Lesions of the Vestibular System Disrupt Hippocampal Theta Rhythm in the Rat

Russell, Noah A.; Horii, Arata; Smith, Paul F.; Darlington, Cynthia L.; Bilkey, David K.

doi:10.1152/jn.00953.2005

Cited by 112 publications

(116 citation statements)

References 83 publications

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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.…”

Section: Discussioncontrasting

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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Section: Discussioncontrasting

confidence: 99%

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

et al. 2014

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“…The results are unlikely to arise solely due to diminished vestibular inputs in VR because vestibular lesions caused significant behavioral deficits, reduction in theta power and unaltered peak firing rates 15,26 , all of which are in contrast to our data.…”

contrasting

confidence: 99%

“…This is also consistent with the observation that maze-cleaning between sessions induced place field instability and remapping 12 . The results are unlikely to arise solely due to diminished vestibular inputs in VR because vestibular lesions caused significant behavioral deficits, reduction in theta power and unaltered peak firing rates 15,26 , all of which are in contrast to our data.…”

contrasting

confidence: 99%

Hippocampal motifs

Aghajan¹,

Acharya²,

Cushman³

et al. 2013

Preprint

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Dorsal Hippocampal neurons provide an allocentric map of space 1, characterized by three key properties. First, their firing is spatially selective 1-3 , termed a rate code. Second, as animals traverse through place fields, neurons sustain elevated firing rates for long periods, however this has received little attention. Third the theta-phase of spikes within this sustained activity varies with animal's location, termed phase-precession or a temporal code [4][5][6][7][8][9][10] . The precise relationship between these properties and the mechanisms governing them are not understood, although distal visual cues (DVC) are thought to be sufficient to reliably elicit them 2,3 . Hence, we measured rat CA1 neurons' activity during random foraging in two-dimensional VR-where only DVC provide consistent allocentric location information-and compared it with their activity in real world (RW). Surprisingly, we found little spatial selectivity in VR. This is in sharp contrast to robust spatial selectivity commonly seen in one-dimensional RW and VR [7][8][9][10][11] , or two-dimensional RW [1][2][3] . Despite this, neurons in VR generated approximately two-second long phase precessing spike sequences, termed "hippocampal motifs". Motifs, and "Motif-fields", an aggregation of all motifs of a neuron, had qualitatively similar properties including theta-scale temporal coding in RW and VR, but the motifs were far less spatially localized in VR. These results suggest that intrinsic, network mechanisms generate temporally coded hippocampal motifs, which can be dissociated from their spatial selectivity. Further, DVC alone are insufficient to localize motifs spatially to generate a robust rate code.When an animal explores a two-dimensional environment, hippocampal neurons fire in a spatially selective fashion to form an allocentric map of space 1 . The mechanisms governing this selectivity remain to be understood. DVC are thought to be the primary factor governing hippocampal spatial selectivity 2,3 , although the contribution of other modalities have not been ruled out 12,13 . While these uncontrolled cues are difficult to eliminate in RW, they can be either removed or made spatially non-informative in VR. Hence, rodent hippocampal activity has been recently measured on one-dimensional mazes where neurons show comparable spatial selectivity in RW and VR [7][8][9]11 . Spatial selectivity on one-dimensional All rights reserved. No reuse allowed without permission.(which was not peer-reviewed) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.The copyright holder for this preprint . http://dx.doi.org/10.1101/001636 doi: bioRxiv preprint first posted online Dec. 31, 2013; 2 VR tracks could arise not only from DVC 2,3 , but also from self-motion cues 9,14,15 or intrinsic network mechanisms 9,16-19 because these are highly correlated with spatial location. To unequivocally determine the contribution of only DVC it is necessary to measure hippocampal activity in a two-dimensional VR where ra...

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“…Co-recorded theta-modulated firing in the thalamus (quantified by analyzing theta-related spike autocorrelograms) also was not affected by the optogeneticinduced instability (Table S2). This finding further indicates that the experimental manipulation was specific to the inputs to the HD network and not to the vestibular system in general, since vestibular system lesions lead to reduced power and frequency in the hippocampal theta rhythm without affecting the relationship between firing rate and linear velocity [32].…”

Section: Locomotion Is Not Affected By Disruption Of the Nph → Dtn Pamentioning

confidence: 82%

The Head-Direction Signal Plays a Functional Role as a Neural Compass during Navigation

Butler¹,

Smith²,

Meer³

et al. 2017

Current Biology

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SUMMARYThe rat limbic system contains head direction (HD) cells that fire according to heading in the horizontal plane, and these cells are thought to provide animals with an internal compass. Previous work has found that HD cell tuning correlates with behavior on navigational tasks, but a direct, causal link between HD cells and navigation has not been demonstrated. Here, we show that pathway-specific optogenetic inhibition of the nucleus prepositus caused HD cells to become directionally unstable under dark conditions without affecting the animals' locomotion. Then, using the same technique, we found that this decoupling of the HD signal in the absence of visual cues caused the animals to make directional homing errors, and that the magnitude and direction of these errors were in a range that corresponded to the degree of instability observed in the HD signal. These results provide evidence that the HD signal plays a causal role as a neural compass in navigation.

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Lesions of the Vestibular System Disrupt Hippocampal Theta Rhythm in the Rat

Cited by 112 publications

References 83 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

Hippocampal motifs

The Head-Direction Signal Plays a Functional Role as a Neural Compass during Navigation

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