Elsevier

NeuroImage

Volume 170, 15 April 2018, Pages 373-384
NeuroImage

Defining the most probable location of the parahippocampal place area using cortex-based alignment and cross-validation

https://doi.org/10.1016/j.neuroimage.2017.04.040Get rights and content

Highlights

  • A probabilistic place ROI was created from cortex-based alignment in 24 participants

  • Cross-validation shows that this ROI predicts place selectivity in new participants

  • This ROI predicts voxels with peak place selectivity in >500 participants

  • The collateral/lingual sulcal junction is most predictive of place selectivity

  • We share this predictive ROI with the field (vpnl.stanford.edu/PlaceSelectivity)

Abstract

The parahippocampal place area (PPA) is a widely studied high-level visual region in the human brain involved in place and scene processing. The goal of the present study was to identify the most probable location of place-selective voxels in medial ventral temporal cortex. To achieve this goal, we first used cortex-based alignment (CBA) to create a probabilistic place-selective region of interest (ROI) from one group of 12 participants. We then tested how well this ROI could predict place selectivity in each hemisphere within a new group of 12 participants. Our results reveal that a probabilistic ROI (pROI) generated from one group of 12 participants accurately predicts the location and functional selectivity in individual brains from a new group of 12 participants, despite between subject variability in the exact location of place-selective voxels relative to the folding of parahippocampal cortex. Additionally, the prediction accuracy of our pROI is significantly higher than that achieved by volume-based Talairach alignment. Comparing the location of the pROI of the PPA relative to published data from over 500 participants, including data from the Human Connectome Project, shows a striking convergence of the predicted location of the PPA and the cortical location of voxels exhibiting the highest place selectivity across studies using various methods and stimuli. Specifically, the most predictive anatomical location of voxels exhibiting the highest place selectivity in medial ventral temporal cortex is the junction of the collateral and anterior lingual sulci. Methodologically, we make this pROI freely available (vpnl.stanford.edu/PlaceSelectivity), which provides a means to accurately identify a functional region from anatomical MRI data when fMRI data are not available (for example, in patient populations). Theoretically, we consider different anatomical and functional factors that may contribute to the consistent anatomical location of place selectivity relative to the folding of high-level visual cortex.

Introduction

The parahippocampal place area (PPA) is a functional region of the brain that responds more strongly to images of scenes and places compared to other classes of visual stimuli and is critical for scene and place recognition, as well as navigation (Aguirre et al., 1998; Epstein and Kanwisher, 1998, Epstein, 2008). Typically, the PPA is defined from functional magnetic resonance imaging (fMRI) experiments. The PPA is located within a gross anatomical territory that contains several macroanatomical structures including the collateral sulcus (CoS), the lingual sulcus, (LS), and the parahippocampal gyrus (PHG; Aguirre et al., 1998, Avidan et al., 2002, Epstein, 2008, Epstein and Kanwisher, 1998, Levy et al., 2004, Nasr et al., 2011, Weiner and Grill-Spector, 2010, Weiner et al., 2010). These macranatomical structures span several centimeters, making it hard to precisely predict the exact location of place selectivity from cortical folding patterns alone, which was nicely summarized in a recent review (Epstein, 2014).1 A question remains whether it is possible to accurately identify the most probable location of these place-selective voxels without needing to acquire functional MRI data. Such a feat would be especially useful in patient populations and other participant groups in which it may be relatively easy to acquire anatomical data, but difficult to acquire functional data.

Of course, the identification of the PPA is complicated by (at least) four methodological considerations. First, the PPA definition may depend on the type of experiment, task, and stimuli used. Second, the boundaries of the PPA may depend on the statistical threshold used. Third, the spatial extent and localization of the PPA may vary if defined within the native brain space of an individual or based on a group analysis. Fourth, the size of the PPA may depend on data acquisition choices (e.g. large vs. small voxels) and data analysis choices (e.g. liberal smoothing vs. no spatial smoothing). The present study aims to identify and to predict the most probable location of place-selective voxels within medial VTC of an individual brain that is impervious to these methodological decisions.

To achieve this goal, the present study implemented a three-fold approach. First, we generated a probabilistic group ROI of place-selective voxels using cortex-based alignment (Fischl et al., 1999). Second, we quantified how well this probabilistic ROI predicts the location of the PPA, as well as place-selective fMRI responses, from an independent experiment and a separate set of participants. Third, we tested if this probabilistic ROI also captures the locus of highest place selectivity in (a) our data and (b) a separate set of data collected from over 500 participants by other researchers using different stimuli, tasks, and methods (shared from Nasr et al., 2014 and the Human Connectome Project, Barch et al., 2013).

The results from these analyses demonstrate that (a) the anatomical location of place-selective voxels relative to cortical folding is consistent across participants, (b) the probabilistic ROI identifies the location of the PPA in individual brains from multiple independent datasets, and (c) the probabilistic ROI encapsulates voxels in medial VTC exhibiting the highest place selectivity in our data as well as shared data from other labs. Our probabilistic ROI of place selectivity is freely available with this study aligned to the FreeSurfer average cortical surface (vpnl.stanford.edu/PlaceSelectivity).

Section snippets

Participants

To identify place-selective voxels, 12 adults (5 females) participated in fMRI Study 1 and 12 independent adults (8 females) participated in fMRI Study 2. Procedures were approved by the Stanford Internal Review Board on human participants research.

Functional localizer

12 adults participated in 4 runs of an fMRI functional localizer experiment (6 min/run; from Stigliani et al., 2015; http://vpnl.stanford.edu/fLoc/). Each run consisted of 16 s blocks, which contained different images from the same category presented

Place-selective voxels in medial VTC are located in the banks of the CoS with inter-subject variability

Our data illustrate that macroanatomical features create a reliable set of landmarks that confine place selectivity in medial ventral temporal cortex (VTC), which replicates and extends previous findings (Aguirre et al., 1998, Epstein and Kanwisher, 1998, Nasr et al., 2011, Nasr et al., 2014, Weiner et al., 2010, Weiner and Grill-Spector, 2010). For example, our data show that place-selective voxels are consistently located within the banks of the collateral sulcus (CoS) in individual

Discussion

In this study, we examined the relationship between cortical folding patterns and the most probable location of place selectivity in medial ventral temporal cortex (VTC). Our results show that cortical folding patterns and probabilistic predictions reliably identify place-selective voxels in medial VTC across individuals and experiments. Below, we discuss these findings in the context of (1) predicting functional regions from cortical folding across the visual hierarchy and (2)

Conclusion

The present study shows that the location of place-selective voxels in medial VTC relative to cortical folding is so consistent that it could be predicted from a probabilistic ROI generated from independent groups of participants. These findings extend recent results showing that cortical positions of high-level visual areas in the ventral temporal lobe are reliably arranged relative to the macroanatomy. Our results are important because they reveal regularities in the functional organization

Conflicts of interest

None.

Acknowledgements

Author contributions.

KW: designed the study, performed morphological analyses, defined fROIs in Study 1, generated pROIs, performed the statistical analyses, and wrote the manuscript.

MB: developed and implemented cortex based alignment tools, developed tools for the analytical pipeline across studies, and collected anatomical data used for morphological analyses.

NW, GG: collected data and defined fROIs from Study 2.

AS: collected data and defined fROIs from Study 1.

KNK: analyzed data from the

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