Functional corticostriatal connection topographies predict goal directed behaviour in humans

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.

[1]  G. Salmon,et al.  Attention deficit hyperactivity disorder. , 2018, British journal of hospital medicine.

[2]  Koen V. Haak,et al.  Connectopic mapping with resting-state fMRI , 2016, NeuroImage.

[3]  G. V. Van Hoesen,et al.  Widespread corticostriate projections from temporal cortex of the rhesus monkey , 1981, The Journal of comparative neurology.

[4]  Essa Yacoub,et al.  The WU-Minn Human Connectome Project: An overview , 2013, NeuroImage.

[5]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

[6]  Marisa O. Hollinshead,et al.  The organization of the human cerebral cortex estimated by intrinsic functional connectivity. , 2011, Journal of neurophysiology.

[7]  S. Haber,et al.  Estimates of Projection Overlap and Zones of Convergence within Frontal-Striatal Circuits , 2014, The Journal of Neuroscience.

[8]  A. Gelfand,et al.  Handbook of spatial statistics , 2010 .

[9]  O. Hikosaka,et al.  Reward-dependent spatial selectivity of anticipatory activity in monkey caudate neurons. , 2002, Journal of neurophysiology.

[10]  D. Ilstrup,et al.  A Double-blind, Placebo-Controlled Study , 2017 .

[11]  K. Doya,et al.  Representation of Action-Specific Reward Values in the Striatum , 2005, Science.

[12]  S. Leh,et al.  Fronto-striatal connections in the human brain: A probabilistic diffusion tractography study , 2007, Neuroscience Letters.

[13]  Ludovica Griffanti,et al.  Automatic denoising of functional MRI data: Combining independent component analysis and hierarchical fusion of classifiers , 2014, NeuroImage.

[14]  P. Mahadevan,et al.  An overview , 2007, Journal of Biosciences.

[15]  R. Badgaiyan Dopamine is released in the striatum during human emotional processing , 2010, Neuroreport.

[16]  Angelo Antonini,et al.  Pathological gambling in patients with Parkinson's disease is associated with fronto‐striatal disconnection: A path modeling analysis , 2011, Movement disorders : official journal of the Movement Disorder Society.

[17]  Suzanne N. Haber,et al.  Corticostriatal circuitry , 2016, Dialogues in clinical neuroscience.

[18]  Kristina M. Visscher,et al.  The neural bases of momentary lapses in attention , 2006, Nature Neuroscience.

[19]  S. Haber,et al.  Defining the Caudal Ventral Striatum in Primates: Cellular and Histochemical Features , 2002, The Journal of Neuroscience.

[20]  Mikhail Belkin,et al.  Laplacian Eigenmaps and Spectral Techniques for Embedding and Clustering , 2001, NIPS.

[21]  D. Pandya,et al.  Corticostriatal connections of the superior temporal region in rhesus monkeys , 1998, The Journal of comparative neurology.

[22]  P. Maclean CEREBRAL EVOLUTION AND EMOTIONAL PROCESSES: NEW FINDINGS ON THE STRIATAL COMPLEX , 1972, Annals of the New York Academy of Sciences.

[23]  B. Balleine,et al.  The Role of the Dorsal Striatum in Reward and Decision-Making , 2007, The Journal of Neuroscience.

[24]  N. Volkow,et al.  Dopamine Transporters in Striatum Correlate with Deactivation in the Default Mode Network during Visuospatial Attention , 2009, PloS one.

[25]  Christian F. Doeller,et al.  Functional topography of the human entorhinal cortex , 2015, eLife.

[26]  Richard S. J. Frackowiak,et al.  Evidence for Segregated and Integrative Connectivity Patterns in the Human Basal Ganglia , 2008, The Journal of Neuroscience.

[27]  E. Yeterian,et al.  Cortico-striate projections in the rhesus monkey: The organization of certain cortico-caudate connections , 1978, Brain Research.

[28]  Stefan Haufe,et al.  On the interpretation of weight vectors of linear models in multivariate neuroimaging , 2014, NeuroImage.

[29]  B. Greenberg,et al.  Deep Brain Stimulation for Intractable Obsessive Compulsive Disorder: Pilot Study Using a Blinded, Staggered-Onset Design , 2010, Biological Psychiatry.

[30]  S. Haber,et al.  Reward-Related Cortical Inputs Define a Large Striatal Region in Primates That Interface with Associative Cortical Connections, Providing a Substrate for Incentive-Based Learning , 2006, The Journal of Neuroscience.

[31]  A. Hariri,et al.  Preference for Immediate over Delayed Rewards Is Associated with Magnitude of Ventral Striatal Activity , 2006, The Journal of Neuroscience.

[32]  Mark Jenkinson,et al.  The minimal preprocessing pipelines for the Human Connectome Project , 2013, NeuroImage.

[33]  Nikolaus R. McFarland,et al.  Striatonigrostriatal Pathways in Primates Form an Ascending Spiral from the Shell to the Dorsolateral Striatum , 2000, The Journal of Neuroscience.

[34]  G. Marcus,et al.  The topographic brain: from neural connectivity to cognition , 2007, Trends in Neurosciences.

[35]  Y. Agid,et al.  Delayed response tasks in basal ganglia lesions in man: Further evidence for a striato-frontal cooperation in behavioural adaptation , 1996, Neuropsychologia.

[36]  G. E. Alexander,et al.  Parallel organization of functionally segregated circuits linking basal ganglia and cortex. , 1986, Annual review of neuroscience.

[37]  Wolfgang M. Pauli,et al.  Regional specialization within the human striatum for diverse psychological functions , 2016, Proceedings of the National Academy of Sciences.

[38]  Stephen M. Smith,et al.  Multi-level block permutation , 2015, NeuroImage.

[39]  John D. Storey,et al.  Empirical Bayes Analysis of a Microarray Experiment , 2001 .

[40]  B. Biswal,et al.  Functional connectivity of human striatum: a resting state FMRI study. , 2008, Cerebral cortex.

[41]  R. Buckner,et al.  The organization of the human striatum estimated by intrinsic functional connectivity. , 2012, Journal of neurophysiology.

[42]  C. Kelly,et al.  L-Dopa Modulates Functional Connectivity in Striatal Cognitive and Motor Networks: A Double-Blind Placebo-Controlled Study , 2009, NeuroImage.

[43]  T. Verstynen,et al.  Converging Structural and Functional Connectivity of Orbitofrontal, Dorsolateral Prefrontal, and Posterior Parietal Cortex in the Human Striatum , 2014, The Journal of Neuroscience.

[44]  Nasser M. Nasrabadi,et al.  Pattern Recognition and Machine Learning , 2006, Technometrics.

[45]  Kim F. Nimon,et al.  Tools to Support Interpreting Multiple Regression in the Face of Multicollinearity , 2012, Front. Psychology.

[46]  R Cameron Craddock,et al.  A whole brain fMRI atlas generated via spatially constrained spectral clustering , 2012, Human brain mapping.

[47]  Timothy E. J. Behrens,et al.  The topographic connectome , 2013, Current Opinion in Neurobiology.

[48]  Abraham Z. Snyder,et al.  Function in the human connectome: Task-fMRI and individual differences in behavior , 2013, NeuroImage.

[49]  David Badre,et al.  Microstructural organizational patterns in the human corticostriatal system. , 2012, Journal of neurophysiology.

[50]  T. Powell,et al.  The connexions of the striatum and globus pallidus: synthesis and speculation. , 1971, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[51]  S. Haber The primate basal ganglia: parallel and integrative networks , 2003, Journal of Chemical Neuroanatomy.

[52]  S. Haber,et al.  The Reward Circuit: Linking Primate Anatomy and Human Imaging , 2010, Neuropsychopharmacology.

[53]  P. Goldman-Rakic,et al.  Longitudinal topography and interdigitation of corticostriatal projections in the rhesus monkey , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[54]  Michael X. Cohen,et al.  Connectivity-based segregation of the human striatum predicts personality characteristics , 2009, Nature Neuroscience.

[55]  Michael X. Cohen,et al.  Connectivity-based segregation of the human striatum predicts personality characteristics , 2009, Nature Neuroscience.

[56]  Mark W. Woolrich,et al.  Network modelling methods for FMRI , 2011, NeuroImage.

[57]  Thomas E. Nichols,et al.  A positive-negative mode of population covariation links brain connectivity, demographics and behavior , 2015, Nature Neuroscience.

[58]  Kalina Christoff,et al.  Localizing the rostrolateral prefrontal cortex at the individual level , 2007, NeuroImage.