Balancing the Mind Vestibular Induced Facilitation of Egocentric Mental
01 Jan 2012-
TL;DR: The results show that vestibular information can influence higher-order cognitive processes, such as the body schema and mental imagery, as well as top-down imagined whole-body rotations, including the precuneus and tempero-parietal junction.
Abstract: The body schema is a key component in accomplishing egocentric mental transformations, which rely on bodily reference frames. These reference frames are based on a plurality of different cognitive and sensory cues among which the vestibular system plays a prominent role. We investigated whether a bottom-up influence of vestibular stimulation modulates the ability to perform egocentric mental transformations. Participants were significantly faster to make correct spatial judgments during vestibular stimulation as compared to sham stimulation. Interestingly, no such effects were found for mental transformation of hand stimuli or during mental transformations of letters, thus showing a selective influence of vestibular stimulation on the rotation of whole-body reference frames. Furthermore, we found an interaction with the angle of rotation and vestibular stimulation demonstrating an increase in facilitation during mental body rotations in a direction congruent with rightward vestibular afferents. We propose that facilitation reflects a convergence in shared brain areas that process bottom-up vestibular signals and top-down imagined whole-body rotations, including the precuneus and tempero-parietal junction. Ultimately, our results show that vestibular information can influence higher-order cognitive processes, such as the body schema and mental imagery.
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TL;DR: A new pathway is hypothesized via the basal ganglia, potentially involved in spatial learning and spatial memory, from the anatomical network of vestibular cognition.
Abstract: Recent discoveries have emphasized the role of the vestibular system in cognitive processes such as memory, spatial navigation and bodily self-consciousness. A precise understanding of the vestibular pathways involved is essential to understand the consequences of vestibular diseases for cognition, as well as develop therapeutic strategies to facilitate recovery. The knowledge of the “vestibular cortical projections areas”, defined as the cortical areas activated by vestibular stimulation, has dramatically increased over the last several years from both anatomical and functional points of view. Four major pathways have been hypothesized to transmit vestibular information to the vestibular cortex: 1) the vestibulo-thalamo-cortical pathway, which probably transmits spatial information about the environment via the parietal, entorhinal and perirhinal cortices to the hippocampus and is associated with spatial representation and self-versus object motion distinctions; 2) the pathway from the dorsal tegmental nucleus via the lateral mammillary nucleus, the anterodorsal nucleus of the thalamus to the entorhinal cortex, which transmits information for estimations of the head direction; 3) the pathway via the nucleus reticularis pontis oralis, the supramammillary nucleus and the medial septum to the hippocampus, which transmits information supporting hippocampal theta rhythm and memory; and 4) a possible pathway via the cerebellum, and the ventral lateral nucleus of the thalamus (perhaps to the parietal cortex), which transmits information for spatial learning. Finally a new pathway is hypothesized via the basal ganglia, potentially involved in spatial learning and spatial memory. From these pathways, progressively emerges the anatomical network of vestibular cognition.
241 citations
Cites background from "Balancing the Mind Vestibular Induc..."
...In humans, the temporoparietal junction could also integrate vestibular input involved in mental rotation tasks in an egocentric reference frame (Falconer and Mast, 2012)....
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TL;DR: The current literature is reviewed, possible causal links between vestibular dysfunction and cognitive performance are discussed, and areas of future research are suggested.
Abstract: A growing body of literature suggests the inner ear vestibular system has a substantial impact on cognitive function. The strongest evidence exists in connecting vestibular function to the cognitive domain of visuospatial ability, which includes spatial memory, navigation, mental rotation, and mental representation of three-dimensional space. Substantial evidence also exists suggesting the vestibular system has an impact on attention and cognitive processing ability. The cognitive domains of memory and executive function are also implicated in a number of studies. We will review the current literature, discuss possible causal links between vestibular dysfunction and cognitive performance, and suggest areas of future research.
197 citations
Cites background from "Balancing the Mind Vestibular Induc..."
...But a study by Mast et al. in 2006 with fewer participants found CVS did not change performance on low-imagery cognitive tasks (deciding if a statement was true or false) and, contrary to the previous studies, CVS worsened performance on high imagery tasks (mental rotation, memory of an image)....
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...Two studies found improvements in visuospatial ability (mental rotation, spatial memory) in response to unilateral CVS [9,47], while another found no effect on a quantitative visual-imagery recognition task [4]....
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...In caloric vestibular stimulation (CVS) cold and/or warm water is infused into the external auditory canal; the change in temperature leads to a change in density and subsequent motion of the endolymphatic fluid of the horizontal semicircular canal, leading to perceived head motion in the plane of the canal and nystagmus [14]....
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...Despite the use of sham and control stimulations, it is also possible that the cognitive changes seen in GVS and CVS are due to some other effect of the stimulation, such as the sensations produced by electrical current or temperature changes....
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...These authors suggested the changes (both improvement and impairments) in cognitive performance could be explained by changes in cerebral blood flow that has been seen in functional imaging during CVS, but the changes seen in func- tional brain imaging are not entirely consistent across studies and could be used to justify either conclusion [9,15,22,90,126,143]....
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TL;DR: The evidence that vestibular loss causes cognitive disorders, especially spatial memory deficits, in animals and humans is summarized and the evidence that these deficits are not due to hearing loss, problems with motor control, oscillopsia or anxiety and depression is critically evaluated.
Abstract: In addition to the deficits in the vestibulo-ocular and vestibulo-spinal reflexes that occur following vestibular dysfunction, there is substantial evidence that vestibular loss also causes cognitive disorders, some of which may be due to the reflexive deficits and some of which are related to the role that ascending vestibular pathways to the limbic system and cortex play in spatial orientation. In this review we summarise the evidence that vestibular loss causes cognitive disorders, especially spatial memory deficits, in animals and humans and critically evaluate the evidence that these deficits are not due to hearing loss, problems with motor control, oscillopsia or anxiety and depression. We review the evidence that vestibular lesions affect head direction and place cells as well as the emerging evidence that artificial activation of the vestibular system, using galvanic vestibular stimulation, can modulate cognitive function.
110 citations
Cites background from "Balancing the Mind Vestibular Induc..."
...Falconer and Mast (2012) have recently reported that CVS can enhance performance in an egocentric transformation task....
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TL;DR: Three emerging streams of research in vestibular science are—at least in part—associated with different neuronal core mechanisms: spatial transformations draw on parietal areas, body representation is associated with somatosensory areas, and affective processes involve insular and cingulate cortices, all of which receive Vestibular input.
Abstract: A growing number of studies in humans demonstrate the involvement of vestibular information in tasks that are seemingly remote from well-known functions such as space constancy or postural control. In this review article we point out three emerging streams of research highlighting the importance of vestibular input: (1) Spatial Cognition: Modulation of vestibular signals can induce specific changes in spatial cognitive tasks like mental imagery and the processing of numbers. This has been shown in studies manipulating body orientation (changing the input from the otoliths), body rotation (changing the input from the semicircular canals), in clinical findings with vestibular patients, and in studies carried out in microgravity. There is also an effect in the reverse direction; top-down processes can affect perception of vestibular stimuli. (2) Body Representation: Numerous studies demonstrate that vestibular stimulation changes the representation of body parts, and sensitivity to tactile input or pain. Thus, the vestibular system plays an integral role in multisensory coordination of body representation. (3) Affective Processes and Disorders: Studies in psychiatric patients and patients with a vestibular disorder report a high comorbidity of vestibular dysfunctions and psychiatric symptoms. Recent studies investigated the beneficial effect of vestibular stimulation on psychiatric disorders, and how vestibular input can change mood and affect. These three emerging streams of research in vestibular science are—at least in part—associated with different neuronal core mechanisms. Spatial transformations draw on parietal areas, body representation is associated with somatosensory areas, and affective processes involve insular and cingulate cortices, all of which receive vestibular input. Even though a wide range of different vestibular cortical projection areas has been ascertained, their functionality still is scarcely understood.
104 citations
Cites background from "Balancing the Mind Vestibular Induc..."
...Congruent motion can facilitate mental rotation of one’s own body (Falconer and Mast, 2012; van Elk and Blanke, 2013) while absent or disturbed vestibular input can impair it (Grabherr et al., 2007; Lenggenhager et al., 2008)....
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...It is important to point out that some studies provide evidence that vestibular input influences performance in mental rotation tasks only then when the task involves a representation of one’s own body or perspective (Lenggenhager et al., 2008; Dilda et al., 2012; Falconer and Mast, 2012)....
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...…been investigated through own-body rotation (van Elk and Blanke, 2013), changing the input from the semicircular canals by CVS (Mast et al., 2006; Falconer and Mast, 2012), changing the input of the vestibular nerve by GVS (Lenggenhager et al., 2008; Dilda et al., 2012), microgravity studies…...
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TL;DR: It is proposed that the core of the human vestibular cortex consists of at least two separate areas, which are referred to together as PIVC and PIC and there are parallels to the proposed organization in humans.
Abstract: Here, we review the structure and function of a core region in the vestibular cortex of humans that is located in the midposterior Sylvian fissure and referred to as the parieto-insular vestibular ...
84 citations
References
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TL;DR: Related perceptual, motor, and cognitive performances were examined to reveal the accuracy of the properties of action spontaneously represented when mentally simulating moving one's hand, and suggest that sensorimotor structures support mental simulations of actions.
Abstract: Related perceptual, motor, and cognitive performances were examined to reveal the accuracy of the properties of action spontaneously represented when mentally simulating moving one's hand. The kinematic configuration of the body represented and transformed in mental simulations was not fixed or canonical but corresponded to one's current configuration. Mental simulation time mimicked movement time for natural efficient movement from a posture midway between each of the hand's joint limits into many other postures. Equal time was required for simulated and real movements into more common, comfortable postures; shorter but proportional time was required for simulated movement than real movement into less common postures that involved longer trajectories, coordinated activity at more joints, motion near extremes of joint limits, and uncomfortable kinesthetic sensations. The findings suggest that sensorimotor structures support mental simulations of actions.
668 citations
TL;DR: Converging evidence from animal and human studies suggests that the primate brain constructs various body-part-centred representations of space, based on the integration of visual, tactile and proprioceptive information.
545 citations
TL;DR: It is suggested that the temporoparietal junction is a crucial structure for the conscious experience of the normal self, mediating spatial unity of self and body, and also suggest that impaired processing at the TPJ may lead to pathological selves such as OBEs.
Abstract: The spatial unity of self and body is challenged by various philosophical considerations and several phenomena, perhaps most notoriously the "out-of-body experience" (OBE) during which one's visual perspective and one's self are experienced to have departed from their habitual position within one's body. Although researchers started examining isolated aspects of the self, the neurocognitive processes of OBEs have not been investigated experimentally to further our understanding of the self. With the use of evoked potential mapping, we show the selective activation of the temporoparietal junction (TPJ) at 330-400 ms after stimulus onset when healthy volunteers imagined themselves in the position and visual perspective that generally are reported by people experiencing spontaneous OBEs. Interference with the TPJ by transcranial magnetic stimulation (TMS) at this time impaired mental transformation of one's own body in healthy volunteers relative to TMS over a control site. No such TMS effect was observed for imagined spatial transformations of external objects, suggesting the selective implication of the TPJ in mental imagery of one's own body. Finally, in an epileptic patient with OBEs originating from the TPJ, we show partial activation of the seizure focus during mental transformations of her body and visual perspective mimicking her OBE perceptions. These results suggest that the TPJ is a crucial structure for the conscious experience of the normal self, mediating spatial unity of self and body, and also suggest that impaired processing at the TPJ may lead to pathological selves such as OBEs.
506 citations
TL;DR: This PET study showed for the first time that cortical and subcortical activation by vestibular caloric stimulation depends on the handedness of the subjects and on the side of the stimulated ear.
Abstract: The aim of this (15)O-labelled H(2)O bolus positron emission tomography (PET) study was to analyse the hemispheric dominance of the vestibular cortical system. Therefore, the differential effects of caloric vestibular stimulation (right or left ear irrigation with warm water at 44 degrees C) on cortical and subcortical activation were studied in 12 right-handed and 12 left-handed healthy volunteers. Caloric irrigation induces a direction-specific sensation of rotation and nystagmus. Significant regional cerebral blood flow increases were found in a network within both hemispheres, including the superior frontal gyrus/sulcus, the precentral gyrus and the inferior parietal lobule with the supramarginal gyrus. These areas correspond best to the cortical ocular motor centres, namely the prefrontal cortex, the frontal eye field and the parietal eye field, known to be involved in the processing of caloric nystagmus. Furthermore, distinct temporo-parietal activations could be separated in the posterior part of the insula with the adjacent superior temporal gyrus, the inferior parietal lobule and precuneus. These areas fit best to the human homologues of multisensory vestibular cortex areas identified in the monkey and correspond to the parieto-insular vestibular cortex (PIVC), the visual temporal sylvian area (VTS) and areas 7 and 6. Further cortical activations were seen in the anterior insula, the inferior frontal gyrus and anterior cingulum. The subcortical activation pattern in the putamen, thalamus and midbrain is consistent with the organization of efferent ocular motor pathways. Cortical and subcortical activation of the described areas was bilateral during monaural stimulation, but predominant in the hemisphere ipsilateral to the stimulated ear and exhibited a significant right hemispheric dominance for vestibular and ocular motor structures in right-handed volunteers. Similarly, a significant left hemispheric dominance was found in the 12 left-handed volunteers. Thus, this PET study showed for the first time that cortical and subcortical activation by vestibular caloric stimulation depends (i) on the handedness of the subjects and (ii) on the side of the stimulated ear. Maximum activation was therefore found when the non-dominant hemisphere was ipsilateral to the stimulated ear, i.e. in the right hemisphere of right-handed subjects during caloric irrigation of the right ear and in the left hemisphere of left-handed subjects during caloric irrigation of the left ear. The localization of handedness and vestibular dominance in opposite hemispheres might conceivably indicate that the vestibular system and its hemispheric dominance, which matures earlier during ontogenesis, determine right- or left-handedness.
477 citations
"Balancing the Mind Vestibular Induc..." refers background in this paper
..., 2005; Tsakiris, Costantini, & Haggard, 2008), and is activated by CVS (Dieterich et al., 2003; Fasold et al., 2002; Indovina et al., 2005)....
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..., 2007) and rightward self-motion information from the vestibular system (Dieterich et al., 2003; Fasold et al., 2002; Indovina et al., 2005; Marcelli et al., 2009; Suzuki et al., 2001; Vitte et al., 1996): The temporo-parietal junction has been implicated in egocentric mental transformation tasks (Blanke et al....
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TL;DR: The widespread Vestibular projections to the multimodal human PIVC, somatosensory cortex, area MST, intraparietal sulcus and hippocampus explain the large influence of vestibular signals on self-motion perception, spatial navigation, internal models of gravity, one's body perception and bodily self-consciousness.
455 citations