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Functional corticostriatal connection topographies predict goal-directed behaviour in humans

Nature Human Behaviour volume 1, Article number: 0146 (2017) Cite this article

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Abstract

Anatomical tracing studies in non-human primates have suggested that corticostriatal connectivity is topographically organized: nearby locations in striatum are connected with nearby locations in cortex. The topographic organization of corticostriatal connectivity is thought to underpin many goal-directed behaviours, but these topographies have not been completely characterized in humans and their relationship to uniquely human behaviours remains to be fully determined. Instead, the dominant approach employs parcellations that cannot model the continuous nature of the topography, nor accommodate overlapping cortical projections in the striatum. Here we employ a different approach to studying human corticostriatal circuitry: we estimate smoothly varying and spatially overlapping ‘connection topographies’ from resting-state functional magnetic resonance imaging. These correspond exceptionally well with and extend the topographies predicted from primate tracing studies. We show that striatal topography is preserved in regions not previously known to have topographic connections with the striatum and that many goal-directed behaviours can be mapped precisely onto individual variations in the spatial layout of striatal connectivity.

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Figure 1: Summary of the analysis pipeline.
Figure 2: Correspondence with previous studies in animal models.
Figure 3: Relative importance of different variables in driving the multivariate correspondence between the topography from the left striatum and the behavioural set (derived from all 466 subjects used in the analysis).
Figure 4: Relative importance of different variables in driving the multivariate correspondence between the topography from the right striatum and the behavioural set (derived from all 466 subjects used in the analysis).

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Acknowledgements

We acknowledge support from The Netherlands Organization for Scientific Research (NWO) by VIDI grants to A.F.M. (grant no. 016.156.415) and C.F.B. (864.12.003), a VENI grant to K.V.H. (016.171.068) and under the Gravitation Programme (024.001.006 supporting A.F.M.). We also acknowledge funding from the Wellcome Trust UK Strategic Award (098369/Z/12/Z). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Author notes

  1. Andre F. Marquand and Koen V. Haak: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Cognitive Neuroscience, Radboud University Medical Centre, Kapittelweg 29, , Nijmegen, 6525 EN, The Netherlands

    Andre F. Marquand, Koen V. Haak & Christian F. Beckmann

  2. Donders Centre for Cognitive Neuroimaging, Donders Institute for Brain, Cognition and Behaviour, Kapittelweg 29, , Nijmegen, 6525 EN, The Netherlands

    Andre F. Marquand, Koen V. Haak & Christian F. Beckmann

  3. Department of Neuroimaging, Centre for Neuroimaging Sciences, Institute of Psychiatry, King’s College London, De Crespigny Park, London, SE5 8AF, UK

    Andre F. Marquand

  4. Oxford Centre for Functional Magnetic Resonance Imaging of the Brain (FMRIB), University of Oxford, Oxford, OX3 9DU, UK

    Christian F. Beckmann

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Contributions

A.F.M., K.V.H. and C.F.B. devised the experiments, A.F.M. and K.V.H. analysed the data and all authors wrote the manuscript.

Corresponding author

Correspondence to Andre F. Marquand.

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Competing interests

C.F.B. is director of and shareholder in SBGNeuro Ltd. The other authors declare no competing interests.

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Supplementary Methods, Supplementary Figures 1–5, Supplementary References

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Marquand, A., Haak, K. & Beckmann, C. Functional corticostriatal connection topographies predict goal-directed behaviour in humans. Nat Hum Behav 1, 0146 (2017). https://doi.org/10.1038/s41562-017-0146

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