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Anchoring the neural compass: coding of local spatial reference frames in human medial parietal lobe

A Corrigendum to this article was published on 26 May 2015

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Abstract

The neural systems that code for location and facing direction during spatial navigation have been investigated extensively; however, the mechanisms by which these quantities are referenced to external features of the world are not well understood. To address this issue, we examined behavioral priming and functional magnetic resonance imaging activity patterns while human subjects recalled spatial views from a recently learned virtual environment. Behavioral results indicated that imagined location and facing direction were represented during this task, and multivoxel pattern analyses indicated that the retrosplenial complex (RSC) was the anatomical locus of these spatial codes. Critically, in both cases, location and direction were defined on the basis of fixed elements of the local environment and generalized across geometrically similar local environments. These results suggest that RSC anchors internal spatial representations to local topographical features, thus allowing us to stay oriented while we navigate and retrieve from memory the experience of being in a particular place.

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Figure 1: Map and images of the virtual environment.
Figure 2: Summary of the analysis scheme.
Figure 3: Behavioral priming for facing direction and location in experiment 1.
Figure 4: Coding of facing direction and location in RSC activation patterns in experiment 2.
Figure 5: Visualization of pattern similarities in RSC.
Figure 6: Multivoxel patterns in RSC contain sufficient information about the spatial relations between views to reconstruct the spatial organization of the environment.
Figure 7: Whole-brain searchlight analysis of multivoxel coding of local direction.

Change history

  • 12 January 2015

    In the version of this article initially published, three citations present in an earlier draft were omitted. To correct this, the following sentence and phrase have been inserted in the first paragraph of the Results section "Whole-brain analyses," before the third sentence and at the end of the fourth, respectively: "This locus is just posterior to retrosplenial cortex proper (Brodmann area 29/30), which has been previously implicated in the coding of spatially fixed objects59." "..., an area that has been previously implicated in the coding of directional information60,61." In the sentence before these inserts, the corresponding description "and just posterior to the retrosplenial cortex proper" has been deleted. The references are as follows: 59. Auger, S.D. & Maguire, E.A. Assessing the mechanism of response in the retrosplenial cortex of good and poor navigators. Cortex 49, 2904–2913 (2013). 60. Schindler, A. & Bartels, A. Parietal cortex codes for egocentric space beyond the field of view. Curr. Biol. 23, 177–182 (2013). 61. Spiers, H.J. & Maguire, E.A. A navigational guidance system in the human brain. Hippocampus 17, 618–626 (2007). The error has been corrected in the HTML and PDF versions of the article.

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Acknowledgements

This research was supported by the US National Institutes of Health (EY022350) and the National Science Foundation (SBE-0541957 and SBE-1041707). We thank A. Stigliani for assistance with data collection and three anonymous referees for useful comments on an earlier version of the manuscript.

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Authors

Contributions

S.A.M., L.K.V. and R.A.E. designed the experiments. S.A.M. and J.R. collected the data. S.A.M. analyzed data with input from L.K.V. and R.A.E. S.A.M. and R.A.E. wrote the manuscript.

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Correspondence to Steven A Marchette.

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The authors declare no competing financial interests.

Integrated supplementary information

Supplementary Figure 1 Reaction time as a function of local direction in experiments 1 and 2.

A. Reaction times in Experiment 1 were faster for imagined views facing the back wall of the museums (local North) than for imagined views facing other directions. Repeated-measures ANOVA revealed a main effect of local direction of the imagined heading, F(3,63) = 8.221, p = 0.0001, and a post-hoc contrast [−3 for the back wall, 1 1 1 for the other directions] confirmed that participants were reliably faster when imagining facing the back wall of the museum compared to the other directions, F(1, 21) = 23.196, p = 0.000008. B. Reaction times in Experiment 2 were faster for imagined views facing the back wall of the museums (local North) than for imagined views facing other directions. Repeated-measures ANOVA revealed a main effect of local direction of the imagined heading, F(3,69) = 11.865, p = 0.000002, and a post-hoc contrast [–3 for the back wall, 1 1 1 for the other directions] confirmed that participants were reliably faster when imagining facing the back wall of the museum compared to the other directions, F(1,23) = 14.077, p = 0.0004. Error bars in both panels indicate standard error of the mean.

Supplementary Figure 2 Decoding of facing direction and location from fMRI activity patterns in the left superior parietal lobe (SPL).

A. Decoding of local direction in left SPL. Left panel. Pattern similarity between views that face the same direction in local space (black bars) was greater than pattern similarity between views that face different local direction (gray bars), (F(1,23) = 27.881, p = 0.00002). There was no main effect of museum, F(1,23) = 1.114, p = 0.302, and local direction did not interact with museum, F(1,23) = 2.359, p = 0.135. Right panel. Residual coding of global direction in left SPL. Pattern similarity was greater for views in different museums that faced the same global but different local directions than for views in different museums that faced different directions in both reference frames (t(23) = 2.349, p = 0.028). B. Decoding of location defined in the local reference frame in SPL. Left panel. Average pattern similarity between views in the same or geometrically-equivalent corners (black bars) was greater than average pattern similarity between views in different corners (gray bars) (F(1,23) = 8.429, p = 0.008). There was no main effect of museum, F(1,23) = 1.524, p = 0.230, and local location did not interact with museum, F(1,23) = 1.840, p = 0.188. Right panel. Absence of residual coding of location in the global reference frame in left SPL. Pattern similarity in SPL was no greater for views in different museums that were in equivalent locations as defined by the global reference frame than for views that did not share location in either the global or local reference frames (t(23) = 1.191, p = 0.245). Error bars in both panels indicate standard error of the mean.

Supplementary Figure 3 Decoding of facing direction from fMRI activity patterns in other functionally and anatomically defined regions of interest.

Decoding of local direction within parahippocampal place area (PPA), occipital place area (OPA/TOS), early visual cortex (EVC), hippocampus, and pre-subiculum. Pattern similarity between views that face the same direction in local space was only marginally greater than pattern similarity between views that face different local directions in the PPA and OPA/TOS (PPA: F(1,23) = 4.247, p = 0.051; OPA/TOS: F(1,23) = 3.463, p = 0.076), while EVC, presubiculum and hippocampus showed no evidence of direction coding (all ps > 0.38). In addition, patterns of activity in OPA/TOS and EVC contained sufficient information to decode the identity of the museum (OPA/TOS: F(1,23) = 5.175, p = 0.033; EVC: F(1,23) = 6.481, p = 0.018), while patterns of activity in PPA, presubiculum, and hippocampus did not (all ps > 0.16). We did not observe interactions between museum and direction coding in any of these regions (all ps > 0.13). In a previous experiment, we observed robust evidence of direction coding within the presubiculum when participants viewed familiar scenes from their college campus4. There are at least four differences between the two studies that could potentially explain this discrepancy. First, differences in task: in the previous experiment participants viewed scenes and reported which (canonical) direction they faced in the world, whereas in our current experiment participants viewed words and never explicitly reported their own heading. Second, differences in environmental familiarity: it may be that more extensive training, or training with both idiothetic and allothetic inputs, is necessary for the presubiculum to engage during memory recall. Third, the number of distinct problems that subjects had to solve was smaller in the earlier experiment (16 problems repeated 17 times each) than in the current experiment (96 problems repeated 5 or 6 times); as such, subjects in the earlier experiment may have relied more heavily on episodic memory to re-create the spatial codes retrieved on earlier trials leading to greater presubicular involvement. Finally, the voxel size was larger in the current experiment (3×3×3 mm) compared to the earlier experiment (3×3×2 mm) which might have made presubicular activity patterns more difficult to discern in the current case.

Supplementary Figure 4 Decoding of location from fMRI activity patterns in other functionally and anatomically defined regions of interest.

Decoding of location within parahippocampal place area (PPA), occipital place area (OPA/TOS), early visual cortex (EVC), hippocampus, and pre-subiculum. Pattern similarity between views in the same or geometrically-equivalent corners was not reliably greater than pattern similarity between views in different corners in any of these ROIs (all ps > 0.22). Main effects of museum were observed in OPA/TOS (F(1,23) = 5.151, p = 0.033) and EVC (F(1,23) = 7.311, p = 0.013) but not in PPA, presubiculum, or hippocampus (all ps > 0.70). We observed no interactions between location and museum in any of these regions (all ps > 0.19). Error bars in both panels indicate standard error of the mean.

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Marchette, S., Vass, L., Ryan, J. et al. Anchoring the neural compass: coding of local spatial reference frames in human medial parietal lobe. Nat Neurosci 17, 1598–1606 (2014). https://doi.org/10.1038/nn.3834

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