Skip to main content
SpringerLink
Log in

Association between human gray matter metabotropic glutamate receptor-5 availability in vivo and white matter properties: a [11C]ABP688 PET and diffusion tensor imaging study

  • Original Article
  • Published:
Brain Structure and Function Aims and scope Submit manuscript

Abstract

Excitatory corticofugal projections in the subcortical white matter (WM) convey signals arising from local neuronal activity in the gray matter (GM). We hypothesized that metabotropic glutamate receptor-5 (mGluR5) availability in GM, as a surrogate marker for local glutamatergic neuronal activity, correlates with WM properties in healthy brain. We examined the relationship in healthy individuals between GM mGluR5 availability measured in vivo using [11C]ABP688 positron emission tomography (PET) and WM properties measured as fractional anisotropy (FA) using diffusion tensor imaging (DTI). Twenty-three healthy volunteers underwent this multimodal imaging. We calculated mGluR5 availability, [11C]ABP688 binding potential (BPND), using the simplified reference tissue model, and generated DTI FA maps using FMRIB’s Diffusion Toolbox (FDT) along with Tract-Based Spatial Statistics (TBSS). To investigate the relationship between mGluR5 availability and FA, we performed voxel-wise and region of interest (ROI)-based analyses. The voxel-wise analysis showed significant positive correlations between the whole cerebral GM [11C]ABP688 BPND and the FA in widespread WM regions including the corpus callosum body, internal capsule, and corona radiata (FWE corrected p < 0.05). The ROI-based analysis also revealed significant positive correlations (Bonferroni-corrected threshold p < 0.00021) between [11C]ABP688 BPND in the frontal and parietal cortical GM and FA in the internal capsule (anterior limb and retrolenticular part). Using a novel multimodal imaging interrogation, we provide the first evidence that GM mGluR5 availability is significantly positively associated with WM properties in healthy subjects. Future comparison studies could determine whether this relationship is perturbed in neuropsychiatric disorders with dysregulated mGluR5 signaling.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Abdallah CG, Sanacora G, Duman RS, Krystal JH (2015) Ketamine and rapid-acting antidepressants: a window into a new neurobiology for mood disorder therapeutics. Annu Rev Med 66:509–523

    CAS  Google Scholar 

  • Akkus F, Ametamey SM, Treyer V, Burger C, Johayem A, Umbricht D, Gomez Mancilla B, Sovago J, Buck A, Hasler G (2013) Marked global reduction in mGluR5 receptor binding in smokers and ex-smokers determined by [11C]ABP688 positron emission tomography. Proc Natl Acad Sci USA 110:737–742

    CAS  Google Scholar 

  • Akkus F, Treyer V, Johayem A, Ametamey SM, Mancilla BG, Sovago J, Buck A, Hasler G (2016) Association of long-term nicotine abstinence with normal metabotropic glutamate receptor-5 binding. Biol Psychiatry 79:474–480

    CAS  Google Scholar 

  • Ametamey SM, Kessler LJ, Honer M, Wyss MT, Buck A, Hintermann S, Auberson YP, Gasparini F, Schubiger PA (2006) Radiosynthesis and preclinical evaluation of 11C-ABP688 as a probe for imaging the metabotropic glutamate receptor subtype 5. J Nucl Med 47:698–705

    CAS  Google Scholar 

  • Ametamey SM, Treyer V, Streffer J, Wyss MT, Schmidt M, Blagoev M, Hintermann S, Auberson Y, Gasparini F, Fischer UC, Buck A (2007) Human PET studies of metabotropic glutamate receptor subtype 5 with 11C-ABP688. J Nucl Med 48:247–252

    CAS  Google Scholar 

  • Axer H, Keyserlingk DG (2000) Mapping of fiber orientation in human internal capsule by means of polarized light and confocal scanning laser microscopy. J Neurosci Methods 94:165–175

    CAS  Google Scholar 

  • Balu DT, Basu AC, Corradi JP, Cacace AM, Coyle JT (2012) The NMDA receptor co-agonists, D-serine and glycine, regulate neuronal dendritic architecture in the somatosensory cortex. Neurobiol Dis 45:671–682

    CAS  Google Scholar 

  • Balu DT, Coyle JT (2012) Neuronal D-serine regulates dendritic architecture in the somatosensory cortex. Neurosci Lett 517:77–81

    CAS  PubMed  PubMed Central  Google Scholar 

  • Berry-Kravis EM, Lindemann L, Jønch AE, Apostol G, Bear MF, Carpenter RL, Crawley JN, Curie A, Des Portes V, Hossain F, Gasparini F, Gomez-Mancilla B, Hessl D, Loth E, Scharf SH, Wang PP, Von Raison F, Hagerman R, Spooren W, Jacquemont S (2018) Drug development for neurodevelopmental disorders: lessons learned from fragile X syndrome. Nat Rev Drug Discov 17:280–299

    CAS  Google Scholar 

  • Berthele A, Platzer S, Laurie DJ, Weis S, Sommer B, Zieglgänsberger W, Conrad B, Tölle TR (1999) Expression of metabotropic glutamate receptor subtype mRNA (mGluR1-8) in human cerebellum. NeuroReport 10:3861–3867

    CAS  Google Scholar 

  • Byrnes KR, Loane DJ, Stoica BA, Zhang J, Faden AI (2012) Delayed mGluR5 activation limits neuroinflammation and neurodegeneration after traumatic brain injury. J Neuroinflammation 9:43

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chaki S, Ago Y, Palucha-Paniewiera A, Matrisciano F, Pilc A (2013) mGlu2/3 and mGlu5 receptors: potential targets for novel antidepressants. Neuropharmacology 66:40–52

    CAS  Google Scholar 

  • Chen Z, Chen X, Chen Z, Liu M, He H, Ma L, Yu S (2017) Alteration of gray matter texture features over the whole brain in medication-overuse headache using a 3-dimentional texture analysis. J Headache Pain 18:112

    PubMed  PubMed Central  Google Scholar 

  • Chokshi V, Gao M, Grier BD, Owens A, Wang H, Worley PF, Lee HK (2019) Input-specific metaplasticity in the visual cortex requires Homer1a-mediated mGluR5 Signaling. Neuron 104:736–748

    CAS  Google Scholar 

  • Daggett LP, Sacaan AI, Akong M, Rao SP, Hess SD, Liaw C, Urrutia A, Jachec C, Ellis SB, Dreessen J, Knöpfel T, Landwehrmeyer GB, Testa CM, Young AB, Varney M, Johnson EC, Veliçelebi G (1995) Molecular and functional characterization of recombinant human metabotropic glutamate receptor subtype 5. Neuropharmacology 34:871–886

    CAS  Google Scholar 

  • DeLorenzo C, Kumar JS, Mann JJ, Parsey RV (2011a) In vivo variation in metabotropic glutamate receptor subtype 5 binding using positron emission tomography and [11C]ABP688. J Cereb Blood Flow Metab 31:2169–2180

    CAS  PubMed  PubMed Central  Google Scholar 

  • DeLorenzo C, Milak MS, Brennan KG, Kumar JS, Mann JJ, Parsey RV (2011b) In vivo positron emission tomography imaging with [11C]ABP688: binding variability and specificity for the metabotropic glutamate receptor subtype 5 in baboons. Eur J Nucl Med Mol Imag 38:1083–1094

    CAS  Google Scholar 

  • DeLorenzo C, Sovago J, Gardus J, Xu J, Yang J, Behrje R, Kumar JS, Devanand DP, Pelton GH, Mathis CA, Mason NS, Gomez-Mancilla B, Aizenstein H, Mann JJ, Parsey RV (2015) Characterization of brain mGluR5 binding in a pilot study of late-life major depressive disorder using positron emission tomography and [11C]ABP688. Transl Psychiatry 5:e693

    CAS  PubMed  PubMed Central  Google Scholar 

  • DeLorenzo C, Gallezot JD, Gardus J, Yang J, Planeta B, Nabulsi N, Ogden RT, Labaree DC, Huang YH, Mann JJ, Gasparini F, Lin X, Javitch JA, Parsey RV, Carson RE, Esterlis I (2017) In vivo variation in same-day estimates of metabotropic glutamate receptor subtype 5 binding using [(11)C]ABP688 and [(18)F]FPEB. J Cereb Blood Flow Metab 37:2716–2727

    CAS  Google Scholar 

  • Deschwanden A, Karolewicz B, Feyissa AM, Treyer V, Ametamey SM, Johayem A, Burger C, Auberson YP, Sovago J, Stockmeier CA, Buck A, Hasler G (2011) Reduced metabotropic glutamate receptor 5 density in major depression determined by [(11)C]ABP688 PET and postmortem study. Am J Psychiatry 168:727–734

    PubMed  PubMed Central  Google Scholar 

  • DeVito LM, Balu DT, Kanter BR, Lykken C, Basu AC, Coyle JT, Eichenbaum H (2011) Serine racemase deletion disrupts memory for order and alters cortical dendritic morphology. Genes Brain Behav 10:210–222

    CAS  Google Scholar 

  • DuBois JM, Rousset OG, Rowley J, Porras-Betancourt M, Reader AJ, Labbe A, Massarweh G, Soucy JP, Rosa-Neto P, Kobayashi E (2016) Characterization of age/sex and the regional distribution of mGluR5 availability in the healthy human brain measured by high-resolution [(11)C]ABP688 PET. Eur J Nucl Med Mol Imag 43:152–162

    CAS  Google Scholar 

  • Elmenhorst D, Minuzzi L, Aliaga A, Rowley J, Massarweh G, Diksic M, Bauer A, Rosa-Neto P (2010) In vivo and in vitro validation of reference tissue models for the mGluR(5) ligand [(11)C]ABP688. J Cereb Blood Flow Metab 30:1538–1549

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fields RD (2015) A new mechanism of nervous system plasticity: activity-dependent myelination. Nat Rev Neurosci 16:756–767

    CAS  PubMed  PubMed Central  Google Scholar 

  • First MB, Spitzer RL, Gibbon M, Williams JBW (1996) Structured clinical interview for DSM-IV axis I disorders research version (SCID-I). New York State Psychiatric Institute Biometrics Research, New York

    Google Scholar 

  • Gerhard DM, Wohleb ES, Duman RS (2016) Emerging treatment mechanisms for depression: focus on glutamate and synaptic plasticity. Drug Discov Today 21:454–464

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gogliettino AR, Potenza MN, Yip SW (2016) White matter development and tobacco smoking in young adults: a systematic review with recommendations for future research. Drug Alcohol Dep 162:26–33

    Google Scholar 

  • Herman EJ, Bubser M, Conn PJ, Jones CK (2012) Metabotropic glutamate receptors for new treatments in schizophrenia. Handb Exp Pharmacol 213:297–365

    CAS  Google Scholar 

  • Holmes A, Spanagel R, Krystal JH (2013) Glutamatergic targets for new alcohol medications. Psychopharmacology 229:539–554

    CAS  Google Scholar 

  • Horio M, Fujita Y, Hashimoto K (2013) Therapeutic effects of metabotropic glutamate receptor 5 positive allosteric modulator CDPPB on phencyclidine-induced cognitive deficits in mice. Fundam Clin Pharmacol 27:483–488

    CAS  Google Scholar 

  • Hudkins M, O'Neill J, Tobias MC, Bartzokis G, London ED (2012) Cigarette smoking and white matter microstructure. Psychopharmacology 221:285–295

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hughes ZA, Neal SJ, Smith DL, Sukoff Rizzo SJ, Pulicicchio CM, Lotarski S, Lu S, Dwyer JM, Brennan J, Olsen M, Bender CN, Kouranova E, Andree TH, Harrison JE, Whiteside GT, Springer D, O'Neil SV, Leonard SK, Schechter LE, Dunlop J, Rosenzweig-Lipson S, Ring RH (2013) Negative allosteric modulation of metabotropic glutamate receptor 5 results in broad spectrum activity relevant to treatment resistant depression. Neuropharmacology 66:202–214

    CAS  Google Scholar 

  • Hulka LM, Treyer V, Scheidegger M, Preller KH, Vonmoos M, Baumgartner MR, Johayem A, Ametamey SM, Buck A, Seifritz E, Quednow BB (2014) Smoking but not cocaine use is associated with lower cerebral metabotropic glutamate receptor 5 density in humans. Mol Psychiatry 19:625–632

    CAS  Google Scholar 

  • Jacquemont S, Curie A, des Portes Torrioli V, Berry-Kravis E, Hagerman RJ, Ramos FJ, Cornish K, He Y, Paulding C, Neri G, Chen F, Hadjikhani N, Martinet D, Meyer J, Beckmann JS, Delange K, Brun A, Bussy G, Gasparini F, Hilse T, Floesser A, Branson J, Bilbe G, Johns D, Gomez-Mancilla B (2011) Epigenetic modification of the FMR1 gene in fragile X syndrome is associated with differential response to the mGluR5 antagonist AFQ056. Sci Transl Med 3:64 (ral)

    Google Scholar 

  • Jia Z, Lu Y, Henderson J, Taverna F, Romano C, Abramow-Newerly W, Wojtowicz JM, Roder J (1998) Selective abolition of the NMDA component of long-term potentiation in mice lacking mGluR5. Learn Mem 5:331–343

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kim HW, Lee DG (2017) Resting-state metabolism of hand knob area on (18)F-FDG PET-CT according to hand function and tractography of corticospinal tract after stroke. Ann Rehabil Med 41:171–177

    PubMed  PubMed Central  Google Scholar 

  • Kwag J, Paulsen O (2012) Gating of NMDA receptor-mediated hippocampal spike timing-dependent potentiation by mGluR5. Neuropharmacology 63:701–709

    CAS  PubMed  PubMed Central  Google Scholar 

  • Luján R, Shigemoto R, López-Bendito G (2005) Glutamate and GABA receptor signalling in the developing brain. Neuroscience 130:567–580

    Google Scholar 

  • Luyt K, Varadi A, Molnar E (2003) Functional metabotropic glutamate receptors are expressed in oligodendrocyte progenitor cells. J Neurochem 84:1452–1464

    CAS  Google Scholar 

  • Luyt K, Váradi A, Durant CF, Molnár E (2006) Oligodendroglial metabotropic glutamate receptors are developmentally regulated and involved in the prevention of apoptosis. J Neurochem 99:641–656

    CAS  Google Scholar 

  • Maddock RJ, Casazza GA, Fernandez DH, Maddock MI (2016) Acute modulation of cortical glutamate and GABA content by physical activity. J Neurosci 36:2449–2457

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mathews WB, Kuwabara H, Stansfield K, Valentine H, Alexander M, Kumar A, Hilton J, Dannals RF, Wong DF, Gasparini F (2014) Dose-dependent, saturable occupancy of the metabotropic glutamate subtype 5 receptor by fenobam as measured with [(11)C]ABP688 PET imaging. Synapse 68:565–573

    CAS  PubMed  PubMed Central  Google Scholar 

  • McGinnity CJ, Hammers A, Riaño Barros DA, Luthra SK, Jones PA, Trigg W, Micallef C, Symms MR, Brooks DJ, Koepp MJ, Duncan JS (2014) Initial evaluation of 18F-GE-179, a putative PET tracer for activated N-methyl D-aspartate receptors. J Nucl Med 55:423–430

    CAS  Google Scholar 

  • Micu I, Plemel JR, Lachance C, Proft J, Jansen AJ, Cummins K, van Minnen J, Stys PK (2016) The molecular physiology of the axo-myelinic synapse. Exp Neurol 276:41–50

    CAS  Google Scholar 

  • Moretto E, Murru L, Martano G, Sassone J, Passafaro M (2018) Glutamatergic synapses in neurodevelopmental disorders. Prog Neuropsychopharmacol Biol Psychiatry 84:328–342

    CAS  Google Scholar 

  • Park HJ, Kim CH, Park ES, Park B, Oh SR, Oh MK, Park CI, Lee JD (2013) Increased GABA-A receptor binding and reduced connectivity at the motor cortex in children with hemiplegic cerebral palsy: a multimodal investigation using 18F-fluoroflumazenil PET, immunohistochemistry, and MR imaging. J Nucl Med 54:1263–1269

    CAS  Google Scholar 

  • Sampaio-Baptista C, Johansen-Berg H (2017) White matter plasticity in the adult brain. Neuron 96:1239–1251

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sanacora G, Zarate CA, Krystal JH, Manji HK (2008) Targeting the glutamatergic system to develop novel, improved therapeutics for mood disorders. Nat Rev Drug Discov 7:426–437

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sánchez SM, Duarte-Abritta B, Abulafia C, De Pino G, Bocaccio H, Castro MN, Sevlever GE, Fonzo GA, Nemeroff CB, Gustafson DR, Guinjoan SM, Villarreal MF (2020) White matter fiber density abnormalities in cognitively normal adults at risk for late-onset Alzheimer’s disease. J Psychiatr Res 122:79–87

    Google Scholar 

  • Scavuzzo CJ, Moulton CJ, Larsen RJ (2018) The use of magnetic resonance spectroscopy for assessing the effect of diet on cognition. Nutr Neurosci 21:1–15

    CAS  Google Scholar 

  • Scheefhals N, MacGillavry HD (2018) Functional organization of postsynaptic glutamate receptors. Mol Cell Neurosci 91:82–94

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schilling LP, Pascoal TA, Zimmer ER, Mathotaarachchi S, Shin M, de Mello Rieder CR, Gauthier S, Palmini A, Rosa-Neto P, Alzheimer’s Disease Neuroimaging Initiative (2019) Regional amyloid-β load and white matter abnormalities contribute to hypometabolism in Alzheimer’s dementia. Mol Neurobiol 56:4916–4924

    CAS  Google Scholar 

  • Schoenberger M, Schroeder FA, Placzek MS, Carter RL, Rosen BR, Hooker JM, Sander CY (2018) In vivo [(18)F]GE-179 brain signal does not show NMDA-specific modulation with drug challenges in rodents and nonhuman primates. ACS Chem Neurosci 9:298–305

    CAS  Google Scholar 

  • Shigemoto R, Nomura S, Ohishi H, Sugihara H, Nakanishi S, Mizuno N (1993) Immunohistochemical localization of a metabotropic glutamate receptor, mGluR5, in the rat brain. Neurosci Lett 163:53–57

    CAS  Google Scholar 

  • Shimony JS, McKinstry RC, Akbudak E, Aronovitz JA, Snyder AZ, Lori NF, Cull TS, Conturo TE (1999) Quantitative diffusion-tensor anisotropy brain MR imaging: normative human data and anatomic analysis. Radiology 212:770–784

    CAS  Google Scholar 

  • Slifstein M, Laruelle M (2001) Models and methods for derivation of in vivo neuroreceptor parameters with PET and SPECT reversible radiotracers. Nucl Med Biol 28:595–608

    CAS  Google Scholar 

  • Smart K, Cox SML, Scala SG, Tippler M, Jaworska N, Boivin M, Séguin JR, Benkelfat C, Leyton M (2019) Sex differences in [(11)C]ABP688 binding: a positron emission tomography study of mGlu5 receptors. Eur J Nucl Med Mol Imag 46:1179–1183

    CAS  Google Scholar 

  • Sullivan JM, Lim K, Labaree D, Lin SF, McCarthy TJ, Seibyl JP, Tamagnan G, Huang Y, Carson RE, Ding YS, Morris ED (2013) Kinetic analysis of the metabotropic glutamate subtype 5 tracer [(18)F]FPEB in bolus and bolus-plus-constant-infusion studies in humans. J Cereb Blood Flow Metab 33:532–541

    CAS  Google Scholar 

  • Takumi Y, Matsubara A, Rinvik E, Ottersen OP (1999) The arrangement of glutamate receptors in excitatory synapses. Ann NY Acad Sci 868:474–482

    CAS  Google Scholar 

  • Tu JC, Xiao B, Naisbitt S, Yuan JP, Petralia RS, Brakeman P, Doan A, Aakalu VK, Lanahan AA, Sheng M, Worley PF (1999) Coupling of mGluR/Homer and PSD-95 complexes by the Shank family of postsynaptic density proteins. Neuron 23:583–592

    CAS  Google Scholar 

  • Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15:273–289

    CAS  Google Scholar 

  • Umene-Nakano W, Yoshimura R, Kakeda S, Watanabe K, Hayashi K, Nishimura J, Takahashi H, Moriya J, Ide S, Ueda I, Hori H, Ikenouchi-Sugita A, Katsuki A, Atake K, Abe O, Korogi Y, Nakamura J (2014) Abnormal white matter integrity in the corpus callosum among smokers: tract-based spatial statistics. PLoS ONE 9:e87890

    PubMed  PubMed Central  Google Scholar 

  • Vanzulli I, Butt AM (2015) mGluR5 protect astrocytes from ischemic damage in postnatal CNS white matter. Cell Calcium 58:423–430

    CAS  PubMed  PubMed Central  Google Scholar 

  • Virta A, Barnett A, Pierpaoli C (1999) Visualizing and characterizing white matter fiber structure and architecture in the human pyramidal tract using diffusion tensor MRI. Magn Reson Imag 17:1121–1133

    CAS  Google Scholar 

  • Walhovd KB, Johansen-Berg H, Káradóttir RT (2014) Unraveling the secrets of white matter–bridging the gap between cellular, animal and human imaging studies. Neuroscience 276:2–13

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wassenaar TM, Yaffe K, van der Werf YD, Sexton CE (2019) Associations between modifiable risk factors and white matter of the aging brain: insights from diffusion tensor imaging studies. Neurobiol Aging 80:56–70

    PubMed  PubMed Central  Google Scholar 

  • Wu Y, Carson RE (2002) Noise reduction in the simplified reference tissue model for neuroreceptor functional imaging. J Cereb Blood Flow Metab 22:1440–1452

    PubMed  Google Scholar 

Download references

Acknowledgements

This research was supported by the Brain Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Science, ICT and Future Planning (2016M3C7A1914451). We thank all the participants who took part in this study, and Eun-Sook Kim for her research coordination. We thank Inglewood Biomedical Imaging for valuable help in manuscript editing.

Funding

This research was supported by the Brain Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Science, ICT and Future Planning (2016M3C7A1914451).

Author information

Authors and Affiliations

  1. Neuroscience Research Institute, Gachon University, Incheon, South Korea

    Song E. Kim, Yo-Han Joo, Young-Don Son, Hang-Keun Kim, Sang-Yoon Lee, Min-Woo Lee, Tatsuo Ido & Jong-Hoon Kim

  2. Department of Biomedical Engineering, College of Health Science, Gachon University, Incheon, South Korea

    Young-Don Son & Hang-Keun Kim

  3. Gachon Advanced Institute for Health Science and Technology, Graduate School, Incheon, South Korea

    Young-Don Son, Hang-Keun Kim, Sang-Yoon Lee & Jong-Hoon Kim

  4. Department of Neuroscience, Gachon University College of Medicine, Gachon University, Incheon, South Korea

    Sang-Yoon Lee

  5. Department of Psychiatry, Gil Medical Center, Gachon University College of Medicine, Neuroscience Research Institute, Gachon University, 1198 Guwol-dong, Namdong-gu, Incheon, 405-760, South Korea

    Jong-Hoon Kim

Authors
  1. Song E. Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yo-Han Joo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Young-Don Son
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hang-Keun Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sang-Yoon Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Min-Woo Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Tatsuo Ido
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jong-Hoon Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jong-Hoon Kim.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Ethical approval

The study protocol was approved by the Institutional Review Board of the Gachon University Gil Medical Center, and all procedures used in the study were conducted in accordance with the ethical standards of the institutional research ethics committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

Informed consent

Written informed consent was obtained from all participants after they had received a full explanation of the study procedures.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 42 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kim, S.E., Joo, YH., Son, YD. et al. Association between human gray matter metabotropic glutamate receptor-5 availability in vivo and white matter properties: a [11C]ABP688 PET and diffusion tensor imaging study. Brain Struct Funct 225, 1805–1816 (2020). https://doi.org/10.1007/s00429-020-02094-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-020-02094-7

Keywords

Search

Navigation