The vestibular contribution to the head direction signal and navigation

Yoder, Ryan M.; Taube, Jeffrey S.

doi:10.3389/fnint.2014.00032

Cited by 130 publications

(108 citation statements)

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“…The mechanism by which vestibular dysfunction is associated with cognitive dysfunction is unclear, although several potential pathways have been hypothesized. Loss of peripheral vestibular input may lead to atrophy of areas within the cortical vestibular network, including the “head direction cells” within the thalamus, subiculum, and entorhinal cortex; the temporoparietal junction; and the part of the hippocampus that contains “place cells.” Substantial convergence with visual streams of information occurs in these cortical sites, specifically in the hippocampus and medial superior temporal area . A study of 10 individuals with bilateral vestibular failure found that they developed significant hippocampal atrophy and associated impairments in visuospatial tasks such as navigation in a virtual maze .…”

Section: Discussionmentioning

confidence: 99%

“…Increasing evidence demonstrates important connections between the vestibular system and various domains of cognitive function, most notably visuospatial ability, but also memory, executive function, and attention . Studies in animals and individuals with unilateral or bilateral vestibular loss suggest that the vestibular system provides critical information about spatial orientation, spatial memory, and spatial navigation …”

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confidence: 99%

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Association Between Visuospatial Ability and Vestibular Function in the Baltimore Longitudinal Study of Aging

Bigelow

Semenov

Treviño

et al. 2015

J American Geriatrics Society

102

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OBJECTIVES To investigate the relationship between vestibular loss associated with aging and age-related decline in visuospatial function. DESIGN Cross-sectional analysis within a prospective cohort study. SETTING Baltimore Longitudinal Study of Aging (BLSA). PARTICIPANTS Community-dwelling BLSA participants with a mean age of 72 (range 26–91) (N = 183). MEASUREMENTS Vestibular function was measured using vestibular-evoked myogenic potentials. Visuospatial cognitive tests included Card Rotations, Purdue Pegboard, Benton Visual Retention Test, and Trail-Making Test Parts A and B. Tests of executive function, memory, and attention were also considered. RESULTS Participants underwent vestibular and cognitive function testing. In multiple linear regression analyses, poorer vestibular function was associated with poorer performance on Card Rotations (P = .001), Purdue Pegboard (P = .005), Benton Visual Retention Test (P = 0.008), and Trail-Making Test Part B (P = .04). Performance on tests of executive function and verbal memory were not significantly associated with vestibular function. Exploratory factor analyses in a subgroup of participants who underwent all cognitive tests identified three latent cognitive abilities: visuospatial ability, verbal memory, and working memory and attention. Vestibular loss was significantly associated with lower visuospatial and working memory and attention factor scores. CONCLUSION Significant consistent associations between vestibular function and tests of visuospatial ability were observed in a sample of community-dwelling adults. Impairment in visuospatial skills is often one of the first signs of dementia and Alzheimer’s disease. Further longitudinal studies are needed to evaluate whether the relationship between vestibular function and visuospatial ability is causal.

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

Association Between Visuospatial Ability and Vestibular Function in the Baltimore Longitudinal Study of Aging

Bigelow

Semenov

Treviño

et al. 2015

J American Geriatrics Society

102

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“…The otolith organs also contribute to head direction cell function, but this contribution appears to be relatively less than that of the canals; otoconia-deficient mice have head direction cells that are directionally tuned, but this tuning degrades over time [22]. Nevertheless, the degraded head direction signal of otoconia-deficient mice is paralleled by deficits in the performance of directional navigation tasks such as the radial arm maze, food-carrying (homing) task, and Y-maze alternation [4, 23, 24] for review, see [25]. However, otoconia-deficient mice were able to accurately perceive the goal location during the probe trial on a Barnes maze, suggesting place recognition was intact [23].…”

Section: Introductionmentioning

confidence: 99%

Otolith dysfunction alters exploratory movement in mice

Blankenship

Cherep

Donaldson

et al. 2017

Behavioural Brain Research

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The organization of rodent exploratory behavior appears to depend on self-movement cue processing. As of yet, however, no studies have directly examined the vestibular system’s contribution to the organization of exploratory movement. The current study sequentially segmented open field behavior into progressions and stops in order to characterize differences in movement organization between control and otoconia-deficient tilted mice under conditions with and without access to visual cues. Under completely dark conditions, tilted mice exhibited similar distance traveled and stop times overall, but had significantly more circuitous progressions, larger changes in heading between progressions, and less stable clustering of home bases, relative to control mice. In light conditions, control and tilted mice were similar on all measures except for the change in heading between progressions. This pattern of results is consistent with otoconia-deficient tilted mice using visual cues to compensate for impaired self-movement cue processing. This work provides the first empirical evidence that signals from the otolithic organs mediate the organization of exploratory behavior, based on a novel assessment of spatial orientation.

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“…Under normal conditions, the HD signal is primarily controlled by visual landmark information (Goodridge and Taube, 1995;Goodridge et al, 1998; Yoder et al, 2011), but several studies have also shown the importance of idiothetic information (vestibular, motor, and proprioceptive cues;Taube et al, 1990b; Taube and Burton, 1995;Goodridge et al, 1998;Stackman et al, 2003;van der Meer et al, 2010;Valerio and Taube, 2012).…”

Section: Introductionmentioning

confidence: 99%

Head Direction Cell Activity Is Absent in Mice without the Horizontal Semicircular Canals

Valério

Taube

2016

J. Neurosci.

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Head direction (HD) cells fire when an animal faces a particular direction in its environment, and they are thought to represent the neural correlate of the animal's perceived spatial orientation. Previous studies have shown that vestibular information is critical for generating the HD signal but have not delineated whether information from all three semicircular canals or just the horizontal canals, which are primarily sensitive to angular head rotation in the horizontal (yaw) plane, are critical for the signal. Here, we monitored cell activity in the anterodorsal thalamus (ADN), an area known to contain HD cells, in epstatic circler (Ecl) mice, which have a bilateral malformation of the horizontal (lateral) semicircular canals. Ecl mice and their littermates that did not express the mutation (controls) were implanted with recording electrodes in the ADN. Results confirm the important role the horizontal canals play in forming the HD signal. Although normal HD cell activity (Raleigh's r Ͼ 0.4) was recorded in control mice, no such activity was found in Ecl mice, although some cells had activity that was mildly modulated by HD (0.4 Ͼ r Ͼ 0.2). Importantly, we also observed activity in Ecl mice that was best characterized as bursty-a pattern of activity similar to an HD signal but without any preferred firing direction. These results suggest that the neural structure for the HD network remains intact in Ecl mice, but the absence of normal horizontal canals results in an inability to control the network properly and brings about an unstable HD signal. Key words: anterior thalamus; navigation; orientation; place cell; spatial; vestibular IntroductionHead direction (HD) cells, first discovered in the postsubiculum (Ranck, 1984;Taube et al., 1990a), discharge when an animal is facing a specific direction, independent of its location and behavior in space. Under normal conditions, the HD signal is primarily controlled by visual landmark information (Goodridge and Taube, 1995;Goodridge et al., 1998; Yoder et al., 2011), but several studies have also shown the importance of idiothetic information (vestibular, motor, and proprioceptive cues;Taube et al., 1990b; Taube and Burton, 1995;Goodridge et al., 1998;Stackman et al., 2003;van der Meer et al., 2010;Valerio and Taube, 2012).The influence of the vestibular system on HD cell firing has been a focus of many studies (Taube et al., 1990b; McNaughton et al., 1991). Indeed, the information coded by the horizontal semicircular canals (the acceleration of rotational head movements) makes it an ideal candidate for providing information about the animal's head movements in the yaw plane. Furthermore, the anatomical projections from the vestibular nuclei to the HD network via the nucleus prepositus hypoglosis, supragenual nucleus, and dorsal tegmental nucleus (DTN) reinforced this hypothesis (Biazoli et al., 2006 Sept. 9, 2014; revised Oct. 23, 2015; accepted Nov. 16, 2015. Author contributions: S.V. and J.S.T. designed research; S.V. performed research; S.V. and J.S.T. ana...

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The vestibular contribution to the head direction signal and navigation

Cited by 130 publications

References 128 publications

Association Between Visuospatial Ability and Vestibular Function in the Baltimore Longitudinal Study of Aging

Association Between Visuospatial Ability and Vestibular Function in the Baltimore Longitudinal Study of Aging

Otolith dysfunction alters exploratory movement in mice

Head Direction Cell Activity Is Absent in Mice without the Horizontal Semicircular Canals

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