Lever, C; Burton, S; Jeewajee, A; O'Keefe, J; Burgess, N; (2009) Boundary vector cells in the subiculum of the hippocampal formation. Journal of Neuroscience , 29 (31) 9771 - 9777. 10.1523/​JNEUROSCI.1319-09.2009.

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Abstract

Stretching a familiar rectangular environment along one axis results in a stretching of place cell (PC) firing fields (“place fields”) along the same axis (O’Keefe and Burgess, 1996). To explain this finding, we predicted “boundary vector cells” (BVCs) as inputs to the PCs (O’Keefe and Burgess, 1996, Burgess et al., 2000; Hartley et al., 2000). A BVC would fire whenever an environmental boundary intersected a receptive field located at a specific distance from the rat in a specific allocentric direction (Fig. 1A), with breadth of tuning to distance that increases with the preferred distance (Fig. 1B). The firing of a BVC depends solely on the rat’s location relative to environmental boundaries and is independent of the rat’s heading direction. BVCs with receptive fields peaked farther from the animal have broader firing fields than those peaked closer to it. Figure 1C shows the BVC firing field (above) generated by a specific BVC receptive field (below). The firing of a PC is a thresholded sum of the firing of the BVCs synapsing onto it. If a PC’s input consists of a random selection of BVCs, then this model captures the statistics of the shape, number, and size of place fields as a function of the configuration of environmental boundaries (Hartley et al., 2000). Notably, the proportion of BVCs with a specific preferred distance has to decrease with preferred distance, so as to provide even coverage despite the increase in breadth of tuning (Hartley et al., 2000). As the environment becomes familiar, plasticity in the BVC-to-PC connections causes a “tidying” of PC firing, such that regions of lower firing rate are lost, whereas regions of higher firing rate strengthen (Barry and Burgess, 2007), consistent with experimental data from CA1 (Lever et al., 2002b; Barry et al., 2006; Karlsson and Frank, 2008). The power of the BVC model is seen in its ability to predict the effects of environmental manipulations on BVC and PC firing. For example, Figure 1D shows the different spatial firing patterns expected of the BVC in Figure 1C in four different environmental configurations, assuming that the sense of direction is held constant. Firing occurs at locations where the environmental boundary intersects the BVC’s receptive field, producing crescent-shaped firing in the cylinder, firing parallel to one or more walls in a square box, and an additional firing field if a barrier perpendicular to the BVC’s preferred direction is introduced into the environment. This second BVC field in response to insertion of a barrier should also be mirrored by the appearance of second fields in downstream PCs (Burgess et al., 2000), a prediction confirmed by Hartley et al. (2000) and Lever et al. (2002b). Plasticity in the BVC–PC connections (Barry and Burgess, 2007) satisfactorily models the disappearance of one of the two place fields once the configuration becomes familiar (Lever et al., 2002b; Rivard et al., 2004; Barry et al., 2006). Examining the effects of environmental shape on place fields was pioneered by Muller and Kubie (1987), whereas Sharp (1999) noted the importance of environmental boundaries for subicular firing. Here, we report cells recorded in the dorsal subiculum that fulfill the criteria for BVCs. Barry et al. (2006) presented a preliminary description of these cells.

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