Hippocampal spatial representations require vestibular input

Stackman, Robert W.; Clark, Ann S.; Taube, Jeffrey S.

doi:10.1002/hipo.1112

Cited by 342 publications

(275 citation statements)

References 84 publications

(100 reference statements)

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“…Although diminished vestibular cues during random foraging in VR might account for reduced spatial selectivity compared to during random foraging in RW, it is inconsistent with the presence of spatial selectivity in the systematic-pillar tasks, in which the nature of paths and resulting vestibular cues are similar to those in the random-pillar task. Further, vestibular lesions caused substantial behavioral deficits, reductions in theta power and unaltered peak firing rates 15,46 , all of which are in contrast to our data. These results suggest that the repeated pairing of cues, or lack thereof, is the key reason for the difference in two-dimensional spatial selectivity.…”

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confidence: 99%

“…However, the activity of place cells is also influenced by other sensory and motor cues, including specific and nonspecific proximal cues, such as olfactory and somatosensory cues [4][5][6][7][8][9][10] , and locomotion cues such as optic flow and proprioception, which together with vestibular cues are thought to provide self-motion information for path integration [11][12][13] . 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 .…”

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confidence: 85%

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

et al. 2014

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“…Vestibular inputs are necessary for path integration [58][59][60][61]. Passive rotation has been shown to modulate the activity of place cells [62,63] while bilateral vestibular inactivation or damage abolished location-specific firing of place cells [64,65]. We suggest here that vestibular stimulation enhanced hippocampal LTP, which may be necessary for the formation of place fields [66][67][68].…”

Section: Vestibular Stimulation Enhances Ltpmentioning

confidence: 83%

Vestibular stimulation enhances hippocampal long-term potentiation via activation of cholinergic septohippocampal cells

Tai

Leung

2012

Behavioural Brain Research

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“…There is ample evidence to suggest that the head direction system contributes to the maintenance of the place code. Perhaps most compellingly, disruption of the vestibular sense disrupts the head direction system and also has a profound effect on the hippocampal place code (Russell, Horii, Smith, Darlington, & Bilkey, 2003;Stackman, Clark, & Taube, 2002).…”

Section: Mechanisms Of Contextual Evolution In Ecmentioning

confidence: 99%

The Temporal Context Model in Spatial Navigation and Relational Learning: Toward a Common Explanation of Medial Temporal Lobe Function Across Domains.

Howard¹,

Fotedar²,

Datey³

et al. 2005

Psychological Review

271

334

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The medial temporal lobe (MTL) has been studied extensively at all levels of analysis, yet its function remains unclear. Theory regarding the cognitive function of the MTL has centered along 3 themes. Different authors have emphasized the role of the MTL in episodic recall, spatial navigation, or relational memory. Starting with the temporal context model (M. W. Howard and M. J. , a distributed memory model that has been applied to benchmark data from episodic recall tasks, the authors propose that the entorhinal cortex supports a gradually changing representation of temporal context and the hippocampus proper enables retrieval of these contextual states. Simulation studies show this hypothesis explains the firing of place cells in the entorhinal cortex and the behavioral effects of hippocampal lesion in relational memory tasks. These results constitute a first step towards a unified computational theory of MTL function that integrates neurophysiological, neuropsychological and cognitive findings.The medial temporal lobe (MTL) is a region that includes the hippocampus proper, the subicular complex and parahippocampal cortical regions, including entorhinal, perirhinal, and parahippocampal/postrhinal cortices. A great deal of data from neuropsychology (e.g. Eichenbaum & Cohen, 2001;Scoville & Milner, 1957;Squire, 1992) and functional imaging (e.g. Fernandez, Effern, Grunwald, et al., 1999;Stern, Corkin, Gonzalez, et al., 1996;Wagner et al., 1998) has converged on the idea that the MTL is important in learning and memory. In order to bridge the gap between cognition and cellular-level physiology, we need a mechanistic, mesoscopic description of MTL computational function. We already have several successful verbally-formulated theories of the cognitive function of the MTL. These are described in turn in the following subsections. This paper will attempt to draw these multiple verbal theories together into a single computational framework that is consistent with known neurophysiological and neuroanatomical data.

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Hippocampal spatial representations require vestibular input

Cited by 342 publications

References 84 publications

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

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

Vestibular stimulation enhances hippocampal long-term potentiation via activation of cholinergic septohippocampal cells

The Temporal Context Model in Spatial Navigation and Relational Learning: Toward a Common Explanation of Medial Temporal Lobe Function Across Domains.

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