Peer review process
Revised: This Reviewed Preprint has been revised by the authors in response to the previous round of peer review; the eLife assessment and the public reviews have been updated where necessary by the editors and peer reviewers.
Read more about eLife’s peer review process.Editors
- Reviewing EditorNoah CowanJohns Hopkins University, Baltimore, United States of America
- Senior EditorKate WassumUniversity of California, Los Angeles, Los Angeles, United States of America
Reviewer #1 (Public review):
Assessment:
This fundamental work advances our understanding of navigation and path integration in mammals by using a clever behavioral paradigm. The paper provides compelling evidence that mice are able to create and use a cognitive map to find "short cuts" in an environment, using only the location of rewards relative to the point of entry to the environment and path integration, and need not rely on visual landmarks.
Summary:
The authors have designed a novel experimental apparatus called the 'Hidden Food Maze (HFM)' and a beautiful suite of behavioral experiments using this apparatus to investigate the interplay between allothetic and idiothetic cues in navigation. The results presented provide a clear demonstration of the central claim of the paper, namely that mice only need a fixed start location and path integration to develop a cognitive map. The experiments and analyses conducted to test the main claim of the paper -- that the animals have formed a cognitive map -- are conclusive and include many thoughtfully designed control experiments to eliminate alternatives.
Strengths:
The 90 degree rotationally symmetric design and use of 4 distal landmarks and 4 quadrants with their corresponding rotationally equivalent locations (REL) lends itself to teasing apart the influence of path integration and landmark-based navigation in a clever way. The authors use a complete set of experiments and associated controls to show that mice can use a start location and path integration to develop a cognitive map and generate shortcut routes to new locations.
Weaknesses:
There were no major weaknesses identified that were not addressed during revisions.
Reviewer #3 (Public review):
Summary:
How is it that animals find learned food locations in their daily life? Do they use landmarks to home in on these learned locations or do they learn a path based on self-motion (turn left, take ten steps forward, turn right, etc.). This study carefully examines this question in a well-designed behavioral apparatus. A key finding is that to support the observed behavior in the hidden food arena, mice appear to not use the distal cues that are present in the environment for performing this task. Removal of such cues did not change the learning rate, for example. In a clever analysis of whether the resulting cognitive map based on self-motion cues could allow a mouse to take a shortcut, it was found that indeed they are. The work nicely shows the evolution of the rodent's learning of the task, and the role of active sensing in the targeted reduction of uncertainty of food location proximal to its expected location.
Strengths:
A convincing demonstration that mice can synthesize a cognitive map for the finding of a static reward using body frame-based cues. Showing that uncertainty of final target location is resolved by an active sensing process of probing holes proximal to the expected location. Showing that changing the position of entry into the arena rotates the anticipated location of the reward in a manner consistent with failure to use distal cues.
Weaknesses:
Weaknesses: The Reviewing Editor felt that previously identified weaknesses from Reviewer #3 were adequately addressed in the final manuscript.