Geometric Cues Influence Head Direction Cells Only Weakly in Nondisoriented Rats

Knight, Rebecca; Hayman, Robin; Ginzberg, Lin Lin; Jeffery, Kate J.

doi:10.1523/jneurosci.2257-11.2011

Cited by 38 publications

(36 citation statements)

References 31 publications

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“…HD cells are located in a number of regions that interact, directly or indirectly, with the hippocampus, including the medial entorhinal cortex [45], retrosplenial cortex [46], postsubiculum [47], and anterodorsal thalamic nuclei [48]. The preferred directions of HD cells are typically found to be strongly coupled to the alignment of the hippocampal map [32], and spatial geometry is thought to play an important role in determining these preferred directions under disoriented conditions [38,39]. Thus, the hippocampal map may be oriented by HD input in a bottom-up manner [37,49].…”

Section: Discussionmentioning

confidence: 99%

“…Previous studies examining place cell responses in chambers containing nongeometric cues but without orienting geometry have yielded conflicting results, with some findings suggesting that the hippocampal map is unstable following disorientation [32], and others suggesting that this map is stable and can be oriented by nongeometric cues [33]. Related work examining head direction (HD) cells, whose activity correlates with the alignment of the hippocampal map under oriented conditions, has yielded similar discrepancies in disoriented animals [32,34–37], though some studies suggest a privileged role for spatial geometry [38,39]. Thus, whether the hippocampal map is oriented by geometry following disorientation, and whether this map relates to reorientation behavior, remains unresolved.…”

Section: Introductionmentioning

confidence: 99%

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Environmental Geometry Aligns the Hippocampal Map during Spatial Reorientation

et al. 2017

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Summary When a navigator's internal sense of direction is disrupted, she must rely on external cues to regain her bearings, a process termed spatial reorientation. Extensive research has demonstrated that the geometric shape of the environment exerts powerful control over reorientation behavior, but the neural and cognitive mechanisms underlying this phenomenon are not well understood. Whereas some theories claim that geometry controls behavior through an allocentric mechanism potentially tied to the hippocampus, others postulate that disoriented navigators reach their goals by using an egocentric view-matching strategy. To resolve this debate, we characterized hippocampal representations during reorientation. We first recorded from CA1 cells as disoriented mice foraged in chambers of various shapes. We found that the alignment of the recovered hippocampal map was determined by the geometry of the chamber, but not by nongeometric cues, even when these cues could be used to disambiguate geometric ambiguities. We then recorded hippocampal activity as disoriented mice performed a classical goal-directed spatial memory task in a rectangular chamber. Again, we found that the recovered hippocampal map aligned solely to the chamber geometry. Critically, we also found a strong correspondence between the hippocampal map alignment and the animal's behavior, making it possible to predict the search location of the animal from neural responses on a trial-by-trial basis. Together, these results demonstrate that spatial reorientation involves the alignment of the hippocampal map to local geometry. We hypothesize that geometry may be an especially salient cue for reorientation because it is an inherently stable aspect of the environment.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Environmental Geometry Aligns the Hippocampal Map during Spatial Reorientation

et al. 2017

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“…In rodents, the homologous regions are postrhinal cortex (34), which has been shown to be important for place recognition (35), and retrosplenial cortex, which has been shown to be important for deriving directional information from environmental cues (36). Retrosplenial cortex contains head direction (HD) cells, which discharge selectively when the head of an animal is oriented in a particular facing direction (37), and a previous report demonstrated that these cells are primarily sensitive to environmental geometry rather than nongeometric features after disorientation (38). In addition, neurons that code allocentric locations relative to geometric boundaries have been identified in the entorhinal cortex (39) and subiculum (40) of the rodent, and these cells might be important for retrieving the location of the reward within the chamber after chamber identity and heading have been reestablished.…”

Section: Discussionmentioning

confidence: 99%

Place recognition and heading retrieval are mediated by dissociable cognitive systems in mice

Julian

Keinath

Muzzio

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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A lost navigator must identify its current location and recover its facing direction to restore its bearings. We tested the idea that these two tasks-place recognition and heading retrieval-might be mediated by distinct cognitive systems in mice. Previous work has shown that numerous species, including young children and rodents, use the geometric shape of local space to regain their sense of direction after disorientation, often ignoring nongeometric cues even when they are informative. Notably, these experiments have almost always been performed in single-chamber environments in which there is no ambiguity about place identity. We examined the navigational behavior of mice in a two-chamber paradigm in which animals had to both recognize the chamber in which they were located (place recognition) and recover their facing direction within that chamber (heading retrieval). In two experiments, we found that mice used nongeometric features for place recognition, but simultaneously failed to use these same features for heading retrieval, instead relying exclusively on spatial geometry. These results suggest the existence of separate systems for place recognition and heading retrieval in mice that are differentially sensitive to geometric and nongeometric cues. We speculate that a similar cognitive architecture may underlie human navigational behavior.navigation | scene perception | spatial representation | geometry processing | neural specialization A navigator who becomes lost must solve two tasks to regain her bearings. First, she must identify her current location, a process we term place recognition. Second, she must identify her current facing direction, a process we term heading retrieval. These two tasks are logically dissociable from each other: A "you are here" map identifies location without revealing heading, whereas a compass reveals heading without identifying location. Neurophysiological work on rodents suggests that the outputs of these two processes are represented by distinct neural populations: Location is coded in the hippocampus, in both general terms (different environments elicit different hippocampal maps) and specific terms (place cells fire at specific coordinates within an environment), whereas heading is encoded by head direction (HD) cells in several structures including the postsubiculum, thalamus, and retrosplenial cortex (1-3). However, little is known about the systems that determine these quantities from perceptual inputs. In particular, it is not known whether place recognition and heading retrieval are mediated by the same or different processing streams.Here, we use a novel behavioral paradigm to test the hypothesis that the mechanisms that mediate place recognition at the coarse level (i.e., identification of the current environment) in mice are dissociable from the mechanisms that mediate heading retrieval. We use a variant of a spatial reorientation task that has been used extensively to study navigation behavior in a variety of species, including rodents and human children (4-7...

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“…A cylinder was selected as a recording arena to minimise the influence of the environment’s geometry as an orienting cue (Golob et al, 2001; Knight et al, 2011). Attached to the inner wall of the cylinder with Velcro tape were two 50 × 50 cm cue cards (Figure 1(b)) made from black and/or white polypropylene sheets, each subtending ~77° of arc, and located 180° apart.…”

Section: Methodsmentioning

confidence: 99%

Retrosplenial and postsubicular head direction cells compared during visual landmark discrimination

Lozano

Page

Philippe

et al. 2017

Brain and Neuroscience Advances

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Background:Visual landmarks are used by head direction (HD) cells to establish and help update the animal’s representation of head direction, for use in orientation and navigation. Two cortical regions that are connected to primary visual areas, postsubiculum (PoS) and retrosplenial cortex (RSC), possess HD cells: we investigated whether they differ in how they process visual landmarks.Methods:We compared PoS and RSC HD cell activity from tetrode-implanted rats exploring an arena in which correct HD orientation required discrimination of two opposing landmarks having high, moderate or low discriminability.Results:RSC HD cells had higher firing rates than PoS HD cells and slightly lower modulation by angular head velocity, and anticipated actual head direction by ~48 ms, indicating that RSC spiking leads PoS spiking. Otherwise, we saw no differences in landmark processing, in that HD cells in both regions showed equal responsiveness to and discrimination of the cues, with cells in both regions having unipolar directional tuning curves and showing better discrimination of the highly discriminable cues. There was a small spatial component to the signal in some cells, consistent with their role in interacting with the place cell navigation system, and there was also slight modulation by running speed. Neither region showed theta modulation of HD cell spiking.Conclusions:That the cells can immediately respond to subtle differences in spatial landmarks is consistent with rapid processing of visual snapshots or scenes; similarities in PoS and RSC responding may be due either to similar computations being performed on the visual inputs, or to rapid sharing of information between these regions. More generally, this two-cue HD cell paradigm may be a useful method for testing rapid spontaneous visual discrimination capabilities in other experimental settings.

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Geometric Cues Influence Head Direction Cells Only Weakly in Nondisoriented Rats

Cited by 38 publications

References 31 publications

Environmental Geometry Aligns the Hippocampal Map during Spatial Reorientation

Environmental Geometry Aligns the Hippocampal Map during Spatial Reorientation

Place recognition and heading retrieval are mediated by dissociable cognitive systems in mice

Retrosplenial and postsubicular head direction cells compared during visual landmark discrimination

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