A previously undescribed scene-selective site is the key to encoding ego-motion in natural environments

Reviewer #1 (Public Review):

Summary:
The authors ran a series of experiments with separate subject populations, different stimuli, and on two different MRI scanners (one 3T, one 7T) to establish a scenes-selective region on the intraparietal gyrus that they decided to name PIGS. I think that IPA (intraparietal place area) would also have been a good choice with an allusion to a beverage rather than a domestic animal. The authors show that PIGS can be detected robustly through a series of experiments. They anatomically and functionally separate PIGS from nearby V6, which encodes optic flow. The authors determined that PIGS encodes ego-motion.

Strengths:
The robust detection of PIGS in several experiments with different sets of participants and on different scanners makes these results convincing. The functional differentiation is well executed.

Weaknesses:
The distinction of PIGS from nearby OPA, which has also been implied in navigation and ego-motion, is not as clear as it could be.

Impact:
Overall, this is a valuable contribution to the cognitive neuroscience of the visual system. It shows that there is still room for discovering details of visual processing, given recent advances in scanning technology, statistical methods, and larger sample sizes.

Reviewer #2 (Public Review):

Summary
The authors report an extensive series of neuroimaging experiments (at both 3T and 7T) to provide evidence for a scene-selective visual area in the human posterior parietal cortex (PIGS) that is distinct from the main three (parahippocampal place area, PPA; occipital place area, OPA; medial place area, MPA) typically reported in the literature. Further, they argue that in comparison with the other three, this region may specifically be involved in representing ego-motion in natural contexts. The characterization of this scene-selective region provides a useful reference point for studies of scene processing in humans.

Strengths
One of the major strengths of the work is the extensive series of experiments reported, showing clear reproducibility of the main finding and providing functional insight into the region studied. The results are clearly presented and for the most part, convincing.

Weaknesses
One of the major weaknesses of the work is the failure to relate the current results to other findings in the literature, making it hard to assess whether it is is a "previously undescribed scene-selective site".

First, the scene-selective region identified appears to overlap with regions that have previously been identified in terms of their retinotopic properties. In particular, it is unclear whether this region overlaps with V7/IPS0 and/or IPS1. This is particularly important since prior work has shown that OPA often overlaps with v7/IPS0 (Silson et al, 2016, Journal of Vision). The findings would be much stronger if the authors could show how the location of PIGS relates to retinotopic areas (other than V6, which they do currently consider). I wonder if the authors have retinotopic mapping data for any of the participants included in this study. If not, the authors could always show atlas-based definitions of these areas (e.g. Wang et al, 2015, Cerebral Cortex).

Second, recent studies have reported a region anterior to OPA that seems to be involved in scene memory (Steel et al, 2021, Nature Communications; Steel et al, 2023, The Journal of Neuroscience; Steel et al, 2023, biorXiv). Is this region distinct from PIGS? Based on the figures in those papers, the scene memory-related region is inferior to V7/IPS0, so characterizing the location of PIGS to V7/IPS0 as suggested above would be very helpful here as well.

If PIGS overlaps with either of V7/IPS0 or the scene memory-related area described by Steel and colleagues, then arguably it is not a newly defined region (although the characterization provided here still provides new information).

Another reason that it would be helpful to relate PIGS to this scene memory area is that this scene memory area has been shown to have activity related to the amount of visuospatial context (Steel et al, 2023, The Journal of Neuroscience). The conditions used to show the sensitivity of PIGS to ego-motion also differ in the visuospatial context that can be accessed from the stimuli. Even if PIGS appears distinct from the scene memory area, the degree of visuospatial context is an alternative account of what might be represented in PIGS.

Reviewer #3 (Public Review):

Summary:
The authors report a scene-selective area in the posterior intraparietal gyrus (PIGS). This area lies outside the classical three scene-selective regions (PPA/TPA, RSC/MPA, TOS/OPA), and is selective for ego-motion.

Strengths:
The authors firmly establish the location and selectivity of the new area through a series of well-crafted controlled experiments. They show that the area can be missed with too much smoothing, thus providing a case for why it has not been previously described. They show that it appears in much the same location in different subjects, with different magnetic field strengths, and with different stimulus sets. Finally, they show that it is selective for ego-motion - defined as a series of sequential photographs of an egocentric trajectory along a path. They further clarify that the area is not generically motion-selective by showing that it does not respond to biological motion without an ego-motion component to it. All statistics are standard and sound; the evidence presented is strong.

Weaknesses:
There are few weaknesses in this work. If pressed, I might say that the stimuli depicting ego-motion do not, strictly speaking, depict motion, but only apparent motion between 2m apart photographs. However, this choice was made to equate frame rates and motion contrast between the 'ego-motion' and a control condition, which is a useful and valid approach to the problem. Some choices for visualization of the results might be made differently; for example, outlines of the regions might be shown in more plots for easier comparison of activation locations, but this is a minor issue.

This is a very strong paper.

Author Response

Reviewer 1:

Comment 1.1: The distinction of PIGS from nearby OPA, which has also been implied in navigation and ego-motion, is not as clear as it could be.

Response1.1: The main functional distinction between TOS/OPA and PIGS is that TOS/OPA responds preferentially to moving vs. stationary stimuli (even concentric rings), likely due to its overlap with the retinotopic motion-selective visual area V3A, for which this is a defining functional property (e.g. Tootell et al., 1997, J Neurosci). In comparison, PIGS does not show such a motion-selectivity. Instead, PIGS responds preferentially to more complex forms of motion within scenes. In this revision, we tried to better highlight this point in the Discussion (see also the response to the first comment from Reviewer #2).

Reviewer 2:

Comment 2.1: First, the scene-selective region identified appears to overlap with regions that have previously been identified in terms of their retinotopic properties. In particular, it is unclear whether this region overlaps with V7/IPS0 and/or IPS1. This is particularly important since prior work has shown that OPA often overlaps with v7/IPS0 (Silson et al, 2016, Journal of Vision). The findings would be much stronger if the authors could show how the location of PIGS relates to retinotopic areas (other than V6, which they do currently consider). I wonder if the authors have retinotopic mapping data for any of the participants included in this study. If not, the authors could always show atlas-based definitions of these areas (e.g. Wang et al, 2015, Cerebral Cortex).

Response 2.1: We thank the reviewers for reminding us to more clearly delineate this issue of possible overlap, including the information provided by Silson et al, 2016. The issue of possible overlap between area TOS/OPA and the retinotopic visual areas, both in humans and non-human primates, was also clarified by our team in 2011 (Nasr et al., 2011). As you can see in the enclosed figure, and consistent with those previous studies, TOS/OPA overlaps with visual areas V3A/B and V7. Whereas PIGS is located more dorsally close to IPS2-4. As shown here, there is no overlap between PIGS and TOS/OPA and there is no overlap between PIGS and areas V3A/B and V7. To more directly address the reviewer’s concern, in the next revision, we will show the relative position of PIGS and the retinotopic areas (at least) in one individual subject.

Author response image 1.

The relative location of PIGS, TOS/OPA and the retinotopic visual areas. The left panel showed the result of high-resolution (7T; voxel size = 1 mm; no spatial smoothing) polar angle mapping in one individual. The right panel shows the location of scene-selective areas PIGS and TOS/OPA in the same subject (7T; voxel size = 1 mm; no spatial smoothing). While area TOS/OPA shows some overlap with the retinotopic visual areas V3A/B and V7, PIGS shows partial overlap with area IPS2-4. In both panels, the activity maps are overlaid on the subjects’ own reconstructed brain surface.

Comment 2.2: Second, recent studies have reported a region anterior to OPA that seems to be involved in scene memory (Steel et al, 2021, Nature Communications; Steel et al, 2023, The Journal of Neuroscience; Steel et al, 2023, biorXiv). Is this region distinct from PIGS? Based on the figures in those papers, the scene memory-related region is inferior to V7/IPS0, so characterizing the location of PIGS to V7/IPS0 as suggested above would be very helpful here as well. If PIGS overlaps with either of V7/IPS0 or the scene memory-related area described by Steel and colleagues, then arguably it is not a newly defined region (although the characterization provided here still provides new information).

Response 2.2: The lateral-place memory area (LPMA) is located on the lateral brain surface, anterior relative to the IPS (see Figure 1 from Steel et al., 2021 and Figure 3 from Steel et al., 2023). In contrast, PIGS is located on the posterior brain surface, also posterior relative to the IPS. In other words, they are located on two different sides of a major brain sulcus. In this revision we have clarified this point, including the citations by Steel and colleagues.

Comments 2.3: Another reason that it would be helpful to relate PIGS to this scene memory area is that this scene memory area has been shown to have activity related to the amount of visuospatial context (Steel et al, 2023, The Journal of Neuroscience). The conditions used to show the sensitivity of PIGS to ego-motion also differ in the visuospatial context that can be accessed from the stimuli. Even if PIGS appears distinct from the scene memory area, the degree of visuospatial context is an alternative account of what might be represented in PIGS.

Response 2.3: The reviewer raises an interesting point. One minor confusion is that we may be inadvertently referring to two slightly different types of “visuospatial context”. Specifically, the stimuli used in the ego-motion experiment here (i.e. coherently vs. incoherently changing scenes) represent the same scenes, and the only difference between the two conditions is the sequence of images across the experimental blocks. In that sense, the two experimental conditions may be considered to have the same visuospatial context. However, it could be also argued that the coherently changing scenes provide more information about the environmental layout. In that case, considering the previous reports that PPA/TPA and RSC/MPA may also be involved in layout encoding (Epstein and Kanwisher 1998; Wolbers et al. 2011), we expected to see more activity within those regions in response to coherently compared incoherently changing scenes. These issues are now more explicitly discussed in the revised article.

Reviewer 3:

Comment 3.1: There are few weaknesses in this work. If pressed, I might say that the stimuli depicting ego-motion do not, strictly speaking, depict motion, but only apparent motion between 2s apart photographs. However, this choice was made to equate frame rates and motion contrast between the 'ego-motion' and a control condition, which is a useful and valid approach to the problem. Some choices for visualization of the results might be made differently; for example, outlines of the regions might be shown in more plots for easier comparison of activation locations, but this is a minor issue.

Response 3.1: We thank the reviewer for these constructive suggestions, and we agree with their comment that the ego-motion stimuli are not smooth, even though they were refreshed every 100 ms. However, the stimuli were nevertheless coherent enough to activate areas V6 and MT, two major areas known to respond preferentially to coherent compared to incoherent motion.

Epstein, R., and N. Kanwisher. 1998. 'A cortical representation of the local visual environment', Nature, 392: 598-601.

Wolbers, T., R. L. Klatzky, J. M. Loomis, M. G. Wutte, and N. A. Giudice. 2011. 'Modality-independent coding of spatial layout in the human brain', Curr Biol, 21: 984-9.