. 2015 Jun 12;348(6240):1241-4.

doi: 10.1126/science.1255905. Epub 2015 Jun 11.

BRAIN NETWORKS. Correlated gene expression supports synchronous activity in brain networks

Jonas Richiardi¹, Andre Altmann², Anna-Clare Milazzo³, Catie Chang⁴, M Mallar Chakravarty⁵, Tobias Banaschewski⁶, Gareth J Barker⁷, Arun L W Bokde⁸, Uli Bromberg⁹, Christian Büchel⁹, Patricia Conrod¹⁰, Mira Fauth-Bühler¹¹, Herta Flor¹², Vincent Frouin¹³, Jürgen Gallinat¹⁴, Hugh Garavan¹⁵, Penny Gowland¹⁶, Andreas Heinz¹⁴, Hervé Lemaître¹⁷, Karl F Mann¹¹, Jean-Luc Martinot¹⁷, Frauke Nees¹², Tomáš Paus¹⁸, Zdenka Pausova¹⁹, Marcella Rietschel²⁰, Trevor W Robbins²¹, Michael N Smolka²², Rainer Spanagel²³, Andreas Ströhle¹⁴, Gunter Schumann²⁴, Mike Hawrylycz²⁵, Jean-Baptiste Poline²⁶, Michael D Greicius²⁷; IMAGEN consortium

Collaborators, Affiliations

Collaborators

IMAGEN consortium:
Lisa Albrecht, Chris Andrew, Mercedes Arroyo, Eric Artiges, Semiha Aydin, Christine Bach, Tobias Banaschewski, Alexis Barbot, Gareth Barker, Nathalie Boddaert, Arun Bokde, Zuleima Bricaud, Uli Bromberg, Ruediger Bruehl, Christian Büchel, Arnaud Cachia, Anna Cattrell, Patricia Conrod, Patrick Constant, Jeffrey Dalley, Benjamin Decideur, Sylvane Desrivieres, Tahmine Fadai, Herta Flor, Vincent Frouin, Jürgen Gallinat, Hugh Garavan, Fanny Gollier Briand, Penny Gowland, Bert Heinrichs, Andreas Heinz, Nadja Heym, Thomas Hübner, James Ireland, Bernd Ittermann, Tianye Jia, Mark Lathrop, Dirk Lanzerath, Claire Lawrence, Hervé Lemaitre, Katharina Lüdemann, Christine Macare, Catherine Mallik, Jean-François Mangin, Karl Mann, Jean-Luc Martinot, Eva Mennigen, Fabiana Mesquita de Carvahlo, Xavier Mignon, Ruben Miranda, Kathrin Müller, Frauke Nees, Charlotte Nymberg, Marie-Laure Paillere, Tomas Paus, Zdenka Pausova, Jean-Baptiste Poline, Luise Poustka, Michael Rapp, Gabriel Robert, Jan Reuter, Marcella Rietschel, Stephan Ripke, Trevor Robbins, Sarah Rodehacke, John Rogers, Alexander Romanowski, Barbara Ruggeri, Christine Schmäl, Dirk Schmidt, Sophia Schneider, MarkGunter Schumann, Florian Schubert, Yannick Schwartz, Michael Smolka, Wolfgang Sommer, Rainer Spanagel, Claudia Speiser, Tade Spranger, Alicia Stedman, Sabina Steiner, Dai Stephens, Nicole Strache, Andreas Ströhle, Maren Struve, Naresh Subramaniam, Lauren Topper, Walter, Robert Whelan, Steve Williams, Juliana Yacubian, Monica Zilbovicius, C Peng Wong, Steven Lubbe, Lourdes Martinez-Medina, Alinda Fernandes, Amir Tahmasebi

Affiliations

¹ Functional Imaging in Neuropsychiatric Disorders Laboratory, Department of Neurology and Neurological Sciences, Stanford University, Stanford, CA, USA. Laboratory of Neurology and Imaging of Cognition, Department of Neuroscience, University of Geneva, Geneva, Switzerland. jonas.richiardi@unige.ch greicius@stanford.edu.
² Functional Imaging in Neuropsychiatric Disorders Laboratory, Department of Neurology and Neurological Sciences, Stanford University, Stanford, CA, USA.
³ The War Related Illness and Injury Study Center, VA Palo Alto Health Care System, Palo Alto, CA, USA. Functional Imaging in Neuropsychiatric Disorders Laboratory, Department of Neurology and Neurological Sciences, Stanford University, Stanford, CA, USA.
⁴ Advanced MRI Section, Laboratory of Functional and Molecular Imaging, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD, USA.
⁵ Cerebral Imaging Centre, Douglas Mental Health University Institute, Montreal, Canada. Departments of Psychiatry and Biomedical Engineering, McGill University, Montreal, Canada.
⁶ Department of Child and Adolescent Psychiatry, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.
⁷ Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.
⁸ Institute of Neuroscience, Trinity College Dublin, Dublin, Ireland.
⁹ Universitaetsklinikum Hamburg Eppendorf, Hamburg, Germany.
¹⁰ Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK. Department of Psychiatry, Université de Montréal, Centre Hospitalier Universitaire (CHU) Ste Justine Hospital, Montréal, Canada.
¹¹ Department of Addictive Behaviour and Addiction Medicine, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.
¹² Department of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.
¹³ Neurospin, Commissariat à l'Energie Atomique et aux Energies Alternatives, Paris, France.
¹⁴ Department of Psychiatry and Psychotherapy, Campus Charité Mitte, Charité-Universitätsmedizin Berlin, Berlin, Germany.
¹⁵ Institute of Neuroscience, Trinity College Dublin, Dublin, Ireland. Departments of Psychiatry and Psychology, University of Vermont, Burlington, VT, USA.
¹⁶ School of Physics and Astronomy, University of Nottingham, Nottingham, UK.
¹⁷ Institut National de la Santé et de la Recherche Médicale, INSERM Unit 1000 "Neuroimaging and Psychiatry," University Paris Sud, Orsay, France. INSERM Unit 1000 at Maison de Solenn, Assistance Publique Hôpitaux de Paris (APHP), Cochin Hospital, University Paris Descartes, Sorbonne Paris Cité, Paris, France.
¹⁸ Rotman Research Institute, University of Toronto, Toronto, Canada. School of Psychology, University of Nottingham, Nottingham, UK.
¹⁹ The Hospital for Sick Children, University of Toronto, Toronto, Canada.
²⁰ Department of Genetic Epidemiology in Psychiatry, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.
²¹ Behavioural and Clinical Neuroscience Institute and Department of Psychology, University of Cambridge, Cambridge, UK.
²² Department of Psychiatry and Psychotherapy, and Neuroimaging Center, Technische Universität Dresden, Dresden, Germany.
²³ Department of Psychopharmacology, Central Institute of Mental Health, Faculty of Clinical Medicine Mannheim, Mannheim, Germany.
²⁴ Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK. Medical Research Council (MRC) Social, Genetic and Developmental Psychiatry (SGDP) Centre, London, UK.
²⁵ Allen Institute for Brain Science, Seattle, WA, USA.
²⁶ Helen Wills Neuroscience Institute, University of California Berkeley, Berkeley, CA, USA.
²⁷ Functional Imaging in Neuropsychiatric Disorders Laboratory, Department of Neurology and Neurological Sciences, Stanford University, Stanford, CA, USA. jonas.richiardi@unige.ch greicius@stanford.edu.

PMID: 26068849
PMCID: PMC4829082
DOI: 10.1126/science.1255905

BRAIN NETWORKS. Correlated gene expression supports synchronous activity in brain networks

Jonas Richiardi et al. Science. 2015.

. 2015 Jun 12;348(6240):1241-4.

doi: 10.1126/science.1255905. Epub 2015 Jun 11.

Authors

Collaborators

IMAGEN consortium:
Lisa Albrecht, Chris Andrew, Mercedes Arroyo, Eric Artiges, Semiha Aydin, Christine Bach, Tobias Banaschewski, Alexis Barbot, Gareth Barker, Nathalie Boddaert, Arun Bokde, Zuleima Bricaud, Uli Bromberg, Ruediger Bruehl, Christian Büchel, Arnaud Cachia, Anna Cattrell, Patricia Conrod, Patrick Constant, Jeffrey Dalley, Benjamin Decideur, Sylvane Desrivieres, Tahmine Fadai, Herta Flor, Vincent Frouin, Jürgen Gallinat, Hugh Garavan, Fanny Gollier Briand, Penny Gowland, Bert Heinrichs, Andreas Heinz, Nadja Heym, Thomas Hübner, James Ireland, Bernd Ittermann, Tianye Jia, Mark Lathrop, Dirk Lanzerath, Claire Lawrence, Hervé Lemaitre, Katharina Lüdemann, Christine Macare, Catherine Mallik, Jean-François Mangin, Karl Mann, Jean-Luc Martinot, Eva Mennigen, Fabiana Mesquita de Carvahlo, Xavier Mignon, Ruben Miranda, Kathrin Müller, Frauke Nees, Charlotte Nymberg, Marie-Laure Paillere, Tomas Paus, Zdenka Pausova, Jean-Baptiste Poline, Luise Poustka, Michael Rapp, Gabriel Robert, Jan Reuter, Marcella Rietschel, Stephan Ripke, Trevor Robbins, Sarah Rodehacke, John Rogers, Alexander Romanowski, Barbara Ruggeri, Christine Schmäl, Dirk Schmidt, Sophia Schneider, MarkGunter Schumann, Florian Schubert, Yannick Schwartz, Michael Smolka, Wolfgang Sommer, Rainer Spanagel, Claudia Speiser, Tade Spranger, Alicia Stedman, Sabina Steiner, Dai Stephens, Nicole Strache, Andreas Ströhle, Maren Struve, Naresh Subramaniam, Lauren Topper, Walter, Robert Whelan, Steve Williams, Juliana Yacubian, Monica Zilbovicius, C Peng Wong, Steven Lubbe, Lourdes Martinez-Medina, Alinda Fernandes, Amir Tahmasebi

Affiliations

¹ Functional Imaging in Neuropsychiatric Disorders Laboratory, Department of Neurology and Neurological Sciences, Stanford University, Stanford, CA, USA. Laboratory of Neurology and Imaging of Cognition, Department of Neuroscience, University of Geneva, Geneva, Switzerland. jonas.richiardi@unige.ch greicius@stanford.edu.
² Functional Imaging in Neuropsychiatric Disorders Laboratory, Department of Neurology and Neurological Sciences, Stanford University, Stanford, CA, USA.
³ The War Related Illness and Injury Study Center, VA Palo Alto Health Care System, Palo Alto, CA, USA. Functional Imaging in Neuropsychiatric Disorders Laboratory, Department of Neurology and Neurological Sciences, Stanford University, Stanford, CA, USA.
⁴ Advanced MRI Section, Laboratory of Functional and Molecular Imaging, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD, USA.
⁵ Cerebral Imaging Centre, Douglas Mental Health University Institute, Montreal, Canada. Departments of Psychiatry and Biomedical Engineering, McGill University, Montreal, Canada.
⁶ Department of Child and Adolescent Psychiatry, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.
⁷ Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.
⁸ Institute of Neuroscience, Trinity College Dublin, Dublin, Ireland.
⁹ Universitaetsklinikum Hamburg Eppendorf, Hamburg, Germany.
¹⁰ Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK. Department of Psychiatry, Université de Montréal, Centre Hospitalier Universitaire (CHU) Ste Justine Hospital, Montréal, Canada.
¹¹ Department of Addictive Behaviour and Addiction Medicine, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.
¹² Department of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.
¹³ Neurospin, Commissariat à l'Energie Atomique et aux Energies Alternatives, Paris, France.
¹⁴ Department of Psychiatry and Psychotherapy, Campus Charité Mitte, Charité-Universitätsmedizin Berlin, Berlin, Germany.
¹⁵ Institute of Neuroscience, Trinity College Dublin, Dublin, Ireland. Departments of Psychiatry and Psychology, University of Vermont, Burlington, VT, USA.
¹⁶ School of Physics and Astronomy, University of Nottingham, Nottingham, UK.
¹⁷ Institut National de la Santé et de la Recherche Médicale, INSERM Unit 1000 "Neuroimaging and Psychiatry," University Paris Sud, Orsay, France. INSERM Unit 1000 at Maison de Solenn, Assistance Publique Hôpitaux de Paris (APHP), Cochin Hospital, University Paris Descartes, Sorbonne Paris Cité, Paris, France.
¹⁸ Rotman Research Institute, University of Toronto, Toronto, Canada. School of Psychology, University of Nottingham, Nottingham, UK.
¹⁹ The Hospital for Sick Children, University of Toronto, Toronto, Canada.
²⁰ Department of Genetic Epidemiology in Psychiatry, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.
²¹ Behavioural and Clinical Neuroscience Institute and Department of Psychology, University of Cambridge, Cambridge, UK.
²² Department of Psychiatry and Psychotherapy, and Neuroimaging Center, Technische Universität Dresden, Dresden, Germany.
²³ Department of Psychopharmacology, Central Institute of Mental Health, Faculty of Clinical Medicine Mannheim, Mannheim, Germany.
²⁴ Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK. Medical Research Council (MRC) Social, Genetic and Developmental Psychiatry (SGDP) Centre, London, UK.
²⁵ Allen Institute for Brain Science, Seattle, WA, USA.
²⁶ Helen Wills Neuroscience Institute, University of California Berkeley, Berkeley, CA, USA.
²⁷ Functional Imaging in Neuropsychiatric Disorders Laboratory, Department of Neurology and Neurological Sciences, Stanford University, Stanford, CA, USA. jonas.richiardi@unige.ch greicius@stanford.edu.

PMID: 26068849
PMCID: PMC4829082
DOI: 10.1126/science.1255905

Abstract

During rest, brain activity is synchronized between different regions widely distributed throughout the brain, forming functional networks. However, the molecular mechanisms supporting functional connectivity remain undefined. We show that functional brain networks defined with resting-state functional magnetic resonance imaging can be recapitulated by using measures of correlated gene expression in a post mortem brain tissue data set. The set of 136 genes we identify is significantly enriched for ion channels. Polymorphisms in this set of genes significantly affect resting-state functional connectivity in a large sample of healthy adolescents. Expression levels of these genes are also significantly associated with axonal connectivity in the mouse. The results provide convergent, multimodal evidence that resting-state functional networks correlate with the orchestrated activity of dozens of genes linked to ion channel activity and synaptic function.

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Figures

**Fig. 1. Functional networks in MRI and gene expression data**
(A) The four functional networks of interest. Red, dorsal default mode; yellow, salience; green, visuospatial; blue, sensorimotor. (B) AIBS brain samples assigned to their corresponding functional network. Solid circles are samples assigned to the four networks of interest, open circles show samples in the nine other networks, and dots show non-network AIBS samples.

**Fig. 2. In vivo functional connectivity differences related to the consensus gene list**
Difference in in vivo functional connectivity between the averages of the top 20 and the bottom 20 subjects in IMAGEN, ranked by genotype score with respect to the consensus list of genes. (A) Difference matrix sorted by functional network (correlation differences smaller than |0.05| are not shown). Positive values indicate connections that are stronger in high genotype score subjects, and negative values indicate the opposite. Connections are mostly increased within functional networks, but also between some functional networks. (B) MNI space sagittal view of within-network connections that are stronger in high-genotype-score subjects. Regions (disks) are coded according to the functional network they belong to: red, dorsal default mode; yellow, salience; green, visuospatial; blue, sensorimotor. Connections (lines) are color-coded to their functional networks. (C) Same, for connections that are stronger in low-genotype-score subjects. The majority of connections are strengthened in high-genotype-score subjects.

**Fig. 3. Mouse mesoscale connectivity and transcriptional similarity**
(A) Mouse isocortex parcellated into 38 regions (23). (B) Corresponding symmetrized, thresholded, and normalized ipsilateral axonal connectivity weights. (C) Transcriptional similarity (genetic correlation), using our consensus list of genes.

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BRAIN NETWORKS. Correlated gene expression supports synchronous activity in brain networks

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