Exploratory patterns of rats on a complex maze provide evidence for topological coding

Poucet, Bruno; Herrmann, Thom

doi:10.1016/s0376-6357(00)00151-0

Cited by 42 publications

(39 citation statements)

References 22 publications

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“…There is our recent modeling work showing the feasibility of spatial learning based on topological information (Dabaghian et al, 2012; Arai et al, 2014); early studies by Piaget and Inhelder showing that children first conceive of spatial relations in topological terms and only later think in terms of geometrical positions (Dawson and Doddington, 1973); and previous studies on rodent navigation showing that place cells respond to topological changes in the environment such as the placement or removal of a barrier across a previously learned route (Poucet and Herrmann, 2001; Alvernhe et al, 2011, 2012). We propose that a topological framework, more like a subway map, would provide the hippocampus a more powerful, flexible, and readily formed spatial substrate for creating experiential memories or evaluating the spatial context of behaviors (Lavenex and Amaral, 2000; Banquet et al, 2005).…”

Section: Discussionmentioning

confidence: 99%

“…This neglect is even more curious in light of Piaget's early work indicating that children first represent space topologically and only later learn to incorporate metrical details into their mental representations of space (Poucet, 1993; O'Keefe and Nadel, 1978). A few studies have shown that place cell firing is responsive to topological changes in the environment such as the placement or removal of a barrier across a previously learned route (Poucet and Herrmann, 2001; Alvernhe et al, 2011), but as noted above, place cells seem to be responsive to an enormous variety of inputs. Our interest ultimately is not whether place cells can respond to topological features of a space, but whether the information conveyed downstream by place cell spiking might encode topological information, which would offer considerable advantages over geometry in terms of computational speed and flexibility.…”

Section: Introductionmentioning

confidence: 99%

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Reconceiving the hippocampal map as a topological template

Dabaghian

Brandt

Frank

2014

eLife

132

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The role of the hippocampus in spatial cognition is incontrovertible yet controversial. Place cells, initially thought to be location-specifiers, turn out to respond promiscuously to a wide range of stimuli. Here we test the idea, which we have recently demonstrated in a computational model, that the hippocampal place cells may ultimately be interested in a space's topological qualities (its connectivity) more than its geometry (distances and angles); such higher-order functioning would be more consistent with other known hippocampal functions. We recorded place cell activity in rats exploring morphing linear tracks that allowed us to dissociate the geometry of the track from its topology. The resulting place fields preserved the relative sequence of places visited along the track but did not vary with the metrical features of the track or the direction of the rat's movement. These results suggest a reinterpretation of previous studies and new directions for future experiments.DOI: http://dx.doi.org/10.7554/eLife.03476.001

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Reconceiving the hippocampal map as a topological template

Dabaghian

Brandt

Frank

2014

eLife

132

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“…Network-like topologic features in spatial behavior were previously noted by Poucet [79], who claimed that spatial representation is primarily built and processed as a topologic depiction of the environment. It was then shown that topologic features exist in spatial representation in rats [80]. Nevertheless, while previous studies have revealed that topologic features such as connectivity are present in the spatial behavior of rats, they did not utilize classical network parameters such as node degree, clustering coefficient, or shortest mean path, making it difficult to compare them to other network-related studies.…”

Section: Discussionmentioning

confidence: 99%

Network Analysis of Rat Spatial Cognition: Behaviorally-Established Symmetry in a Physically Asymmetrical Environment

et al. 2012

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BackgroundWe set out to solve two inherent problems in the study of animal spatial cognition (i) What is a “place”?; and (ii) whether behaviors that are not revealed as differing by one methodology could be revealed as different when analyzed using a different approach.MethodologyWe applied network analysis to scrutinize spatial behavior of rats tested in either a symmetrical or asymmetrical layout of 4, 8, or 12 objects placed along the perimeter of a round arena. We considered locations as the units of the network (nodes), and passes between locations as the links within the network.Principal FindingsWhile there were only minor activity differences between rats tested in the symmetrical or asymmetrical object layouts, network analysis revealed substantial differences. Viewing ‘location’ as a cluster of stopping coordinates, the key locations (large clusters of stopping coordinates) were at the objects in both layouts with 4 objects. However, in the asymmetrical layout with 4 objects, additional key locations were spaced by the rats between the objects, forming symmetry among the key locations. It was as if the rats had behaviorally imposed symmetry on the physically asymmetrical environment. Based on a previous finding that wayfinding is easier in symmetrical environments, we suggest that when the physical attributes of the environment were not symmetrical, the rats established a symmetric layout of key locations, thereby acquiring a more legible environment despite its complex physical structure.Conclusions and SignificanceThe present study adds a behavioral definition for “location”, a term that so far has been mostly discussed according to its physical attributes or neurobiological correlates (e.g. - place and grid neurons). Moreover, network analysis enabled the assessment of the importance of a location, even when that location did not display any distinctive physical properties.

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“…Previous evidence for topological coding was provided by experiments on behavior in response to spatial changes, which suggested exploration to be renewed after topological changes (e.g., Poucet et al 1986), and by path choice studies (e.g., Poucet 1984;Poucet and Herrmann 2001;Poucet et al 1990). However, these previous experiments suffered from a lack of appropriate control measures.…”

Section: Discussionmentioning

confidence: 99%

Rats build and update topological representations through exploration

2011

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Although rats are able to build complex spatial representations of their surroundings during exploration, the nature of the encoded information is still a matter for debate. In particular, it is not well established if rats can process the topological structure of the environment in such a way that they are aware of the connections existing between remote places. Here, rats were first exposed for four 5-min trials to a complex environment divided into several sectors that were separated by doors allowing either unrestricted or restricted access to other sectors. In the fifth test trial, we measured the behavior of the animals while they explored the same environment in which, however, they faced changes that either altered or did not alter the topological structure of the environment. In experiment 1, closing previously opened doors prevented the rat from having direct access between corresponding sectors. In experiment 2, opening previously closed doors allowed direct access between sectors that had not been directly accessible. In each experiment, control doors allowed us to discard the mere influence of door manipulation. We compared the rats' exploratory behavior in response to door manipulations that either strongly altered or did not alter the ability to commute between sectors and found evidence that the animals displayed differential reactions to the two types of door manipulations. This implies that during exploration rats build a precise map of the connectivity of space that can be flexibly updated and used for efficient navigation.

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Exploratory patterns of rats on a complex maze provide evidence for topological coding

Cited by 42 publications

References 22 publications

Reconceiving the hippocampal map as a topological template

Reconceiving the hippocampal map as a topological template

Network Analysis of Rat Spatial Cognition: Behaviorally-Established Symmetry in a Physically Asymmetrical Environment

Rats build and update topological representations through exploration

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