An allocentric human odometer for perceiving distances on the ground plane

Reviewer #1 (Public Review):

This study conducted a series of experiments to comprehensively support the allocentric rather than egocentric visual spatial reference updating for the path-integration mechanism in the control of target-oriented locomotion. Authors firstly manipulated the waiting time before walking to tease apart the influence from spatial working memory in guiding locomotion. They demonstrated that the intrinsic bias in perceiving distance remained constant during walking and that the establishment of a new spatial layout in the brain took a relatively longer time beyond the visual-spatial working memory. In the following experiments, the authors then uncovered that the strength of the intrinsic bias in distance perception along the horizontal direction is reduced when participants' attention is distracted, implying that world-centered path integration requires attentional effort. This study also revealed horizontal-vertical asymmetry in a spatial coding scheme that bears a resemblance to the locomotion control in other animal species such as desert ants.

The overall design of the behavioral experiments is elegant and statistics are well performed to support the authors' viewpoint in the allocentric rather than egocentric visual spatial coding scheme for distance perception along the horizontal line.

It is however worth noting the statement from Gibson in 1979 that for egocentric distances, tangible information arises from the effort required to walk a distance, thus, effort becomes associated through experience with visual distance cues. Accordingly, visual information alone is insufficient to support the awareness of distance. Perceived distance is rather specified by an invariant relationship between distal extent and a persons' potential to perform gross motion actions such as walking. This view is supported later by Proffitt et al. (2003) in which participants wore backpacks and their perceived distance increased compared with the baseline condition. Authors need to acknowledge the physical effort in addition to visual information for the spatial coding and may consider the manipulation of physical efforts in the future to support the robustness of constant intrinsic bias in ground-based spatial coding during walking.

Furthermore, it would be more comprehensive and fit into the Neuroscience Section if the authors can add in current understandings of the spatial reference frames in neuroscience in the introduction and discussion, and provide explanations on how the findings of this study supplement the physiological evidence that supports our spatial perception as well. For instance, world-centered representations of the environment, or cognitive maps, are associated with hippocampal formation while self-centered spatial relationships, or image spaces, are associated with the parietal cortex (see Bottini, R., & Doeller, C. F. (2020). Knowledge Across Reference Frames: Cognitive Maps and Image Spaces. Trends in Cognitive Sciences, 24(8), 606-619. https://doi.org/10.1016/j.tics.2020.05.008 for details)

Reviewer #2 (Public Review):

The study provides a valuable contribution by demonstrating the use of an allocentric spatial reference frame in the perception of the location of a dimly lit target in the dark. While the evidence presented in support of the authors' claims is solid and convincing, it would be beneficial for the study to address potential limitations, such as its ecological validity.

Strengths:
Unlike previous research where observers were stationary during a visual-spatial perception task, this recent study expanded upon prior findings by incorporating bodily movements for the observers. This study is a valuable addition to the literature as it not only discovered that the intrinsic bias is grounded on the home base, but also identified several key characteristics through a series of follow-up experiments. The findings suggest that this "allocentric" spatial coding decays over time, requires attentional resources, can be based solely on vestibular signals, and is most effective in the horizontal direction. In general, this study is interesting, clearly presented, well-thought-out and executed. The results confirmed the conclusions and the study's comprehensive approach offers valuable insights into the nature of intrinsic bias in spatial perception.

The counter-intuitive results presented in the manuscript are intriguing and add to the study's overall appeal. Moreover, the manuscript draws an interesting parallel between human spatial navigation and that of desert ants. This comparison helps to underscore the importance of understanding spatial coding mechanisms across different species and highlights potential avenues for future research.

One aspect I particularly valued about this study was the authors' thorough description of the experimental methods. This level of detail not only highlights the rigor of the research but also enhances the reproducibility of the study, making it more accessible for future researchers.

Weaknesses:
While the current study provides valuable insights into the nature of intrinsic bias in spatial perception, there is a concern regarding its ecological validity. The experimental design involved stringent precautions, such as a very dark room and a small target, to minimize the presence of depth cues. This is in contrast to the real world, where depth information is readily available from the ground and surrounding objects, aiding in our perception of space and depth. As a result, it is unclear to what extent this "allocentric" intrinsic bias is involved in our everyday spatial perception. To provide more context for the general audience, it would be beneficial for the authors to address this issue in their discussion.

The current findings on the "allocentric" coding scheme raise some intriguing questions as to why such a mechanism would be developed and how it could be beneficial. The finding that the "allocentric" coding scheme results in less accurate object localization and requires attentional resources seems counterintuitive and raises questions about its usefulness. However, this observation presents an opportunity for the manuscript to discuss the potential evolutionary advantages or trade-offs associated with this coding mechanism.

The manuscript lacks a thorough description of the data analysis process, particularly regarding the fitting of the intrinsic bias curve (e.g., the blue and gray dashed curve in Figure 3c) and the calculation of the horizontal separation between the curves. It would be beneficial for the authors to provide more detailed information on the specific function and parameters used in the fitting process and the formula used for the separation calculation to ensure the transparency and reproducibility of the study's results.

Reviewer #3 (Public Review):

This study investigated what kind of reference (allocentric or egocentric) frame we used for perception in darkness. This question is essential and was not addressed much before. The authors compared the perception in the walking condition with that in the stationary condition, which successfully separated the contribution of self-movement to the spatial representation. In addition, the authors also carefully manipulated the contribution of the waiting period, attentional load, vestibular input, testing task, and walking direction (forward or backward) to examine the nature of the reference frame in darkness systematically.

I am a bit confused by Figure 2b. Allocentric coordinate refers to the representation of the distance and direction of an object relative to other objects but not relative to the observer. In Figure 2, however, the authors assumed that the perceived target was located on the interception between the intrinsic bias curve and the viewing line from the NEW eye position to the target. This suggests that the perceived object depends on the observer's new location, which seems odd with the allocentric coordinate hypothesis.

According to Fig 2b, the perceived size should be left-shifted and lifted up in the walking condition compared to that in the stationary condition. However, in Figure 3C and Fig 4, the perceived size was the same height as that in the baseline condition.

Is the left-shifted perceived distance possibly reflecting a kind of compensation mechanism? Participants could not see the target's location but knew they had moved forward. Therefore, their brain automatically compensates for this self-movement when judging the location of a target. This would perfectly predict the left-shifted but not upward-shifted data in Fig 3C. A similar compensation mechanism exists for size constancy in which we tend to compensate for distance in computing object size.

According to Fig 2a, the target, perceived target, and eye should be aligned in one straight line. This means that connecting the physical targets and the corresponding perceived target results in straight lines that converge at the eye position. This seems, however, unlikely in Figure 3c.