Contribution of multiple sensory information to place field stability in hippocampal place cells

Save, Étienne; Nerad, Luděk; Poucet, Bruno

doi:10.1002/(sici)1098-1063(2000)10:1<64::aid-hipo7>3.0.co;2-y

Cited by 183 publications

(84 citation statements)

References 39 publications

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“…The repeated pairing model is compatible with many findings, including place cell remapping after a change in the relationship between locomotion cues and distal visual cues 12 , altered spatial selectivity after changes in distal 3,6 or proximal cues [4][5][6][7][8][9] and instability of place fields after maze cleaning between sessions 7 . In each of these cases, place cells remap but spatial selectivity remains intact, presumably because new associations are formed as cues are paired repeatedly in new configurations.…”

Section: Discussionsupporting

confidence: 81%

“…Distal visual cues are thought to reliably determine this spatial selectivity because changing or rotating them causes corresponding large changes in the spatial tuning of place cells 2,3 . 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 .…”

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confidence: 99%

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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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Section: Discussionsupporting

confidence: 81%

mentioning

confidence: 99%

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

et al. 2014

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“…This assumption is supported by the recording data of Hafting et al (2005) showing that entorhinal grid cells exhibit stable firing patterns from the outset of exploration in complete darkness for as long as 20 min. Such a remarkable stability of firing suggests that even in the absence of visual input, firing grids of entorhinal cells are fixed to the environment, possibly by using other sources of external input (Maaswinkel & Whishaw, 1999;Save, Nerad, & Poucet, 2000) in combination with a particular exploration strategy (Whishaw, Hines, & Wallace, 2001). It was shown previously that suitable exploration strategies involving return to previously visited places lead to a stable learning of the connections from view to place cells even in the presence of a noisy path integrator (Arleo & Gerstner, 2000).…”

Section: Simulation 1: Deformation Of Place Fields and Rescaling Of Gmentioning

confidence: 99%

Is there a geometric module for spatial orientation? Insights from a rodent navigation model.

Sheynikhovich¹,

Chavarriaga²,

Strösslin³

et al. 2009

Psychological Review

104

145

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Modern psychological theories of spatial cognition postulate the existence of a geometric module for reorientation. This concept is derived from experimental data showing that in rectangular arenas with distinct landmarks in the corners, disoriented rats often make diagonal errors, suggesting their preference for the geometric (arena shape) over the nongeometric (landmarks) cues. Moreover, sensitivity of hippocampal cell firing to changes in the environment layout was taken in support of the geometric module hypothesis. Using a computational model of rat navigation, the authors proposed and tested the alternative hypothesis that the influence of spatial geometry on both behavioral and neuronal levels can be explained by the properties of visual features that constitute local views of the environment. Their modeling results suggest that the pattern of diagonal errors observed in reorientation tasks can be understood by the analysis of sensory information processing that underlies the navigation strategy employed to solve the task. In particular, 2 navigation strategies were considered: (a) a place-based locale strategy that relies on a model of grid and place cells and (b) a stimulus-response taxon strategy that involves direct association of local views with action choices. The authors showed that the application of the 2 strategies in the reorientation tasks results in different patterns of diagonal errors, consistent with behavioral data. These results argue against the geometric module hypothesis by providing a simpler and biologically more plausible explanation for the related experimental data. Moreover, the same model also describes behavioral results in different types of water-maze tasks.

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“…homing). In this case no external cues are available and place cell activity depends only on PI [5]. Finally, behavioural experiments with rodents indicate that PI can be recalibrated using visual information [4].…”

Section: Introductionmentioning

confidence: 99%

Modelling Path Integrator Recalibration Using Hippocampal Place Cells

Strösslin

Chavarriaga

Sheynikhovich

et al. 2005

Artificial Neural Networks: Biological Inspirations – ICANN 2005

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Abstract. The firing activities of place cells in the rat hippocampus exhibit strong correlations to the animal's location. External (e.g. visual) as well as internal (proprioceptive and vestibular) sensory information take part in controlling hippocampal place fields. Previously it has been observed that when rats shuttle between a movable origin and a fixed target the hippocampus encodes position in two different frames of reference. This paper presents a new model of hippocampal place cells that explains place coding in multiple reference frames by continuous interaction between visual and self-motion information. The model is tested using a simulated mobile robot in a real-world experimental paradigm.

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Contribution of multiple sensory information to place field stability in hippocampal place cells

Cited by 183 publications

References 39 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

Is there a geometric module for spatial orientation? Insights from a rodent navigation model.

Modelling Path Integrator Recalibration Using Hippocampal Place Cells

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