Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Imaging the brain’s immune response to alcohol with [11C]PBR28 TSPO Positron Emission Tomography

Molecular Psychiatry volume 28, pages 3384–3390 (2023)Cite this article

Subjects

Abstract

In humans, the negative effects of alcohol are linked to immune dysfunction in both the periphery and the brain. Yet acute effects of alcohol on the neuroimmune system and its relationships with peripheral immune function are not fully understood. To address this gap, immune response to an alcohol challenge was measured with positron emission tomography (PET) using the radiotracer [11C]PBR28, which targets the 18-kDa translocator protein, a marker sensitive to immune challenges. Participants (n = 12; 5 F; 25–45 years) who reported consuming binge levels of alcohol (>3 drinks for females; >4 drinks for males) 1–3 months before scan day were enrolled. Imaging featured a baseline [11C]PBR28 scan followed by an oral laboratory alcohol challenge over 90 min. An hour later, a second [11C]PBR28 scan was acquired. Dynamic PET data were acquired for at least 90 min with arterial blood sampling to measure the metabolite-corrected input function. [11C]PBR28 volume of distributions (VT) was estimated in the brain using multilinear analysis 1. Subjective effects, blood alcohol levels (BAL), and plasma cytokines were measured during the paradigm. Full completion of the alcohol challenge and data acquisition occurred for n = 8 (2 F) participants. Mean peak BAL was 101 ± 15 mg/dL. Alcohol significantly increased brain [11C]PBR28 VT (n = 8; F(1,49) = 34.72, p > 0.0001; Cohen’s d’=0.8–1.7) throughout brain by 9–16%. Alcohol significantly altered plasma cytokines TNF-α (F(2,22) = 17.49, p < 0.0001), IL-6 (F(2,22) = 18.00, p > 0.0001), and MCP-1 (F(2,22) = 7.02, p = 0.004). Exploratory analyses identified a negative association between the subjective degree of alcohol intoxication and changes in [11C]PBR28 VT. These findings provide, to our knowledge, the first in vivo human evidence for an acute brain immune response to alcohol.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Study design.
Fig. 2: Mean blood alcohol level (n = 10) during and after the alcohol drinking session lasting 90 mins.
Fig. 3: [11C]PBR28 VT (uncorrected for rs6971 genotype), indicative of TSPO levels, increased in all regions after the laboratory alcohol challenge (n = 8).
Fig. 4: Cytokine response to alcohol challenge.

Similar content being viewed by others

Data availability

All data generated or analyzed during this study are included in this published article (and its Supplementary Data files).

References

  1. Erickson EK, Grantham EK, Warden AS, Harris RA. Neuroimmune signaling in alcohol use disorder. Pharm Biochem Behav. 2019;177:34–60.

    Article  CAS  Google Scholar 

  2. Montesinos J, Alfonso-Loeches S, Guerri C. Impact of the innate immune response in the actions of ethanol on the central nervous system. Alcohol Clin Exp Res. 2016;40:2260–70.

    Article  CAS  PubMed  Google Scholar 

  3. Molina PE, Happel KI, Zhang P, Kolls JK, Nelson S. Focus on: Alcohol and the immune system. Alcohol Res Health. 2010;33:97–108.

    PubMed  PubMed Central  Google Scholar 

  4. Orio L, Antón M, Rodríguez-Rojo IC, Correas Á, García-Bueno B, Corral M, et al. Young alcohol binge drinkers have elevated blood endotoxin, peripheral inflammation and low cortisol levels: neuropsychological correlations in women. Addict Biol. 2018;23:1130–44.

    Article  CAS  PubMed  Google Scholar 

  5. Pascual M, Montesinos J, Marcos M, Torres J-L, Costa-Alba P, García-García F, et al. Gender differences in the inflammatory cytokine and chemokine profiles induced by binge ethanol drinking in adolescence. Addict Biol. 2017;22:1829–41.

    Article  CAS  PubMed  Google Scholar 

  6. Leclercq S, De Saeger C, Delzenne N, de Timary P, Stärkel P. Role of inflammatory pathways, blood mononuclear cells, and gut-derived bacterial products in alcohol dependence. Biol Psychiatry. 2014;76:725–33.

    Article  CAS  PubMed  Google Scholar 

  7. Hillmer AT, Holden D, Fowles K, Nabulsi N, West BL, Carson RE, et al. Microglial depletion and activation: A [11 C]PBR28 PET study in nonhuman primates. EJNMMI Res. 2017;7:59.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Szabo G, Saha B. Alcohol’s effect on host defense. Alcohol Res. 2015;37:159–70.

    PubMed  PubMed Central  Google Scholar 

  9. Marshall SA, McClain JA, Kelso ML, Hopkins DM, Pauly JR, Nixon K. Microglial activation is not equivalent to neuroinflammation in alcohol-induced neurodegeneration: the importance of microglia phenotype. Neurobiol Dis. 2013;54:239–51.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Henriques JF, Portugal CC, Canedo T, Relvas JB, Summavielle T, Socodato R. Microglia and alcohol meet at the crossroads: Microglia as critical modulators of alcohol neurotoxicity. Toxicol Lett. 2018;283:21–31.

    Article  CAS  PubMed  Google Scholar 

  11. Walker CD, Risher WC, Risher M-L. Regulation of synaptic development by astrocyte signaling factors and their emerging roles in substance abuse. Cells. 2020;9:297.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Kettenmann H, Kirchhoff F, Verkhratsky A. Microglia: new roles for the synaptic stripper. Neuron. 2013;77:10–18.

    Article  CAS  PubMed  Google Scholar 

  13. Brown GC, Neher JJ. Microglial phagocytosis of live neurons. Nat Rev Neurosci. 2014;15:209–16.

    Article  CAS  PubMed  Google Scholar 

  14. Frick LR, Williams K, Pittenger C. Microglial dysregulation in psychiatric disease. Clin Dev Immunol. 2013;2013:608654.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Melbourne JK, Thompson KR, Peng H, Nixon K. Its complicated: the relationship between alcohol and microglia in the search for novel pharmacotherapeutic targets for alcohol use disorders. Prog Mol Biol Transl Sci. 2019;167:179–221.

    Article  CAS  PubMed  Google Scholar 

  16. Marshall SA, Casachahua JD, Rinker JA, Blose AK, Lysle DT, Thiele TE. IL-1 receptor signaling in the basolateral amygdala modulates binge-like ethanol consumption in male C57BL/6 J mice. Brain Behav Immun. 2016;51:258–67.

    Article  CAS  PubMed  Google Scholar 

  17. Blednov YA, Ponomarev I, Geil C, Bergeson S, Koob GF, Harris RA. Neuroimmune regulation of alcohol consumption: behavioral validation of genes obtained from genomic studies. Addict Biol. 2012;17:108–20.

    Article  CAS  PubMed  Google Scholar 

  18. Valenta JP, Gonzales RA. Chronic intracerebroventricular infusion of monocyte chemoattractant protein-1 leads to a persistent increase in sweetened ethanol consumption during operant self-administration but does not influence sucrose consumption in Long-Evans rats. Alcohol Clin Exp Res. 2016;40:187–95.

    Article  CAS  PubMed  Google Scholar 

  19. Riikonen J, Jaatinen P, Rintala J, Pörsti I, Karjala K, Hervonen A. Intermittent ethanol exposure increases the number of cerebellar microglia. Alcohol Alcohol. 2002;37:421–6.

    Article  CAS  PubMed  Google Scholar 

  20. Pascual M, Blanco AM, Cauli O, Miñarro J, Guerri C. Intermittent ethanol exposure induces inflammatory brain damage and causes long-term behavioural alterations in adolescent rats. Eur J Neurosci. 2007;25:541–50.

    Article  PubMed  Google Scholar 

  21. Marshall SA, Geil CR, Nixon K. Prior binge ethanol exposure potentiates the microglial response in a model of alcohol-induced neurodegeneration. Brain Sci. 2016;6:16.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Qin L, He J, Hanes RN, Pluzarev O, Hong J-S, Crews FT. Increased systemic and brain cytokine production and neuroinflammation by endotoxin following ethanol treatment. J Neuroinflammation. 2008;5:10.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Lewohl JM, Nunez YO, Dodd PR, Tiwari GR, Harris RA, Mayfield RD. Up-regulation of microRNAs in brain of human alcoholics. Alcohol Clin Exp Res. 2011;35:1928–37.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Crews FT, Qin L, Sheedy D, Vetreno RP, Zou J. High mobility group box 1/Toll-like receptor danger signaling increases brain neuroimmune activation in alcohol dependence. Biol Psychiatry. 2013;73:602–12.

    Article  CAS  PubMed  Google Scholar 

  25. Sandiego CM, Gallezot J-D, Pittman B, Nabulsi N, Lim K, Lin S-F, et al. Imaging robust microglial activation after lipopolysaccharide administration in humans with PET. Proc Natl Acad Sci USA. 2015;112:12468–73.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Hillmer AT, Sandiego CM, Hannestad J, Angarita GA, Kumar A, McGovern EM, et al. In vivo imaging of translocator protein, a marker of activated microglia, in alcohol dependence. Mol Psychiatry. 2017;22:1759–66.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Kalk NJ, Guo Q, Owen D, Cherian R, Erritzoe D, Gilmour A, et al. Decreased hippocampal translocator protein (18 kDa) expression in alcohol dependence: a [11 C]PBR28 PET study. Transl Psychiatry. 2017;7:e996.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Kim SW, Wiers CE, Tyler R, Shokri-Kojori E, Jang YJ, Zehra A, et al. Influence of alcoholism and cholesterol on TSPO binding in brain: PET [11 C]PBR28 studies in humans and rodents. Neuropsychopharmacology. 2018;43:1832–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Block ML, Hong J-S. Microglia and inflammation-mediated neurodegeneration: multiple triggers with a common mechanism. Prog Neurobiol. 2005;76:77–98.

    Article  CAS  PubMed  Google Scholar 

  30. Marshall SA, McClain JA, Wooden JI, Nixon K. Microglia dystrophy following binge-like alcohol exposure in adolescent and adult male rats. Front Neuroanat. 2020;14:52.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Hu P, Wang D, Zhang Y, Cai Z, Ye T, Tong L, et al. Apoptosis-triggered decline in hippocampal microglia mediates adolescent intermittent alcohol exposure-induced depression-like behaviors in mice. Neuropharmacology. 2020;170:108054.

    Article  CAS  PubMed  Google Scholar 

  32. Barton EA, Baker C, Leasure JL. Investigation of sex differences in the microglial response to binge ethanol and exercise. Brain Sci. 2017;7:139.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Maeda J, Higuchi M, Inaji M, Ji B, Haneda E, Okauchi T, et al. Phase-dependent roles of reactive microglia and astrocytes in nervous system injury as delineated by imaging of peripheral benzodiazepine receptor. Brain Res. 2007;1157:100–11.

    Article  CAS  PubMed  Google Scholar 

  34. Toyama H, Hatano K, Suzuki H, Ichise M, Momosaki S, Kudo G, et al. In vivo imaging of microglial activation using a peripheral benzodiazepine receptor ligand: [11 C]PK-11195 and animal PET following ethanol injury in rat striatum. Ann Nucl Med. 2008;22:417–24.

    Article  PubMed  Google Scholar 

  35. Obernier JA, White AM, Swartzwelder HS, Crews FT. Cognitive deficits and CNS damage after a 4-day binge ethanol exposure in rats. Pharm Biochem Behav. 2002;72:521–32.

    Article  CAS  Google Scholar 

  36. Saba W, Goutal S, Auvity S, Kuhnast B, Coulon C, Kouyoumdjian V, et al. Imaging the neuroimmune response to alcohol exposure in adolescent baboons: a TSPO PET study using 18 F-DPA-714. Addict Biol. 2018;23:1000–9.

    Article  CAS  PubMed  Google Scholar 

  37. Fujita M, Imaizumi M, Zoghbi SS, Fujimura Y, Farris AG, Suhara T, et al. Kinetic analysis in healthy humans of a novel positron emission tomography radioligand to image the peripheral benzodiazepine receptor, a potential biomarker for inflammation. Neuroimage. 2008;40:43–52.

    Article  PubMed  Google Scholar 

  38. Owen DR, Yeo AJ, Gunn RN, Song K, Wadsworth G, Lewis A, et al. An 18-kDa translocator protein (TSPO) polymorphism explains differences in binding affinity of the PET radioligand PBR28. J Cereb Blood Flow Metab. 2012;32:1–5.

    Article  CAS  PubMed  Google Scholar 

  39. Watson PE, Watson ID, Batt RD. Prediction of blood alcohol concentrations in human subjects. Updating the Widmark Equation. J Stud Alcohol. 1981;42:547–56.

    Article  CAS  PubMed  Google Scholar 

  40. Curtin JJ, Fairchild BA. Alcohol and cognitive control: implications for regulation of behavior during response conflict. J Abnorm Psychol. 2003;112:424–36.

    Article  PubMed  Google Scholar 

  41. Martin CS, Earleywine M, Musty RE, Perrine MW, Swift RM. Development and validation of the biphasic alcohol effects scale. Alcohol Clin Exp Res. 1993;17:140–6.

    Article  CAS  PubMed  Google Scholar 

  42. Morean ME, de Wit H, King AC, Sofuoglu M, Rueger SY, O’Malley SS. The drug effects questionnaire: psychometric support across three drug types. Psychopharmacology. 2013;227:177–92.

    Article  CAS  PubMed  Google Scholar 

  43. Hannestad J, DellaGioia N, Gallezot J-D, Lim K, Nabulsi N, Esterlis I, et al. The neuroinflammation marker translocator protein is not elevated in individuals with mild-to-moderate depression: a [¹¹C]PBR28 PET study. Brain Behav Immun. 2013;33:131–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Park E, Gallezot J-D, Delgadillo A, Liu S, Planeta B, Lin S-F, et al. (11)C-PBR28 imaging in multiple sclerosis patients and healthy controls: test-retest reproducibility and focal visualization of active white matter areas. Eur J Nucl Med Mol Imaging. 2015;42:1081–92.

    Article  CAS  PubMed  Google Scholar 

  45. Jin X, Mulnix T, Gallezot JD, Carson RE. Evaluation of motion correction methods in human brain PET imaging—A simulation study based on human motion data. Med Phys. 2013;40:102503.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Ichise M, Liow J-S, Lu J-Q, Takano A, Model K, Toyama H, et al. Linearized reference tissue parametric imaging methods: application to [11 C]DASB positron emission tomography studies of the serotonin transporter in human brain. J Cereb Blood Flow Metab. 2003;23:1096–112.

    Article  PubMed  Google Scholar 

  47. Neupane SP, Skulberg A, Skulberg KR, Aass HCD, Bramness JG. Cytokine changes following acute ethanol intoxication in healthy men: a crossover study. Mediators Inflamm. 2016;2016:3758590.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Monnig MA, Lamb PS, Parra JM, Cioe PA, Martone CM, Monti PM, et al. Immune response to an acute moderate dose of alcohol in healthy young adults. Alcohol Alcohol. 2020;55:616–23.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Kane CJM, Phelan KD, Douglas JC, Wagoner G, Johnson JW, Xu J, et al. Effects of ethanol on immune response in the brain: region-specific changes in adolescent versus adult mice. Alcohol: Clin Exp Res. 2014;38:384–91.

    Article  CAS  PubMed  Google Scholar 

  50. Tajuddin N, Moon K-H, Marshall SA, Nixon K, Neafsey EJ, Kim H-Y, et al. Neuroinflammation and neurodegeneration in adult rat brain from binge ethanol exposure: abrogation by docosahexaenoic acid. PLoS One. 2014;9:e101223.

    Article  PubMed  PubMed Central  Google Scholar 

  51. Tournier BB, Tsartsalis S, Ceyzériat K, Medina Z, Fraser BH, Grégoire M-C, et al. Fluorescence-activated cell sorting to reveal the cell origin of radioligand binding. J Cereb Blood Flow Metab. 2020;40:1242–55.

    Article  CAS  PubMed  Google Scholar 

  52. Nutma E, Gebro E, Marzin MC, van der Valk P, Matthews PM, Owen DR, et al. Activated microglia do not increase 18 kDa translocator protein (TSPO) expression in the multiple sclerosis brain. Glia. 2021;69:2447–58.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Owen DR, Narayan N, Wells L, Healy L, Smyth E, Rabiner EA, et al. Pro-inflammatory activation of primary microglia and macrophages increases 18 kDa translocator protein expression in rodents but not humans. J Cereb Blood Flow Metab. 2017;37:2679–90.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Tyler RE, Kim SW, Guo M, Jang YJ, Damadzic R, Stodden T, et al. Detecting neuroinflammation in the brain following chronic alcohol exposure in rats: a comparison between in vivo and in vitro TSPO radioligand binding. Eur J Neurosci. 2019;50:1831–42.

    Article  PubMed  Google Scholar 

  55. Leclercq S, Cani PD, Neyrinck AM, Stärkel P, Jamar F, Mikolajczak M, et al. Role of intestinal permeability and inflammation in the biological and behavioral control of alcohol-dependent subjects. Brain Behav Immun. 2012;26:911–8.

    Article  CAS  PubMed  Google Scholar 

  56. Leclercq S, Matamoros S, Cani PD, Neyrinck AM, Jamar F, Stärkel P, et al. Intestinal permeability, gut-bacterial dysbiosis, and behavioral markers of alcohol-dependence severity. Proc Natl Acad Sci USA. 2014;111:E4485–4493.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Hillmer AT, Nadim H, Devine L, Jatlow P, O’Malley SS. Acute alcohol consumption alters the peripheral cytokines IL-8 and TNF-α. Alcohol. 2020;85:95–9.

    Article  CAS  PubMed  Google Scholar 

  58. Bromander S, Anckarsäter R, Kristiansson M, Blennow K, Zetterberg H, Anckarsäter H, et al. Changes in serum and cerebrospinal fluid cytokines in response to non-neurological surgery: an observational study. J Neuroinflammation. 2012;9:242.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Khan W, Corben LA, Bilal H, Vivash L, Delatycki MB, Egan GF, et al. Neuroinflammation in the cerebellum and brainstem in Friedreich Ataxia: an [18 F]-FEMPA PET study. Mov Disord. 2022;37:218–24.

    Article  CAS  PubMed  Google Scholar 

  60. Dantzer R. Neuroimmune interactions: from the brain to the immune system and vice versa. Physiol Rev. 2018;98:477–504.

    Article  CAS  PubMed  Google Scholar 

  61. Woodcock EA, Schain M, Cosgrove KP, Hillmer AT. Quantification of [11 C]PBR28 data after systemic lipopolysaccharide challenge. EJNMMI Res. 2020;10:19.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Matheson GJ, Plavén-Sigray P, Forsberg A, Varrone A, Farde L, Cervenka S. Assessment of simplified ratio-based approaches for quantification of PET [11 C]PBR28 data. EJNMMI Res. 2017;7,:58.

    Article  PubMed  Google Scholar 

  63. Wilhelm CJ, Fuller BE, Huckans M, Loftis JM. Peripheral immune factors are elevated in women with current or recent alcohol dependence and associated with altered mood and memory. Drug Alcohol Depend. 2017;176:71–78.

    Article  PubMed  PubMed Central  Google Scholar 

  64. Maynard ME, Barton EA, Robinson CR, Wooden JI, Leasure JL. Sex differences in hippocampal damage, cognitive impairment, and trophic factor expression in an animal model of an alcohol use disorder. Brain Struct Funct. 2018;223:195–210.

    Article  CAS  PubMed  Google Scholar 

  65. Melbourne JK, Ryan Thompson K, Peng H, Nixon K. Its complicated: the relationship between alcohol and microglia in the search for novel pharmacotherapeutic targets for alcohol use disorders. Prog Mol Biol Transl Sci. 2019;167:179–221.

    Article  CAS  PubMed  Google Scholar 

  66. Lewis SA, Sureshchandra S, Doratt B, Jimenez VA, Stull C, Grant KA, et al. Transcriptional, epigenetic, and functional reprogramming of blood monocytes in non-human primates following chronic alcohol drinking. Front Immunol. 2021;12:724015.

  67. Messaoudi I, Asquith M, Engelmann F, Park B, Brown M, Rau A, et al. Moderate alcohol consumption enhances vaccine-induced responses in rhesus macaques. Vaccine. 2013;32:54–61.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. King AC, de Wit H, McNamara PJ, Cao D. Rewarding, stimulant, and sedative alcohol responses and relationship to future binge drinking. Arch Gen Psychiatry. 2011;68:389–99.

    Article  PubMed  PubMed Central  Google Scholar 

  69. King AC, McNamara PJ, Hasin DS, Cao D. Alcohol challenge responses predict future alcohol use disorder symptoms: a 6-year prospective study. Biol Psychiatry. 2014;75:798–806.

    Article  PubMed  Google Scholar 

  70. King A, Vena A, Hasin DS, deWit H, O’Connor SJ, Cao D. Subjective responses to alcohol in the development and maintenance of alcohol use disorder. Am J Psychiatry. 2021;178:560–71.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank the wonderful staff at the Yale PET center for their expertise and support of radiochemistry, metabolite analysis, and image acquisition. We also thank the staff at the Clinical Neuroscience Research Unit at the Connecticut Mental Health Center and the Hospital Research Unit at the Yale Clinical Center for Investigation for assistance with participant monitoring and evaluation. We thank Dr. Lesley Devine for support with cytokine assays.

Funding

We gratefully acknowledge the funding support from the National Institute on Alcohol Abuse and Alcoholism (K01AA024788; U54AA027989) and State of Connecticut Support for the Clinical Neuroscience Research Unit.

Author information

Authors and Affiliations

  1. Department of Radiology and Biomedical Imaging, Yale University, New Haven, CT, USA

    Nakul R. Raval, David Matuskey, Rachel Miller, Lindsey R. Drake, Michael Kapinos, Nabeel Nabulsi, Yiyun Huang, Richard E. Carson, Kelly P. Cosgrove & Ansel T. Hillmer

  2. Yale PET Center, Yale University, New Haven, CT, USA

    Nakul R. Raval, Gustavo Angarita, David Matuskey, Lindsey R. Drake, Michael Kapinos, Nabeel Nabulsi, Yiyun Huang, Richard E. Carson, Kelly P. Cosgrove & Ansel T. Hillmer

  3. Department of Psychiatry, Yale University, New Haven, CT, USA

    Gustavo Angarita, David Matuskey, Stephanie S. O’Malley, Kelly P. Cosgrove & Ansel T. Hillmer

  4. Department of Neurology, Yale University New Haven, New Haven, CT, USA

    David Matuskey

  5. Department of Biomedical Engineering, Yale School of Engineering and Applied Science, New Haven, CT, USA

    Richard E. Carson & Ansel T. Hillmer

Authors
  1. Nakul R. Raval
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gustavo Angarita
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. David Matuskey
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rachel Miller
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lindsey R. Drake
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Michael Kapinos
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Nabeel Nabulsi
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yiyun Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Richard E. Carson
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Stephanie S. O’Malley
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Kelly P. Cosgrove
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Ansel T. Hillmer
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

ATH, KPC, SSOM, REC: conceptualized study, oversaw data acquisition, NRR, LRD, and ATH: analyzed data, GA, DM: study physicians, RM, MK: key data acquisition and analysis contributions, NN and YH: senior radiochemists, NRR, SSOM, KPC, ATH: prepared initial manuscript draft and figures. All authors contributed edits and revisions to the final manuscript.

Corresponding author

Correspondence to Ansel T. Hillmer.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

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

Supplementary information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Raval, N.R., Angarita, G., Matuskey, D. et al. Imaging the brain’s immune response to alcohol with [11C]PBR28 TSPO Positron Emission Tomography. Mol Psychiatry 28, 3384–3390 (2023). https://doi.org/10.1038/s41380-023-02198-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41380-023-02198-6

Search

Advanced search

Quick links