Neuroepigenetic signatures of age and sex in the living human brain
Abstract
Abstract Age- and sex-related alterations in gene transcription have been demonstrated, however the underlying mechanisms are unresolved. Neuroepigenetic pathways regulate gene transcription in the brain. Here, we measure in vivo expression of the epigenetic enzymes, histone deacetylases (HDACs), across healthy human aging and between sexes using [ 11 C]Martinostat positron emission tomography (PET) neuroimaging ( n = 41). Relative HDAC expression increases with age in cerebral white matter, and correlates with age-associated disruptions in white matter microstructure. A post mortem study confirmed that HDAC1 and HDAC2 paralogs are elevated in white matter tissue from elderly donors. There are also sex-specific in vivo HDAC expression differences in brain regions associated with emotion and memory, including the amygdala and hippocampus. Hippocampus and white matter HDAC expression negatively correlates with emotion regulation skills ( n = 23). Age and sex are associated with HDAC expression in vivo, which could drive age- and sex-related transcriptional changes and impact human behavior.
- Authors:
- more »
- Publication Date:
- Research Org.:
- Massachusetts General Hospital, Boston, MA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC); National Institute on Drug Abuse; National Institute of Mental Health; American Federation for Aging Research (AFAR)
- OSTI Identifier:
- 1619532
- Alternate Identifier(s):
- OSTI ID: 1611049
- Grant/Contract Number:
- SC0008430
- Resource Type:
- Published Article
- Journal Name:
- Nature Communications
- Additional Journal Information:
- Journal Name: Nature Communications Journal Volume: 10 Journal Issue: 1; Journal ID: ISSN 2041-1723
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United Kingdom
- Language:
- English
- Subject:
- 60 APPLIED LIFE SCIENCES; Science & Technology - Other Topics
Citation Formats
Gilbert, Tonya M., Zürcher, Nicole R., Catanese, Mary C., Tseng, Chieh-En J., Di Biase, Maria A., Lyall, Amanda E., Hightower, Baileigh G., Parmar, Anjali J., Bhanot, Anisha, Wu, Christine J., Hibert, Matthew L., Kim, Minhae, Mahmood, Umar, Stufflebeam, Steven M., Schroeder, Frederick A., Wang, Changning, Roffman, Joshua L., Holt, Daphne J., Greve, Douglas N., Pasternak, Ofer, Kubicki, Marek, Wey, Hsiao-Ying, and Hooker, Jacob M. Neuroepigenetic signatures of age and sex in the living human brain. United Kingdom: N. p., 2019.
Web. doi:10.1038/s41467-019-11031-0.
Gilbert, Tonya M., Zürcher, Nicole R., Catanese, Mary C., Tseng, Chieh-En J., Di Biase, Maria A., Lyall, Amanda E., Hightower, Baileigh G., Parmar, Anjali J., Bhanot, Anisha, Wu, Christine J., Hibert, Matthew L., Kim, Minhae, Mahmood, Umar, Stufflebeam, Steven M., Schroeder, Frederick A., Wang, Changning, Roffman, Joshua L., Holt, Daphne J., Greve, Douglas N., Pasternak, Ofer, Kubicki, Marek, Wey, Hsiao-Ying, & Hooker, Jacob M. Neuroepigenetic signatures of age and sex in the living human brain. United Kingdom. https://doi.org/10.1038/s41467-019-11031-0
Gilbert, Tonya M., Zürcher, Nicole R., Catanese, Mary C., Tseng, Chieh-En J., Di Biase, Maria A., Lyall, Amanda E., Hightower, Baileigh G., Parmar, Anjali J., Bhanot, Anisha, Wu, Christine J., Hibert, Matthew L., Kim, Minhae, Mahmood, Umar, Stufflebeam, Steven M., Schroeder, Frederick A., Wang, Changning, Roffman, Joshua L., Holt, Daphne J., Greve, Douglas N., Pasternak, Ofer, Kubicki, Marek, Wey, Hsiao-Ying, and Hooker, Jacob M. Wed .
"Neuroepigenetic signatures of age and sex in the living human brain". United Kingdom. https://doi.org/10.1038/s41467-019-11031-0.
@article{osti_1619532,
title = {Neuroepigenetic signatures of age and sex in the living human brain},
author = {Gilbert, Tonya M. and Zürcher, Nicole R. and Catanese, Mary C. and Tseng, Chieh-En J. and Di Biase, Maria A. and Lyall, Amanda E. and Hightower, Baileigh G. and Parmar, Anjali J. and Bhanot, Anisha and Wu, Christine J. and Hibert, Matthew L. and Kim, Minhae and Mahmood, Umar and Stufflebeam, Steven M. and Schroeder, Frederick A. and Wang, Changning and Roffman, Joshua L. and Holt, Daphne J. and Greve, Douglas N. and Pasternak, Ofer and Kubicki, Marek and Wey, Hsiao-Ying and Hooker, Jacob M.},
abstractNote = {Abstract Age- and sex-related alterations in gene transcription have been demonstrated, however the underlying mechanisms are unresolved. Neuroepigenetic pathways regulate gene transcription in the brain. Here, we measure in vivo expression of the epigenetic enzymes, histone deacetylases (HDACs), across healthy human aging and between sexes using [ 11 C]Martinostat positron emission tomography (PET) neuroimaging ( n = 41). Relative HDAC expression increases with age in cerebral white matter, and correlates with age-associated disruptions in white matter microstructure. A post mortem study confirmed that HDAC1 and HDAC2 paralogs are elevated in white matter tissue from elderly donors. There are also sex-specific in vivo HDAC expression differences in brain regions associated with emotion and memory, including the amygdala and hippocampus. Hippocampus and white matter HDAC expression negatively correlates with emotion regulation skills ( n = 23). Age and sex are associated with HDAC expression in vivo, which could drive age- and sex-related transcriptional changes and impact human behavior.},
doi = {10.1038/s41467-019-11031-0},
journal = {Nature Communications},
number = 1,
volume = 10,
place = {United Kingdom},
year = {2019},
month = {7}
}
https://doi.org/10.1038/s41467-019-11031-0
Web of Science
Works referenced in this record:
Histone Deacetylase Inhibitors Preserve White Matter Structure and Function during Ischemia by Conserving ATP and Reducing Excitotoxicity
journal, March 2011
- Baltan, S.; Murphy, S. P.; Danilov, C. A.
- Journal of Neuroscience, Vol. 31, Issue 11
Dysregulation of the epigenetic landscape of normal aging in Alzheimer’s disease
journal, March 2018
- Nativio, Raffaella; Donahue, Greg; Berson, Amit
- Nature Neuroscience, Vol. 21, Issue 4
Permutation inference for the general linear model
journal, May 2014
- Winkler, Anderson M.; Ridgway, Gerard R.; Webster, Matthew A.
- NeuroImage, Vol. 92
The Original Social Network: White Matter and Social Cognition
journal, June 2018
- Wang, Yin; Olson, Ingrid R.
- Trends in Cognitive Sciences, Vol. 22, Issue 6
HDAC2 negatively regulates memory formation and synaptic plasticity
journal, May 2009
- Guan, Ji-Song; Haggarty, Stephen J.; Giacometti, Emanuela
- Nature, Vol. 459, Issue 7243
Recruitment by the Repressor Freud-1 of Histone Deacetylase-Brg1 Chromatin Remodeling Complexes to Strengthen HTR1A Gene Repression
journal, December 2016
- Souslova, Tatiana; Mirédin, Kim; Millar, Anne M.
- Molecular Neurobiology, Vol. 54, Issue 10
Histone H4 lysine 16 hypoacetylation is associated with defective DNA repair and premature senescence in Zmpste24-deficient mice
journal, July 2011
- Krishnan, V.; Chow, M. Z. Y.; Wang, Z.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 30
HDAC inhibitor–dependent transcriptome and memory reinstatement in cognitive decline models
journal, August 2015
- Benito, Eva; Urbanke, Hendrik; Ramachandran, Binu
- Journal of Clinical Investigation, Vol. 125, Issue 9
Bayesian segmentation of brainstem structures in MRI
journal, June 2015
- Iglesias, Juan Eugenio; Van Leemput, Koen; Bhatt, Priyanka
- NeuroImage, Vol. 113
Histone Deacetylase 2 Inhibition Attenuates Downregulation of Hippocampal Plasticity Gene Expression during Aging
journal, March 2017
- Singh, Padmanabh; Thakur, M. K.
- Molecular Neurobiology, Vol. 55, Issue 3
Ultrastructural Characterization of the Lower Motor System in a Mouse Model of Krabbe Disease
journal, December 2016
- Cappello, Valentina; Marchetti, Laura; Parlanti, Paola
- Scientific Reports, Vol. 6, Issue 1
Reproducibility and consistency of evaluation techniques for HARDI data
journal, September 2008
- Gorczewski, Kamil; Mang, Sarah; Klose, Uwe
- Magnetic Resonance Materials in Physics, Biology and Medicine, Vol. 22, Issue 1
The inactive X chromosome in female mammals is distinguished by a lack of histone H4 acetylation, a cytogenetic marker for gene expression
journal, July 1993
- Jeppesen, Peter; Turner, Bryan M.
- Cell, Vol. 74, Issue 2
Antipsychotic-induced Hdac2 transcription via NF-κB leads to synaptic and cognitive side effects
journal, August 2017
- Ibi, Daisuke; de la Fuente Revenga, Mario; Kezunovic, Nebojsa
- Nature Neuroscience, Vol. 20, Issue 9
Whole Brain Segmentation
journal, January 2002
- Fischl, Bruce; Salat, David H.; Busa, Evelina
- Neuron, Vol. 33, Issue 3
Increased in vivo glial activation in patients with amyotrophic lateral sclerosis: Assessed with [11C]-PBR28
journal, January 2015
- Zürcher, Nicole R.; Loggia, Marco L.; Lawson, Robert
- NeuroImage: Clinical, Vol. 7
Altered Histone Acetylation Is Associated with Age-Dependent Memory Impairment in Mice
journal, May 2010
- Peleg, S.; Sananbenesi, F.; Zovoilis, A.
- Science, Vol. 328, Issue 5979
Measuring emotional intelligence with the MSCEIT V2.0.
journal, January 2003
- Mayer, John D.; Salovey, Peter; Caruso, David R.
- Emotion, Vol. 3, Issue 1
Antidepressant Actions of Histone Deacetylase Inhibitors
journal, September 2009
- Covington, H. E.; Maze, I.; LaPlant, Q. C.
- Journal of Neuroscience, Vol. 29, Issue 37
Epigenetic Priming of Memory Updating during Reconsolidation to Attenuate Remote Fear Memories
journal, January 2014
- Gräff, Johannes; Joseph, Nadine F.; Horn, Meryl E.
- Cell, Vol. 156, Issue 1-2
Structural Brain Changes in Aging: Courses, Causes and Cognitive Consequences
journal, January 2010
- Fjell, Anders M.; Walhovd, Kristine B.
- Reviews in the Neurosciences, Vol. 21, Issue 3
Antidepressant-Like Effects of the Histone Deacetylase Inhibitor, Sodium Butyrate, in the Mouse
journal, July 2007
- Schroeder, Frederick A.; Lin, Cong Lily; Crusio, Wim E.
- Biological Psychiatry, Vol. 62, Issue 1
Age-Related Memory Impairment Is Associated with Disrupted Multivariate Epigenetic Coordination in the Hippocampus
journal, March 2012
- Castellano, James F.; Fletcher, Bonnie R.; Kelley-Bell, Bennett
- PLoS ONE, Vol. 7, Issue 3
Inhibitors of Class 1 Histone Deacetylases Reverse Contextual Memory Deficits in a Mouse Model of Alzheimer's Disease
journal, December 2009
- Kilgore, Mark; Miller, Courtney A.; Fass, Daniel M.
- Neuropsychopharmacology, Vol. 35, Issue 4
A molecular network of the aging human brain provides insights into the pathology and cognitive decline of Alzheimer’s disease
journal, May 2018
- Mostafavi, Sara; Gaiteri, Chris; Sullivan, Sarah E.
- Nature Neuroscience, Vol. 21, Issue 6
Age-dependent epigenetic control of differentiation inhibitors is critical for remyelination efficiency
journal, August 2008
- Shen, Siming; Sandoval, Juan; Swiss, Victoria A.
- Nature Neuroscience, Vol. 11, Issue 9
Regional staging of white matter signal abnormalities in aging and Alzheimer's disease
journal, January 2017
- Lindemer, Emily R.; Greve, Douglas N.; Fischl, Bruce R.
- NeuroImage: Clinical, Vol. 14
Regulation of human SRY subcellular distribution by its acetylation/deacetylation
journal, August 2004
- Thevenet, Laurie; Méjean, Catherine; Moniot, Brigitte
- The EMBO Journal, Vol. 23, Issue 16
HDAC2 regulates atypical antipsychotic responses through the modulation of mGlu2 promoter activity
journal, August 2012
- Kurita, Mitsumasa; Holloway, Terrell; García-Bea, Aintzane
- Nature Neuroscience, Vol. 15, Issue 9
Insights into neuroepigenetics through human histone deacetylase PET imaging
journal, August 2016
- Wey, Hsiao-Ying; Gilbert, Tonya M.; Zürcher, Nicole R.
- Science Translational Medicine, Vol. 8, Issue 351
Age-dependent changes in mean and variance of gene expression across tissues in a twin cohort
journal, December 2017
- Viñuela, Ana; Brown, Andrew A.; Buil, Alfonso
- Human Molecular Genetics, Vol. 27, Issue 4
HDAC1 and HDAC2 control the transcriptional program of myelination and the survival of Schwann cells
journal, March 2011
- Jacob, Claire; Christen, Carlos N.; Pereira, Jorge A.
- Nature Neuroscience, Vol. 14, Issue 4
Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain
journal, January 2002
- Tzourio-Mazoyer, N.; Landeau, B.; Papathanassiou, D.
- NeuroImage, Vol. 15, Issue 1
Kinetic Analysis and Quantification of [ 11 C]Martinostat for in Vivo HDAC Imaging of the Brain
journal, March 2015
- Wey, Hsiao-Ying; Wang, Changning; Schroeder, Frederick A.
- ACS Chemical Neuroscience, Vol. 6, Issue 5
Evidence for brain glial activation in chronic pain patients
journal, January 2015
- Loggia, Marco L.; Chonde, Daniel B.; Akeju, Oluwaseun
- Brain, Vol. 138, Issue 3
In Vivo Imaging of Histone Deacetylases (HDACs) in the Central Nervous System and Major Peripheral Organs
journal, September 2014
- Wang, Changning; Schroeder, Frederick A.; Wey, Hsiao-Ying
- Journal of Medicinal Chemistry, Vol. 57, Issue 19
Epigenetic alterations regulate estradiol-induced enhancement of memory consolidation
journal, March 2010
- Zhao, Z.; Fan, L.; Frick, K. M.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 12
Advances in microstructural diffusion neuroimaging for psychiatric disorders
journal, November 2018
- Pasternak, Ofer; Kelly, Sinead; Sydnor, Valerie J.
- NeuroImage, Vol. 182
A Selective HDAC 1/2 Inhibitor Modulates Chromatin and Gene Expression in Brain and Alters Mouse Behavior in Two Mood-Related Tests
journal, August 2013
- Schroeder, Frederick A.; Lewis, Michael C.; Fass, Daniel M.
- PLoS ONE, Vol. 8, Issue 8
Sex differences in epigenetic mechanisms may underlie risk and resilience for mental health disorders
journal, July 2011
- Jessen, Heather M.; Auger, Anthony P.
- Epigenetics, Vol. 6, Issue 7
Different partial volume correction methods lead to different conclusions: An 18F-FDG-PET study of aging
journal, May 2016
- Greve, Douglas N.; Salat, David H.; Bowen, Spencer L.
- NeuroImage, Vol. 132
Delaying histone deacetylase response to injury accelerates conversion into repair Schwann cells and nerve regeneration
journal, January 2017
- Brügger, Valérie; Duman, Mert; Bochud, Maëlle
- Nature Communications, Vol. 8, Issue 1
The histone deacetylase RPD3 counteracts genomic silencing in Drosophila and yeast
journal, December 1996
- Rubertis, Francesco De; Kadosh, David; Henchoz, Sandra
- Nature, Vol. 384, Issue 6609
White matter pathways and social cognition
journal, July 2018
- Wang, Yin; Metoki, Athanasia; Alm, Kylie H.
- Neuroscience & Biobehavioral Reviews, Vol. 90
The Transcription Factor Yin Yang 1 Is Essential for Oligodendrocyte Progenitor Differentiation
journal, July 2007
- He, Ye; Dupree, Jeff; Wang, Ju
- Neuron, Vol. 55, Issue 2
HDAC1 and HDAC2 regulate oligodendrocyte differentiation by disrupting the β-catenin–TCF interaction
journal, June 2009
- Ye, Feng; Chen, Ying; Hoang, ThaoNguyen
- Nature Neuroscience, Vol. 12, Issue 7
Sex differences and stress across the lifespan
journal, September 2015
- Bale, Tracy L.; Epperson, C. Neill
- Nature Neuroscience, Vol. 18, Issue 10
Psychopathology in Women and Men: Focus on Female Hormones
journal, December 1997
- Seeman, Mary V.
- American Journal of Psychiatry, Vol. 154, Issue 12
Widespread sex differences in gene expression and splicing in the adult human brain
journal, November 2013
- Trabzuni, Daniah; Ramasamy, Adaikalavan; Imran, Sabaena
- Nature Communications, Vol. 4, Issue 1
Hippocampal-dependent antidepressant-like activity of histone deacetylase inhibition
journal, April 2011
- Covington, Herbert E.; Vialou, Vincent F.; LaPlant, Quincey
- Neuroscience Letters, Vol. 493, Issue 3
The Nuclear Receptor Corepressor Has Organizational Effects within the Developing Amygdala on Juvenile Social Play and Anxiety-Like Behavior
journal, March 2010
- Jessen, Heather M.; Kolodkin, Mira H.; Bychowski, Meaghan E.
- Endocrinology, Vol. 151, Issue 3
Recovery of learning and memory is associated with chromatin remodelling
journal, April 2007
- Fischer, Andre; Sananbenesi, Farahnaz; Wang, Xinyu
- Nature, Vol. 447, Issue 7141
Histone Deacetylase 2 in the Mouse Hippocampus: Attenuation of Age- Related Increase by Caloric Restriction
journal, September 2013
- Chouliaras, Leonidas; van den Hove, Daniel; Kenis, Gunter
- Current Alzheimer Research, Vol. 10, Issue 8
Gene regulation and DNA damage in the ageing human brain
journal, June 2004
- Lu, Tao; Pan, Ying; Kao, Shyan-Yuan
- Nature, Vol. 429, Issue 6994
Sex differences in histone modifications in the neonatal mouse brain
journal, January 2009
- Tsai, Houng-Wei; Grant, Patrick A.; Rissman, Emilie F.
- Epigenetics, Vol. 4, Issue 1
Histone Deacetylation during Brain Development Is Essential for Permanent Masculinization of Sexual Behavior
journal, May 2011
- Matsuda, Ken Ichi; Mori, Hiroko; Nugent, Bridget M.
- Endocrinology, Vol. 152, Issue 7
Effects of sex, age, and aggressive traits in man on brain serotonin 5-HT1A receptor binding potential measured by PET using [C-11]WAY-100635
journal, November 2002
- Parsey, Ramin V.; Oquendo, Maria A.; Simpson, Norman R.
- Brain Research, Vol. 954, Issue 2
Prevalence of Parkinsonian Signs and Associated Mortality in a Community Population of Older People
journal, January 1996
- Bennett, David A.; Beckett, Laurel A.; Murray, Anne M.
- New England Journal of Medicine, Vol. 334, Issue 2
Epidemiology of Parkinson’s disease
journal, February 2017
- Tysnes, Ole-Bjørn; Storstein, Anette
- Journal of Neural Transmission, Vol. 124, Issue 8
An epigenetic blockade of cognitive functions in the neurodegenerating brain
journal, February 2012
- Gräff, Johannes; Rei, Damien; Guan, Ji-Song
- Nature, Vol. 483, Issue 7388
Evolving Knowledge of Sex Differences in Brain Structure, Function, and Chemistry
journal, October 2007
- Cosgrove, Kelly P.; Mazure, Carolyn M.; Staley, Julie K.
- Biological Psychiatry, Vol. 62, Issue 8
Experience Modulates the Effects of Histone Deacetylase Inhibitors on Gene and Protein Expression in the Hippocampus: Impaired Plasticity in Aging
journal, August 2015
- Sewal, Angila S.; Patzke, Holger; Perez, Evelyn J.
- The Journal of Neuroscience, Vol. 35, Issue 33
Vorinostat, a histone deacetylase inhibitor, suppresses dendritic cell function and ameliorates experimental autoimmune encephalomyelitis
journal, March 2013
- Ge, Zhenzhen; Da, Yurong; Xue, Zhenyi
- Experimental Neurology, Vol. 241
A Longitudinal Study of Brain Volume Changes in Normal Aging Using Serial Registered Magnetic Resonance Imaging
journal, July 2003
- Scahill, Rachael I.; Frost, Chris; Jenkins, Rhian
- Archives of Neurology, Vol. 60, Issue 7
Advances in functional and structural MR image analysis and implementation as FSL
journal, January 2004
- Smith, Stephen M.; Jenkinson, Mark; Woolrich, Mark W.
- NeuroImage, Vol. 23
Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images
journal, October 2002
- Jenkinson, Mark; Bannister, Peter; Brady, Michael
- NeuroImage, Vol. 17, Issue 2
HDAC6 Brain Mapping with [ 18 F]Bavarostat Enabled by a Ru-Mediated Deoxyfluorination
journal, September 2017
- Strebl, Martin G.; Campbell, Arthur J.; Zhao, Wen-Ning
- ACS Central Science, Vol. 3, Issue 9
Applying FSL to the FIAC data: Model-based and model-free analysis of voice and sentence repetition priming
journal, January 2006
- Beckmann, Christian F.; Jenkinson, Mark; Woolrich, Mark W.
- Human Brain Mapping, Vol. 27, Issue 5
HDAC-mediated deacetylation of NF-κB is critical for Schwann cell myelination
journal, March 2011
- Chen, Ying; Wang, Haibo; Yoon, Sung Ok
- Nature Neuroscience, Vol. 14, Issue 4
REST and stress resistance in ageing and Alzheimer’s disease
journal, March 2014
- Lu, Tao; Aron, Liviu; Zullo, Joseph
- Nature, Vol. 507, Issue 7493
Conserved epigenomic signals in mice and humans reveal immune basis of Alzheimer’s disease
journal, February 2015
- Gjoneska, Elizabeta; Pfenning, Andreas R.; Mathys, Hansruedi
- Nature, Vol. 518, Issue 7539
Opportunities and pitfalls in the quantification of fiber integrity: What can we gain from Q-ball imaging?
journal, May 2010
- Fritzsche, Klaus H.; Laun, Frederik B.; Meinzer, Hans-Peter
- NeuroImage, Vol. 51, Issue 1
PET neuroimaging reveals histone deacetylase dysregulation in schizophrenia
journal, December 2018
- Gilbert, Tonya M.; Zürcher, Nicole R.; Wu, Christine J.
- Journal of Clinical Investigation, Vol. 129, Issue 1
Aging and the Occurrence of Dementia: Findings From a Population-Based Cohort With a Large Sample of Nonagenarians
journal, May 1999
- von Strauss, Eva; Viitanen, Matti; De Ronchi, Diana
- Archives of Neurology, Vol. 56, Issue 5
Reduced recognition memory is correlated with decrease in DNA methyltransferase1 and increase in histone deacetylase2 protein expression in old male mice
journal, June 2014
- Singh, Padmanabh; Thakur, Mahendra K.
- Biogerontology, Vol. 15, Issue 4
Neural plasticity in the ageing brain
journal, January 2006
- Burke, Sara N.; Barnes, Carol A.
- Nature Reviews Neuroscience, Vol. 7, Issue 1
Histone deacetylase activity is altered in brain areas from aged rats
journal, November 2013
- dos Santos Sant’ Anna, Gabriela; Rostirola Elsner, Viviane; Moysés, Felipe
- Neuroscience Letters, Vol. 556
PET Imaging Demonstrates Histone Deacetylase Target Engagement and Clarifies Brain Penetrance of Known and Novel Small Molecule Inhibitors in Rat
journal, September 2014
- Schroeder, F. A.; Wang, C.; Van de Bittner, G. C.
- ACS Chemical Neuroscience, Vol. 5, Issue 10
Quantification of the Serotonin 1A Receptor Using PET: Identification of a Potential Biomarker of Major Depression in Males
journal, January 2015
- Kaufman, Joshua; Sullivan, Gregory M.; Yang, Jie
- Neuropsychopharmacology, Vol. 40, Issue 7