Abstract
Recent studies have shown that place cells in the hippocampus possess firing fields that repeat in physically similar, parallel environments. These results imply that it should be difficult for animals to distinguish parallel environments at a behavioral level. To test this, we trained rats on a novel odor‐location task in an environment with four parallel compartments which had previously been shown to yield place field repetition. A second group of animals was trained on the same task, but with the compartments arranged in different directions, an arrangement we hypothesised would yield less place field repetition. Learning of the odor‐location task in the parallel compartments was significantly impaired relative to learning in the radially arranged compartments. Fewer animals acquired the full discrimination in the parallel compartments compared to those trained in the radial compartments, and the former also required many more sessions to reach criterion compared to the latter. To confirm that the arrangement of compartments yielded differences in place cell repetition, in a separate group of animals we recorded from CA1 place cells in both environments. We found that CA1 place cells exhibited repeated fields across four parallel local compartments, but did not do so when the same compartments were arranged radially. To confirm that the differences in place field repetition across the parallel and radial compartments depended on their angular arrangement, and not incidental differences in access to an extra‐maze visual landmark, we repeated the recordings in a second set of rats in the absence of the orientation landmark. We found, once again, that place fields showed repetition in parallel compartments, and did not do so in radially arranged compartments. Thus place field repetition, or lack thereof, in these compartments was not dependent on extra‐maze cues. Together, these results imply that place field repetition constrains spatial learning. © 2015 Wiley Periodicals, Inc.
Highlights
An influential view of the hippocampus is that it provides a cognitive map of the environment via place cells which represent specific locations (O’Keefe and Nadel, 1978)
Task acquisition was more difficult for animals trained in parallel compartments than for those trained in radial compartments
At both the two and three-compartment stages, animals in the parallel compartments required significantly more trials to reach criterion compared to those trained in the radial compartments (Fig. 2; univariate ANOVA: two compartments: F(1,10) 5 5.6, P < 0.0002; three compartments: F(1,10) 5 4.6, P < 0.001; analysis of four compartments was not done as only two animals in the parallel compartments reached this stage)
Summary
An influential view of the hippocampus is that it provides a cognitive map of the environment via place cells which represent specific locations (O’Keefe and Nadel, 1978). In the Derdikman et al experiments, both grid cells and place cells showed repeated firing in multiple parallel alleyways of a hairpin maze when the animals traversed in the same direction. These results agree with earlier findings that place cells exhibit similar firing fields in two visually identical environments oriented in the same direction and connected by a corridor along one side (Skaggs and McNaughton, 1998; Fuhs et al, 2005). These results suggest that place cells are driven primarily by local cues such as the boundaries, shape, and color of local environments (O’Keefe and Burgess, 1996; Barry et al, 2006; Hartley et al, 2000; Monaco et al, 2014), and are not influenced significantly by linear self-motion cues, which could be used to distinguish these environments (Fuhs et al, 2005, Spiers et al, 2015)
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