additionally, the output of vestibular nuclei suppresses self-motion signals and depends on multisensory stimuli 17 . Indeed, in all the experiments described above, it is difficult to dissociate the contribution of distal visual cues from the contributions of other cues.…”

mentioning

confidence: 99%

Impaired spatial selectivity and intact phase precession in two-dimensional virtual reality

et al. 2014

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During real-world (RW) exploration, rodent hippocampal activity shows robust spatial selectivity, which is hypothesized to be governed largely by distal visual cues, although other sensory-motor cues also contribute. Indeed, hippocampal spatial selectivity is weak in primate and human studies that use only visual cues. To determine the contribution of distal visual cues only, we measured hippocampal activity from body-fixed rodents exploring a two-dimensional virtual reality (VR). Compared to that in RW, spatial selectivity was markedly reduced during random foraging and goal-directed tasks in VR. Instead we found small but significant selectivity to distance traveled. Despite impaired spatial selectivity in VR, most spikes occurred within ~2-s-long hippocampal motifs in both RW and VR that had similar structure, including phase precession within motif fields. Selectivity to space and distance traveled were greatly enhanced in VR tasks with stereotypical trajectories. Thus, distal visual cues alone are insufficient to generate a robust hippocampal rate code for space but are sufficient for a temporal code. npg © 2015 Nature America, Inc. All rights reserved.1 2 2 VOLUME 18 | NUMBER 1 | JANUARY 2015 nature neurOSCIenCe a r t I C l e S same physical location in space can be approached from multiple different directions at different speeds. We thus investigated the contribution of distal visual cues only in determining selectivity in such an experimental setup. RESULTS Nature of spatial selectivity of hippocampal responsesWe measured hippocampal activity during a two-dimensional randomforaging task in RW and VR [35][36][37] with similar distal visual cues (Fig. 1a). In VR, the rats were body-fixed, i.e., their bodies were held in place, with a harness on a floating ball, allowing for head movements but precluding full-body turns, thus minimizing vestibular cues (Online Methods) 21,36 . Rats quickly learned to avoid the virtual edges entirely on the basis of visual cues 36 and spent a similar amount of time away from the edges and in the center of the platform (Fig. 1a) compared to in RW. We measured the activity of 1,066 and 1,238 principal neurons in RW and VR, respectively, in the dorsal CA1 of four rats under a variety of conditions (Online Methods). Neurons fired vigorously in restricted regions of space in RW, as expected (Fig. 1b,c, Supplementary Fig. 1a and Supplementary Video 1) 1 . In contrast, the neurons showed little spatial selectivity in VR during random foraging (Fig. 1b,d and Supplementary Fig. 1b).Across the ensemble, neurons had moderately reduced (25%) mean firing rates but greatly reduced (68%) peak firing rates in VR ( Fig. 2a and Supplementary Fig. 2a). Neurons in VR also had greatly reduced spatial information content (75%), stability (59%), sparsity (42%) and coherence (40%) (Fig. 2b-d and Supplementary Fig. 2b,c) compared to spatially localized, stable and sparse RW rate maps (Fig. 2c). Although the mean firing rate was inversely correlated with information content (Supplementary Fig. 2d)...

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Vestibular System: The Many Facets of a Multimodal Sense

Cited by 761 publications

References 118 publications

Vestibular Asymmetry as the Cause of Idiopathic Scoliosis: A Possible Answer fromXenopus

Vestibular Asymmetry as the Cause of Idiopathic Scoliosis: A Possible Answer fromXenopus

Imagined own-body transformations during passive self-motion

Impaired spatial selectivity and intact phase precession in two-dimensional virtual reality

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