Functional parcellation of human and macaque striatum reveals human-specific connectivity in the dorsal caudate
Xiaojin Liu,
Simon B. Eickhoff,
Svenja Caspers,
Jianxiao Wu,
Sarah Genon,
Felix Hoffstaedter,
Rogier B. Mars,
Iris E. Sommer,
Claudia R. Eickhoff,
Ji Chen,
Renaud Jardri,
Kathrin Reetz,
Imis Dogan,
André Aleman,
Lydia Kogler,
Oliver Gruber,
Julian Caspers,
Christian Mathys,
Kaustubh R. Patil
Affiliations
Xiaojin Liu
Institute of Neuroscience and Medicine (INM-7), Heinrich Heine University Düsseldorf, Düsseldorf, Germany; Institute of Systems Neuroscience, Research Centre Jülich, Jülich, Germany
Simon B. Eickhoff
Institute of Neuroscience and Medicine (INM-7), Heinrich Heine University Düsseldorf, Düsseldorf, Germany; Institute of Systems Neuroscience, Research Centre Jülich, Jülich, Germany
Svenja Caspers
Institute of Neuroscience and Medicine (INM-1), Research Centre Jülich, Jülich, Germany; Institute for Anatomy I, Medical Faculty, Heinrich Heine University Düsseldorf, Düsseldorf, Germany
Jianxiao Wu
Institute of Neuroscience and Medicine (INM-7), Heinrich Heine University Düsseldorf, Düsseldorf, Germany; Institute of Systems Neuroscience, Research Centre Jülich, Jülich, Germany
Sarah Genon
Institute of Neuroscience and Medicine (INM-7), Heinrich Heine University Düsseldorf, Düsseldorf, Germany; Institute of Systems Neuroscience, Research Centre Jülich, Jülich, Germany
Felix Hoffstaedter
Institute of Neuroscience and Medicine (INM-7), Heinrich Heine University Düsseldorf, Düsseldorf, Germany; Institute of Systems Neuroscience, Research Centre Jülich, Jülich, Germany
Rogier B. Mars
Wellcome Centre for Integrative Neuroimaging, Centre for Functional MRI of the Brain (FMRIB), Nuffield Department of Clinical Neurosciences, John Radcliffe Hospital, University of Oxford, Oxford, United Kingdom; Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Nijmegen, Netherlands
Iris E. Sommer
Department of Biomedical Sciences of Cells & Systems, University Medical Center Groningen, Groningen, Netherlands
Claudia R. Eickhoff
Institute of Neuroscience and Medicine (INM-1), Research Centre Jülich, Jülich, Germany; Institute of Clinical Neuroscience and Medical Psychology, Medical Faculty, University of Düsseldorf, Düsseldorf, Germany
Ji Chen
Institute of Neuroscience and Medicine (INM-7), Heinrich Heine University Düsseldorf, Düsseldorf, Germany; Institute of Systems Neuroscience, Research Centre Jülich, Jülich, Germany
Renaud Jardri
Division of Psychiatry, University of Lille, CNRS UMR9193, SCALab & CHU Lille, Fontan Hospital, CURE platform, Lille, France
Kathrin Reetz
JARA-BRAIN Institute Molecular Neuroscience and Neuroimaging, Forschungszentrum Jülich, RWTH Aachen University, Aachen, Germany; Department of Neurology, RWTH Aachen University, Aachen, Germany
Imis Dogan
JARA-BRAIN Institute Molecular Neuroscience and Neuroimaging, Forschungszentrum Jülich, RWTH Aachen University, Aachen, Germany; Department of Neurology, RWTH Aachen University, Aachen, Germany
André Aleman
Department of Neuroscience, University Medical Center Groningen, University of Groningen, Groningen, Netherlands
Lydia Kogler
Department of Psychiatry and Psychotherapy, Medical School, University of Tübingen, Germany
Oliver Gruber
Section for Experimental Psychopathology and Neuroimaging, Department of General Psychiatry, Heidelberg University, Germany
Julian Caspers
Institute of Neuroscience and Medicine (INM-1), Research Centre Jülich, Jülich, Germany; Department of Diagnostic and Interventional Radiology, Medical Faculty, University of Düsseldorf, Düsseldorf, Germany
Christian Mathys
Department of Diagnostic and Interventional Radiology, Medical Faculty, University of Düsseldorf, Düsseldorf, Germany; Research Center Neurosensory Science, Carl von Ossietzky Universität Oldenburg, Oldenburg, Germany; Institute of Radiology and Neuroradiology, Evangelisches Krankenhaus, University of Oldenburg, Oldenburg, Germany
Kaustubh R. Patil
Institute of Neuroscience and Medicine (INM-7), Heinrich Heine University Düsseldorf, Düsseldorf, Germany; Institute of Systems Neuroscience, Research Centre Jülich, Jülich, Germany; Corresponding author.
A wide homology between human and macaque striatum is often assumed as in both the striatum is involved in cognition, emotion and executive functions. However, differences in functional and structural organization between human and macaque striatum may reveal evolutionary divergence and shed light on human vulnerability to neuropsychiatric diseases. For instance, dopaminergic dysfunction of the human striatum is considered to be a pathophysiological underpinning of different disorders, such as Parkinson's disease (PD) and schizophrenia (SCZ). Previous investigations have found a wide similarity in structural connectivity of the striatum between human and macaque, leaving the cross-species comparison of its functional organization unknown. In this study, resting-state functional connectivity (RSFC) derived striatal parcels were compared based on their homologous cortico-striatal connectivity. The goal here was to identify striatal parcels whose connectivity is human-specific compared to macaque parcels. Functional parcellation revealed that the human striatum was split into dorsal, dorsomedial, and rostral caudate and ventral, central, and caudal putamen, while the macaque striatum was divided into dorsal, and rostral caudate and rostral, and caudal putamen. Cross-species comparison indicated dissimilar cortico-striatal RSFC of the topographically similar dorsal caudate. We probed clinical relevance of the striatal clusters by examining differences in their cortico-striatal RSFC and gray matter (GM) volume between patients (with PD and SCZ) and healthy controls. We found abnormal RSFC not only between dorsal caudate, but also between rostral caudate, ventral, central and caudal putamen and widespread cortical regions for both PD and SCZ patients. Also, we observed significant structural atrophy in rostral caudate, ventral and central putamen for both PD and SCZ while atrophy in the dorsal caudate was specific to PD. Taken together, our cross-species comparative results revealed shared and human-specific RSFC of different striatal clusters reinforcing the complex organization and function of the striatum. In addition, we provided a testable hypothesis that abnormalities in a region with human-specific connectivity, i.e., dorsal caudate, might be associated with neuropsychiatric disorders.
