Gender-dependent increases with healthy aging of the human cerebral cannabinoid-type 1 receptor binding using [18F]MK-9470 PET
Abstract
The endocannabinoid system (ECS) is implicated as a regulator of homeostasis of several cerebral functions and is a novel target for drug treatment of neuropyschiatric disorders. So far, the cerebral cannabinoid-type 1 receptor (CB1R) has only been studied using in vitro, animal model, electrophysiological and post-mortem data. We have used positron emission tomography (PET) using a high-affinity, subtype-selective radioligand, [(18)F]MK-9470, to assess the in vivo cerebral CB1R distribution and its variation with healthy aging and gender. Fifty healthy volunteers (25 M/25 F, 18-69 years) underwent [(18)F]MK-9470 PET. Parametric [(18)F]MK-9470 binding maps were constructed, corrected for partial volume effects and analyzed using statistical parametric mapping in a combined categorical (gender) and covariate (age) design. We found that [(18)F]MK-9470 binding to CB1R increased with aging but only in women (p(FWE)<0.05, corrected for multiple comparisons); this was most pronounced in the basal ganglia, lateral temporal cortex and limbic system, especially in the hippocampus. Men showed higher [(18)F]MK-9470 binding then women (p<0.001, uncorrected), in clusters of the limbic system and cortico-striato-thalamic-cortical circuit. Region-dependent and gender-related upregulation of [(18)F]MK-9470 binding with aging is in line with ex vivo findings in rodent studies and may be associated with a changing homeostatic capacity or compensation mechanisms in the ECS that is modulated by sex hormones. In vivo PET of the CB1R will likely improve our understanding of the ECS in several neurological and psychiatric disorders.
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The [18F]MK-9470 study found greater plasma parent fraction and higher normalized brain uptake (SUV) in men.
“That report found greater plasma parent fraction and higher normalized brain uptake (SUV) in men, which is consistent with our findings.”
From Elevated brain cannabinoid CB1 receptor availability in post-traumatic stress disorder: A positron emission tomography study (2013) · cites this paper as [59]
The current study's results are largely in agreement with a previous [18F]MK-9470 PET study on age and gender.
“Our results are largely in agreement with a previous study that used the CB1 PET tracer [18F]MK-9470 to investigate the effects of age and gender59.”
From Elevated brain cannabinoid CB1 receptor availability in post-traumatic stress disorder: A positron emission tomography study (2013) · cites this paper as [59]
Cites
Co-Planar Stereotaxic Atlas of the Human Brain
Talairach, J., & Tournoux, P. (1988) · Medical Entomology and Zoology · Cited by 11,798 · see citing works
International Union of Pharmacology. XXVII. Classification of Cannabinoid Receptors
Howlett, A. C., Barth, F., Bonner, T. I., Cabral, G., Casellas, P., Devane, W. A., Felder, C. C., Herkenham, M., Mackie, K., Martin, B. R., et al. (2002) · Pharmacological Reviews · doi:10.1124/pr.54.2.161 · Cited by 2,819 · see citing works
Cannabinoid receptor localization in brain.
Herkenham, M., Lynn, A. B., Little, M. D., Johnson, M. R., Melvin, L. S., de Costa, B. R., & Rice, K. C. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.5.1932 · Cited by 2,321 · see citing works
Herkenham, M., Lynn, A., Johnson, M., Melvin, L., de Costa, B., & Rice, K. (1991) · The Journal of Neuroscience · doi:10.1523/jneurosci.11-02-00563.1991 · Cited by 2,159 · see citing works
Identification and Functional Characterization of Brainstem Cannabinoid CB<sub>2</sub>Receptors
Van Sickle, M. D., Duncan, M., Kingsley, P. J., Mouihate, A., Urbani, P., Mackie, K., Stella, N., Makriyannis, A., Piomelli, D., Davison, J. S., et al. (2005) · Science · doi:10.1126/science.1115740 · Cited by 1,470 · see citing works
Endocannabinoid Signaling in the Brain
Wilson, R. I., & Nicoll, R. A. (2002) · Science · doi:10.1126/science.1063545 · Cited by 1,260 · see citing works
Pi-Sunyer, X., Aronne, L. J., Heshmati, H. M., Devin, J., Rosenstock, J., & for the RIO-North America Study Group (2006) · JAMA · doi:10.1001/jama.295.7.761 · Cited by 1,209 · see citing works
CB1 Cannabinoid Receptors and On-Demand Defense Against Excitotoxicity
Marsicano, G., Goodenough, S., Monory, K., Hermann, H., Eder, M., Cannich, A., Azad, S. C., Cascio, M. G., Gutiérrez, S. O., van der Stelt, M., et al. (2003) · Science · doi:10.1126/science.1088208 · Cited by 1,208 · see citing works
The endocannabinoid system and its therapeutic exploitation
Marzo, V. D., Bifulco, M., & Petrocellis, L. D. (2004) · Nature Reviews Drug Discovery · doi:10.1038/nrd1495 · Cited by 1,090 · see citing works
Glass, M., Faull, R. L. M., & Dragunow, M. (1997) · Neuroscience · doi:10.1016/s0306-4522(96)00428-9 · Cited by 1,052 · see citing works
Neuropsychology of fear and loathing
Calder, A. J., Lawrence, A. D., & Young, A. W. (2001) · Nature reviews. Neuroscience · doi:10.1038/35072584 · Cited by 927 · see citing works
Patterns of Hand Preference in a Student Population
Briggs, G. G., & Nebes, R. D. (1975) · Cortex · doi:10.1016/s0010-9452(75)80005-0 · Cited by 786 · see citing works
Müller‐Gärtner, H. W., Links, J. M., Prince, J. L., Bryan, R. N., McVeigh, E. R., Leal, J. P., Davatzikos, C. A., & Frost, J. J. (1992) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.1992.81 · Cited by 756 · see citing works
Iversen, L. L. (2003) · Brain · doi:10.1093/brain/awg143 · Cited by 735 · see citing works
Ibrahim, M. M., Porreca, F., Lai, J., Albrecht, P. J., Rice, F. L., Khodorova, A., Davar, G., Makriyannis, A., Vanderah, T. W., Mata, H. P., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0409888102 · Cited by 521 · see citing works
Effect of age and gender on the activity of human hepatic CYP3A
Hunt, C. M., Westerkam, W. R., & Stave, G. M. (1992) · Biochemical Pharmacology · doi:10.1016/0006-2952(92)90010-g · Cited by 426 · see citing works
Wang, L., Liu, J., Harvey-White, J. D., Zimmer, A., & Kunos, G. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0336351100 · Cited by 340 · see citing works
Burns, H. D., Laere, K. V., Bohorquez, S. M. S., Hamill, T. G., Bormans, G. M., Eng, W., Gibson, R. E., Ryan, C. N., Connolly, B., Patel, S., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0703472104 · Cited by 317 · see citing works
Self-citationWestlake, T. M., Howlett, A., Bonner, T., Matsuda, L., & Herkenham, M. (1994) · Neuroscience · doi:10.1016/0306-4522(94)90511-8 · Cited by 290 · see citing works
van der Stelt, M., & Marzo, V. D. (2003) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2003.08.101 · Cited by 286 · see citing works
de Fonseca, F. R., Cebeira, M., Ramos, J. A., Martín, M., & Fernández-Ruiz, J. J. (1994) · Life Sciences · doi:10.1016/0024-3205(94)00585-0 · Cited by 243 · see citing works
Quarantelli, M., Berkouk, K., Prinster, A., Landeau, B., Svarer, C., Balkay, L., Alfano, B., Brunetti, A., Baron, J., & Salvatore, M. (2004) · PubMed · Cited by 224 · see citing works
Anandamide, but not 2‐arachidonoylglycerol, accumulates during in vivo neurodegeneration
Hansen, H. H., Schmid, P. C., Bittigau, P., Lastres‐Becker, I., Berrendero, F., Manzanares, J., Ikonomidou, C., Schmid, H. H. O., Fernández‐Ruiz, J. J., & Hansen, H. S. (2001) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2001.00542.x · Cited by 215 · see citing works
Does cerebral blood flow decline in healthy aging? A PET study with partial-volume correction.
MELTZER, C. C., Cantwell, M. N., Greer, P. J., Ben-Eliezer, D., Smith, G. S., Frank, G., Kaye, W. H., Houck, P. R., & Price, J. C. (2000) · PubMed · Cited by 207 · see citing works
Leterrier, C., Lainé, J., Darmon, M. C., Boudin, H., Rossier, J., & Lenkei, Z. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.5437-05.2006 · Cited by 201 · see citing works
Agonist-Induced Internalization and Trafficking of Cannabinoid CB1Receptors in Hippocampal Neurons
Coutts, A. A., Anavi‐Goffer, S., Ross, R. A., MacEwan, D. J., Mackie, K., Pertwee, R. G., & Irving, A. J. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-07-02425.2001 · Cited by 176 · see citing works
van der Stelt, M., Veldhuis, W. B., Bär, P. R., Veldink, G. A., Vliegenthart, J. F. G., & Nicolay, K. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-17-06475.2001 · Cited by 176 · see citing works
Early age-related cognitive impairment in mice lacking cannabinoid CB1 receptors
Bilkei‐Gorzó, A., Rácz, I., Valverde, O., Otto, M., Michel, K., Sarstre, M., & Zimmer, A. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504640102 · Cited by 166 · see citing works
The ontogeny of cannabinoid receptors in the brain of postnatal and aging rats
Belue, R. C., Howlett, A. C., Westlake, T. M., & Hutchings, D. E. (1995) · Neurotoxicology and Teratology · doi:10.1016/0892-0362(94)00053-g · Cited by 154 · see citing works
Autoradiographic Study of Pre- and Postnatal Distribution of Cannabinoid Receptors in Human Brain
Biegon, A. R., & Kerman, I. A. (2001) · NeuroImage · doi:10.1006/nimg.2001.0939 · Cited by 135 · see citing works
Role of the endocannabinoid system in depression and suicide
Vinod, K. Y., & Hungund, B. L. (2006) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2006.08.006 · Cited by 132 · see citing works
Barrero, F. J., Ampuero, I., Morales, B., Vives, F., Luna, J. D. D., Hoenicka, J., & de Yébenes, J. G. (2005) · The Pharmacogenomics Journal · doi:10.1038/sj.tpj.6500301 · Cited by 117 · see citing works
11C-JHU75528: a radiotracer for PET imaging of CB1 cannabinoid receptors.
Horti, A. G., Fan, H. S., Kuwabara, H., Hilton, J., Ravert, H. T., Holt, D. P., Alexander, M., Kumar, A., Rahmim, A., Scheffel, U., et al. (2006) · PubMed · Cited by 113 · see citing works
Koeppe, R. A., Frey, K. A., Snyder, S. E., Meyer, P., Kilbourn, M. R., & Kuhl, D. E. (1999) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/00004647-199910000-00012 · Cited by 113 · see citing works
Mani, S. K. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.031563998 · Cited by 92 · see citing works
Yasuno, F., Brown, A. K., Zoghbi, S. S., Krushinski, J. H., Chernet, E., Tauscher, J. T., Schaus, J. M., Phebus, L. A., Chesterfield, A. K., Felder, C. C., et al. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301402 · Cited by 88 · see citing works
Romero, J., Berrendero, F., Garcı́a-Gil, L., de la Cruz, P., Ramos, J. A., & Fernández‐Ruíz, J. (1998) · Neuroscience · doi:10.1016/s0306-4522(97)00552-6 · Cited by 86 · see citing works
Changes in cannabinoid receptor binding and mRNA levels in several brain regions of aged rats
Berrendero, F., Romero, J., Garcı́a-Gil, L., Suarez, I., la Cruz, P. D., Ramos, J. A., & Fernández‐Ruíz, J. (1998) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/s0925-4439(98)00042-8 · Cited by 85 · see citing works
Endocannabinoids Mediate the Effects of Acute Stress and Corticosterone on Sex Behavior
Coddington, E. J., Lewis, C. M., Rose, J. D., & Moore, F. L. (2006) · Endocrinology · doi:10.1210/en.2006-0740 · Cited by 78 · see citing works
Maccarrone, M., Attinà, M., Bari, M., Cartoni, A., Ledent, C. A., & Finazzi‐Agrò, A. (2001) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2001.00413.x · Cited by 68 · see citing works
Van Laere, K. J., & Dierckx, R. A. (2001) · Radiology · doi:10.1148/radiol.2213010295 · Cited by 67 · see citing works
In vivo muscarinic 2 receptor imaging in cognitively normal young and older volunteers
Podruchny, T. A., Connolly, C., Bokde, A. L. W., Herscovitch, P., Eckelman, W. C., Kiesewetter, D. O., Sunderland, T., Carson, R. E., & Cohen, R. M. (2003) · Synapse · doi:10.1002/syn.10165 · Cited by 66 · see citing works
Characterization of CB1 cannabinoid receptor immunoreactivity in postmortem human brain homogenates
de Jesús, M. L., Sallés, J., Meana, J. J., & Callado, L. F. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.02.024 · Cited by 56 · see citing works
Mato, S., & Pazos, Á. (2004) · Neuropharmacology · doi:10.1016/j.neuropharm.2003.11.004 · Cited by 53 · see citing works
An increase of sigma1 receptors in the aged monkey brain
Kawamura, K., Kimura, Y., Tsukada, H., Kobayashi, T., Nishiyama, S., Kakiuchi, T., Ohba, H., Harada, N., Matsuno, K., Ishii, K., et al. (2002) · Neurobiology of Aging · doi:10.1016/s0197-4580(02)00152-5 · Cited by 53 · see citing works
Liu, P., Bilkey, D. K., Darlington, C. L., & Smith, P. F. (2003) · Brain Research · doi:10.1016/s0006-8993(03)02872-5 · Cited by 52 · see citing works
The Endocannabinoid System in Ageing: A New Target for Drug Development
Paradisi, A., Oddi, S., & Maccarrone, B. S. P. (2006) · Current Drug Targets · doi:10.2174/1389450110607011539 · Cited by 41 · see citing works
González, S. R., Mena, M. A., Lastres‐Becker, I., Serrano, A., de Yébenes, J. G., Ramos, J. A., & Fernández‐Ruíz, J. (2005) · Brain Research · doi:10.1016/j.brainres.2005.04.010 · Cited by 35 · see citing works
Marx, J. L. (2006) · Science · doi:10.1126/science.311.5759.322 · Cited by 23 · see citing works
Laere, K. V. (2007) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-007-0505-3 · Cited by 20 · see citing works
Gender-specific considerations in the treatment of mood disorders in women across the life cycle.
Cohen, L. S. (2003) · PubMed · Cited by 12 · see citing works
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2 of the 53 references couldn’t be matched to a known paper.
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Hermanns‐Clausen, M., Kneisel, S., Szabó, B., & Auwärter, V. (2012) · Addiction · doi:10.1111/j.1360-0443.2012.04078.x · Cited by 478 · see citing works
Neumeister, A., Normandin, M. D., Pietrzak, R. H., Piomelli, D., Zheng, M. Q., Gujarro-Anton, A., Potenza, M. N., Bailey, C. R., Lin, S. F., Najafzadeh, S., et al. (2013) · Molecular Psychiatry · doi:10.1038/mp.2013.61 · Cited by 361 · see citing works
Sex-Dependent Effects of Cannabis and Cannabinoids: A Translational Perspective
Cooper, Z. D., & Craft, R. M. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2017.140 · Cited by 350 · see citing works
Crane, N. A., Schuster, R. M., Fusar‐Poli, P., & González, R. (2012) · Neuropsychology Review · doi:10.1007/s11065-012-9222-1 · Cited by 310 · see citing works
Cortical surface-based analysis reduces bias and variance in kinetic modeling of brain PET data
Greve, D. N., Svarer, C., Fisher, P. M., Feng, L., Hansen, A. E., Baare, W., Rosen, B., Fischl, B., & Knudsen, G. M. (2014) · NeuroImage · doi:10.1016/j.neuroimage.2013.12.021 · Cited by 264 · see citing works
Wong, D. F., Kuwabara, H., Horti, A. G., Raymont, V., Brašić, J. R., Guevara, M. C., Ye, W., Dannals, R. F., Ravert, H. T., Nandi, A., et al. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.04.034 · Cited by 204 · see citing works
Adolescent exposure to THC in female rats disrupts developmental changes in the prefrontal cortex
Rubino, T., Prini, P., Piscitelli, F., Zamberletti, E., Trusel, M., Melis, M., Sagheddu, C., Ligresti, A., Tonini, R., Marzo, V. D., et al. (2014) · Neurobiology of Disease · doi:10.1016/j.nbd.2014.09.015 · Cited by 191 · see citing works
Functional consequences of marijuana use in adolescents
Jacobus, J., Bava, S., Cohen‐Zion, M., Mahmood, O. M., & Tapert, S. F. (2009) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2009.04.001 · Cited by 185 · see citing works
A Gender Perspective of Addictive Disorders
Fonseca, F., Robles-Martínez, M., Tirado-Muñoz, J., Alías-Ferri, M., Mestre-Pintó, J. I., Coratu, A. M., & Torrens, M. (2021) · Current Addiction Reports · doi:10.1007/s40429-021-00357-9 · Cited by 192 · see citing works
Lisdahl, K. M., McQueeny, T. M., Nagel, B. J., Hanson, K. L., Yang, T. T., & Tapert, S. F. (2009) · Addiction Biology · doi:10.1111/j.1369-1600.2009.00166.x · Cited by 157 · see citing works
The endocannabinoid system in normal and pathological brain ageing
Bilkei‐Gorzó, A. (2012) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2011.0388 · Cited by 157 · see citing works
Schier, A. R. D. M., Ribeiro, N. D. C. R., Coutinho, D. C. O., Machado, S. E. D. C., Arias-Carrión, Ó., Crippa, J. A. S., Zuardi, A. W., Nardi, A. E., & Silva, A. R. (2014) · CNS & Neurological Disorders - Drug Targets · doi:10.2174/1871527313666140612114838 · Cited by 154 · see citing works
[18 F ] MK ‐9470 PET measurement of cannabinoid CB 1 receptor availability in chronic cannabis users
Ceccarini, J., Kuepper, R., Kemels, D., van Os, J., Henquet, C., & Laere, K. V. (2013) · Addiction Biology · doi:10.1111/adb.12116 · Cited by 149 · see citing works
Castelli, M. P., Fadda, P., Casu, A., Spano, M. S., Casti, A., Fratta, W., & Fattore, L. (2014) · Current Pharmaceutical Design · doi:10.2174/13816128113199990430 · Cited by 148 · see citing works
Normandin, M. D., Zheng, M., Lin, K., Mason, N. S., Lin, S.-F., Ropchan, J. R., Labaree, D. C., Henry, S. E., Williams, W. A., Carson, R. E., et al. (2015) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2015.46 · Cited by 141 · see citing works
Sex differences and the endocannabinoid system in pain
Blanton, H. L., Barnes, R. C., McHann, M. C., Bilbrey, J. A., Wilkerson, J. L., & Guindon, J. (2021) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2021.173107 · Cited by 143 · see citing works
Abnormal cerebellar morphometry in abstinent adolescent marijuana users
Lisdahl, K. M., Nagel, B. J., & Tapert, S. F. (2010) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2009.12.004 · Cited by 138 · see citing works
Widespread Decrease of Type 1 Cannabinoid Receptor Availability in Huntington Disease In Vivo
Laere, K. V., Casteels, C., Dhollander, I., Goffin, K. E., Grachev, I. D., Bormans, G. M., & Vandenberghe, W. (2010) · Journal of Nuclear Medicine · doi:10.2967/jnumed.110.077156 · Cited by 122 · see citing works
Self-citationRegional changes in type 1 cannabinoid receptor availability in Parkinson's disease in vivo
Laere, K. V., Casteels, C., Lunskens, S., Goffin, K. E., Grachev, I. D., Bormans, G. M., & Vandenberghe, W. (2011) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2011.02.009 · Cited by 120 · see citing works
Self-citationMechanisms Underlying Sex Differences in Cannabis Use
Calakos, K. C., Bhatt, S., Foster, D. W., & Cosgrove, K. (2017) · Current Addiction Reports · doi:10.1007/s40429-017-0174-7 · Cited by 121 · see citing works
Sex difference in brain CB1 receptor availability in man
Laurikainen, H., Tuominen, L. J., Tikka, M., Merisaari, H., Armio, R.-L., Sormunen, E., Borgan, F., Veronese, M., Howes, O. D., Haaparanta‐Solin, M., et al. (2018) · NeuroImage · doi:10.1016/j.neuroimage.2018.10.013 · Cited by 118 · see citing works
Ceccarini, J., Hompes, T., Verhaeghen, A., Casteels, C., Peuskens, H., Bormans, G., Claes, S., & Van Laere, K. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.0849-13.2014 · Cited by 111 · see citing works
Self-citationSexually Dimorphic Effects of Cannabinoid Compounds on Emotion and Cognition
Rubino, T., & Parolaro, D. (2011) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2011.00064 · Cited by 106 · see citing works
Ceccarini, J., Binder, M. D., van Winkel, R., Peuskens, J., Bormans, G. M., Kranaster, L., Enning, F., Koethe, D., Leweke, F. M., & Laere, K. V. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2013.04.052 · Cited by 108 · see citing works
Self-citationTowards a neurocircuitry in anorexia nervosa: Evidence from functional neuroimaging studies
van Kuyck, K., Gérard, N., Laere, K. V., Casteels, C., Pieters, G., Gabriëls, L. A., & Nuttin, B. (2009) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2009.04.005 · Cited by 106 · see citing works
Self-citationGi/o-Protein Coupled Receptors in the Aging Brain
de Oliveira, P. G., Ramos, M. L., Amaro, A. J. M., Dias, R. A., & Vieira, S. I. (2019) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2019.00089 · Cited by 106 · see citing works
Terry, G. E., Liow, J., Zoghbi, S. S., Hirvonen, J., Farris, A. G., Lerner, A., Tauscher, J. T., Schaus, J. M., Phebus, L. A., Felder, C. C., et al. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2009.06.059 · Cited by 106 · see citing works
Morgan, C. J. A., Freeman, T. P., Powell, J. F., & Curran, H. V. (2016) · Translational Psychiatry · doi:10.1038/tp.2015.219 · Cited by 101 · see citing works
Terry, G. E., Hirvonen, J., Liow, J., Zoghbi, S. S., Gladding, R. L., Tauscher, J. T., Schaus, J. M., Phebus, L. A., Felder, C. C., Morse, C. L., et al. (2009) · Journal of Nuclear Medicine · doi:10.2967/jnumed.109.067074 · Cited by 101 · see citing works
Lorenzetti, V., Solowij, N., Fornito, A., Lubman, D. I., & Yücel, M. (2014) · Current Pharmaceutical Design · doi:10.2174/13816128113199990435 · Cited by 96 · see citing works
Cannabinoids as anticancer therapeutic agents
Kovalchuk, O., & Kovalchuk, I. (2020) · Cell Cycle · doi:10.1080/15384101.2020.1742952 · Cited by 96 · see citing works
In vivo activation of endocannabinoid system in temporal lobe epilepsy with hippocampal sclerosis
Goffin, K. E., Paesschen, W. V., & Laere, K. V. (2011) · Brain · doi:10.1093/brain/awq385 · Cited by 88 · see citing works
Self-citationKeeney, B. K., Raichlen, D. A., Meek, T. H., Wijeratne, R. S., Middleton, K. M., Gerdeman, G. L., & Garland, T. (2008) · Behavioural Pharmacology · doi:10.1097/fbp.0b013e32831c3b6b · Cited by 86 · see citing works
Endocannabinoids, cannabinoids and the regulation of anxiety
Petrie, G. N., Nastase, A. S., Aukema, R. J., & Hill, M. N. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108626 · Cited by 85 · see citing works
Wright, M., Ciano, P. D., & Brands, B. (2020) · Cannabis and Cannabinoid Research · doi:10.1089/can.2019.0052 · Cited by 85 · see citing works
Neumeister, A., Normandin, M. D., Murrough, J. W., Henry, S. E., Bailey, C. R., Luckenbaugh, D. A., Tuit, K. L., Zheng, M., Galatzer‐Levy, I. R., Sinha, R., et al. (2012) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2012.01815.x · Cited by 73 · see citing works
Preclinical evaluation of [11C]NE40, a type 2 cannabinoid receptor PET tracer
Evens, N., Vandeputte, C., Coolen, C., Janssen, P., Sciot, R., Baekelandt, V., Verbruggen, A., Debyser, Z., Laere, K. V., & Bormans, G. M. (2011) · Nuclear Medicine and Biology · doi:10.1016/j.nucmedbio.2011.09.005 · Cited by 73 · see citing works
Self-citationSex‐dependent effects of endocannabinoid modulation of conditioned fear extinction in rats
Morena, M., Nastase, A. S., Santori, A., Cravatt, B. F., Shansky, R. M., & Hill, M. N. (2020) · British Journal of Pharmacology · doi:10.1111/bph.15341 · Cited by 70 · see citing works
In vivo type 1 cannabinoid receptor availability in Alzheimer's disease
Ahmad, R. U., Goffin, K. E., den Stock, J. V., Winter, F. D., Cleeren, E., Bormans, G. M., Tournoy, J., Persoons, P., Laere, K. V., & Vandenbulcke, M. (2013) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2013.10.002 · Cited by 70 · see citing works
Self-citationUse of Cannabis and Cannabinoids for Treatment of Cancer
Cherkasova, V., Wang, B., Gerasymchuk, M., Fiselier, A., Kovalchuk, O., & Kovalchuk, I. (2022) · Cancers · doi:10.3390/cancers14205142 · Cited by 70 · see citing works
Laere, K. V., Goffin, K. E., Bormans, G. M., Casteels, C., Mortelmans, L., Hoon, J. N. J. M. D., Grachev, I. D., Vandenbulcke, M., & Pieters, G. (2009) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2008.530 · Cited by 67 · see citing works
Self-citationNey, L. J., Matthews, A. J., Bruno, R., & Felmingham, K. L. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.07.006 · Cited by 66 · see citing works
Hou, L., Rong, J., Haider, A., Ogasawara, D., Varlow, C., Schafroth, M. A., Mu, L., Gan, J., Xu, H., Fowler, C. J., et al. (2020) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.0c01459 · Cited by 63 · see citing works
Advancing the science on cannabis concentrates and behavioural health
Bidwell, L. C., Martin‐Willett, R., & Karoly, H. C. (2021) · Drug and Alcohol Review · doi:10.1111/dar.13281 · Cited by 60 · see citing works
Virdee, K., Cumming, P. D., Caprioli, D., Jupp, B., Rominger, A., Aigbirhio, F. I., Fryer, T. D., Riss, P. J., & Dalley, J. W. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2012.01.009 · Cited by 60 · see citing works
Acute effects of partial CB1 receptor agonists on cognition – A meta-analysis of human studies
Zhornitsky, S., Pelletier, J., Assaf, R., Giroux, S., Li, C.-S. R., & Potvin, S. (2020) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2020.110063 · Cited by 54 · see citing works
Kinetic analysis of the cannabinoid-1 receptor PET tracer [18F]MK-9470 in human brain
Bohorquez, S. M. S., Hamill, T. G., Goffin, K. E., Lepeleire, I. D., Bormans, G. M., Burns, H. D., & Laere, K. V. (2009) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-009-1340-5 · Cited by 52 · see citing works
Self-citationCannabis Use: Neurobiological, Behavioral, and Sex/Gender Considerations
Nia, A. B., Mann, C. L., Kaur, H., & Ranganathan, M. (2018) · Current Behavioral Neuroscience Reports · doi:10.1007/s40473-018-0167-4 · Cited by 51 · see citing works
Mu, L., Bieri, D., Slavik, R., Drandarov, K., Herde, A. M., Čermak, S., Weber, M., Schibli, R., Krämer, S. D., & Ametamey, S. M. (2013) · Journal of Neurochemistry · doi:10.1111/jnc.12354 · Cited by 50 · see citing works
Ly, H. G., Ceccarini, J., Weltens, N., Bormans, G., van Laere, K., Tack, J., & van Oudenhove, L. (2015) · Psychotherapy and Psychosomatics · doi:10.1159/000375454 · Cited by 44 · see citing works
Self-citationGoffin, K. E., Paesschen, W. V., Dupont, P. J., Baete, K., Palmini, A., Nuyts, J. L., & Laere, K. V. (2010) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-010-1405-5 · Cited by 48 · see citing works
Self-citationCeccarini, J., Weltens, N., Ly, H. G., Tack, J. F., Oudenhove, L. V., & Laere, K. V. (2016) · Translational Psychiatry · doi:10.1038/tp.2016.118 · Cited by 45 · see citing works
Jacobson, M. R., Watts, J. J., Boileau, I., Tong, J., & Mizrahi, R. (2019) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2018.12.014 · Cited by 45 · see citing works
Is There a Role for GPCR Agonist Radiotracers in PET Neuroimaging?
Colom, M., Vidal, B., & Zimmer, L. (2019) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2019.00255 · Cited by 44 · see citing works
The Modulating Role of Sex and Anabolic-Androgenic Steroid Hormones in Cannabinoid Sensitivity
Struik, D., Sanna, F., & Fattore, L. (2018) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2018.00249 · Cited by 42 · see citing works
Aging circadian rhythms and cannabinoids
Hodges, E. L., & Ashpole, N. M. (2019) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2019.03.008 · Cited by 43 · see citing works
Tirado-Muñoz, J., López-Rodríguez, A. B., Fonseca, F., Farré, M., Torrens, M., & Viveros, M. (2020) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2020.100841 · Cited by 42 · see citing works
Verdurand, M., Nguyen, V., Stark, D., Zahra, D., Grégoire, M., Greguric, I. D., & Zavitsanou, K. (2011) · International Journal of Molecular Imaging · doi:10.1155/2011/548123 · Cited by 41 · see citing works
Lichenstein, S. D. (2022) · Current Addiction Reports · doi:10.1007/s40429-022-00450-7 · Cited by 38 · see citing works
PET imaging in multiple sclerosis
Faria, D. D. P., Copray, S. C. V. M., Buchpiguel, C. A., Dierckx, R., & de Vries, E. F. J. (2014) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-014-9544-2 · Cited by 37 · see citing works
Cannabinoids: Revealing their complexity and role in central networks of fear and anxiety
Murkar, A., Koninck, J. D., & Merali, Z. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.09.002 · Cited by 34 · see citing works
Exogenous and Endogenous Cannabinoids Suppress Inhibitory Neurotransmission in the Human Neocortex
Kovacs, F. E., Knop, T., Urbanski, M. J., Freiman, I., Freiman, T. M., Feuerstein, T. J., Zentner, J., & Szabó, B. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.262 · Cited by 34 · see citing works
Tactics for preclinical validation of receptor-binding radiotracers
Lever, S. Z., Fan, K.-H., & Lever, J. R. (2016) · Nuclear Medicine and Biology · doi:10.1016/j.nucmedbio.2016.08.015 · Cited by 33 · see citing works
Pushkin, A. N., Dukes, A. J., Lallai, V., Torres-Mendoza, A., Fowler, J. P., Chen, E., & Fowler, C. D. (2019) · PLoS ONE · doi:10.1371/journal.pone.0211346 · Cited by 31 · see citing works
Ceccarini, J., Casteels, C., Ahmad, R. U., Crabbé, M., de Vliet, L. V., Vanhaute, H., Vandenbulcke, M., Vandenberghe, W., & Laere, K. V. (2019) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-019-04445-x · Cited by 31 · see citing works
Self-citationRisk Factors for Cannabis-Related Mental Health Harms in Older Adults: A Review
Hudson, A., & Hudson, P. (2020) · Clinical Gerontologist · doi:10.1080/07317115.2020.1808134 · Cited by 30 · see citing works
Dow-Edwards, D. L., Frank, A., Wade, D., Weedon, J., & Izenwasser, S. (2016) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2016.09.004 · Cited by 29 · see citing works
Enhancing effects of acute exposure to cannabis smoke on working memory performance
Blaes, S. L., Orsini, C. A., Holik, H., Stubbs, T., Ferguson, S. N., Heshmati, S. C., Bruner, M. M., Wall, S. C., Febo, M., Bruijnzeel, A. W., et al. (2018) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.12.001 · Cited by 26 · see citing works
Interictal Type 1 Cannabinoid Receptor Binding is Increased in Female Migraine Patients
der Schueren, B. V., Laere, K. V., Gérard, N., Bormans, G. M., & Hoon, J. N. J. M. D. (2011) · Headache The Journal of Head and Face Pain · doi:10.1111/j.1526-4610.2011.02030.x · Cited by 29 · see citing works
Self-citationCasteels, C., Koole, M. J. B., Celen, S., Bormans, G. M., & Laere, K. V. (2012) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-012-2163-3 · Cited by 26 · see citing works
Self-citationLipid endocannabinoids in energy metabolism, stress and developmental programming
de Almeida, M. M., Dias-Rocha, C. P., Calviño, C., & Trevenzoli, I. H. (2021) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2021.111522 · Cited by 27 · see citing works
Gender Differences in Dual Diagnoses Associated with Cannabis Use: A Review
Arenas, L. P., Díaz, I., & Arenas, M. C. (2022) · Brain Sciences · doi:10.3390/brainsci12030388 · Cited by 26 · see citing works
Ginsburg, B. C., & Hensler, J. G. (2022) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2022.173339 · Cited by 25 · see citing works
Helin, J. S., Lopez‐Picon, F. R., Kirjavainen, A. K., Pihlaja, R., Snellman, A., Ishizu, T., Löyttyniemi, E., Solin, O. H., Rinne, J. O., & Haaparanta‐Solin, M. (2018) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2018.05.013 · Cited by 25 · see citing works
Gérard, N., Ceccarini, J., Bormans, G. M., Vanbilloen, B., Casteels, C., Goffin, K. E., Bosier, B., Lambert, D. M., & Laere, K. V. (2010) · Journal of Molecular Neuroscience · doi:10.1007/s12031-010-9340-2 · Cited by 25 · see citing works
Self-citationSalort, G., Hernández‐Hernández, E., García-Fuster, M. J., & Garcı́a-Sevilla, J. A. (2020) · Journal of Affective Disorders · doi:10.1016/j.jad.2020.07.074 · Cited by 21 · see citing works
Mu, L., Slavik, R., Herde, A. M., Popaj, K., Čermak, S., Weber, M., Schibli, R., Krämer, S. D., & Ametamey, S. M. (2014) · Pharmaceuticals · doi:10.3390/ph7030339 · Cited by 20 · see citing works
Interaction of Cannabis Use and Aging: From Molecule to Mind
Yoo, H. B., DiMuzio, J. M., & Filbey, F. M. (2019) · Journal of Dual Diagnosis · doi:10.1080/15504263.2019.1665218 · Cited by 19 · see citing works
Radhakrishnan, R., Worhunsky, P. D., Zheng, M., Najafzadeh, S., Gallezot, J., Planeta, B. M., Henry, S. E., Nabulsi, N., Ranganathan, M., Skosnik, P. D., et al. (2022) · NeuroImage · doi:10.1016/j.neuroimage.2022.119674 · Cited by 18 · see citing works
Ertl, N., Lawn, W., Mokrysz, C., Freeman, T. P., Alnagger, N., Borissova, A., Fernandez‐Vinson, N., Lees, R., Ofori, S., Petrilli, K., et al. (2023) · Journal of Psychopharmacology · doi:10.1177/02698811231189441 · Cited by 18 · see citing works
Manca, C., Carta, G., Murru, E., Abolghasemi, A., Ansar, H., Errigo, A., Cani, P. D., Banni, S., & Pes, G. M. (2021) · GeroScience · doi:10.1007/s11357-021-00342-0 · Cited by 18 · see citing works
Sex differences in the acute effects of intravenous (IV) delta-9 tetrahydrocannabinol (THC)
Nia, A. B., Orejarena, M. J., Flynn, L. T., Luddy, C., D’Souza, D. C., Skosnik, P. D., Pittman, B. P., & Ranganathan, M. (2022) · Psychopharmacology · doi:10.1007/s00213-022-06135-3 · Cited by 17 · see citing works
The circulating and central endocannabinoid system in obesity and weight loss
Mattelaer, N., der Schueren, B. V., Oudenhove, L. V., Weltens, N., & Vangoitsenhoven, R. (2024) · International Journal of Obesity · doi:10.1038/s41366-024-01553-z · Cited by 16 · see citing works
Lahdenpohja, S., Rajala, N., Helin, J. S., Haaparanta‐Solin, M., Solin, O. H., Lopez‐Picon, F. R., & Kirjavainen, A. K. (2020) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.0c00313 · Cited by 17 · see citing works
Fuentes, J. J., Mayans, J., Guarro, M., Canosa, I., Mestre-Pintó, J. I., Fonseca, F., & Torrens, M. (2024) · BMC Psychiatry · doi:10.1186/s12888-024-05986-8 · Cited by 14 · see citing works
Vulnerability Factors for the Psychiatric and Behavioral Effects of Cannabis
Bortolato, M., Bini, V., & Tambaro, S. (2010) · Pharmaceuticals · doi:10.3390/ph3092799 · Cited by 14 · see citing works
Aghaei, A. M., Spillane, L. U., Pittman, B. P., Flynn, L. T., Aquino, J. P. D., Nia, A. B., & Ranganathan, M. (2024) · Psychopharmacology · doi:10.1007/s00213-024-06625-6 · Cited by 13 · see citing works
Murray, C. J., Vecchiarelli, H. A., & Tremblay, M. (2023) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2023.1119552 · Cited by 12 · see citing works
Gender Differences in Cannabis Addiction and Dependence
Davis, C. A., & Fattore, L. (2015) · Springer eBooks · doi:10.1007/978-1-4939-2294-9_12 · Cited by 12 · see citing works
PET Imaging of Endocannabinoid System
Horti, A. G., Raymont, V., & Terry, G. E. (2014) · Springer eBooks · doi:10.1007/978-3-642-42014-6_11 · Cited by 11 · see citing works
Effects of cannabis smoke and oral Δ9THC on cognition in young adult and aged rats
Zequeira, S., Gazarov, E. A., Güvenli, A. A., Berthold, E. C., Senetra, A. S., Febo, M., Hiranita, T., McMahon, L. R., Sharma, A., McCurdy, C. R., et al. (2025) · Psychopharmacology · doi:10.1007/s00213-025-06754-6 · Cited by 10 · see citing works
Endocannabinoid System Biomarkers in Alzheimer's Disease
Ferreira, P. C. L., Bellaver, B., Povala, G., Brum, W. S., Tissot, C., Badji, A., Sloan, M. E., Benedet, A. L., Rosa‐Neto, P., Ashton, N. J., et al. (2022) · Cannabis and Cannabinoid Research · doi:10.1089/can.2022.0151 · Cited by 10 · see citing works
Beyond monoamines: II. Novel applications for PET imaging in psychiatric disorders
Royse, S. K., Lopresti, B. J., Mathis, C. A., Tollefson, S., & Narendran, R. (2022) · Journal of Neurochemistry · doi:10.1111/jnc.15657 · Cited by 10 · see citing works
Gräfe, E. L., Reid, H. M. O., Shkolnikov, I., Conway, K., Kit, A., Acosta, C., & Christie, B. R. (2023) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2023.101076 · Cited by 10 · see citing works
Wong, D. F., Kuwabara, H., Horti, A. G., Raymont, V., Brašić, J. R., Guevara, M. C., Nandi, A., Rahmim, A., Ming, J. E., & Cascella, N. G. (2010) · Journal of Nuclear Medicine · Cited by 10 · see citing works
Cannabinoids for the Treatment of Movement Disorders
Catlow, B. J., & Sanchez‐Ramos, J. (2015) · Current Treatment Options in Neurology · doi:10.1007/s11940-015-0370-5 · Cited by 8 · see citing works
Ceccarini, J., Koole, M. J. B., & Laere, K. V. (2022) · Addiction Biology · doi:10.1111/adb.13167 · Cited by 7 · see citing works
Clinical pattern of synthetic cannabinoids users in Upper Egypt: cross-sectional study
Abdelmoneim, W. M., Ghandour, N., Fawzy, M., Mohammed, M. K., Ramadan, A. G., & Abdellah, N. Z. (2022) · Middle East Current Psychiatry · doi:10.1186/s43045-022-00188-y · Cited by 7 · see citing works
Correlations of the CNR1 Gene with Personality Traits in Women with Alcohol Use Disorder
Maciocha, F., Suchanecka, A., Chmielowiec, K., Chmielowiec, J., Ciechanowicz, A., & Boroń, A. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25105174 · Cited by 6 · see citing works
Antinori, S., & Fattore, L. (2017) · Springer eBooks · doi:10.1007/978-3-319-57371-7_2 · Cited by 6 · see citing works
- Authors
- Van Laere, K., Goffin, K., Casteels, C., Dupont, P., Mortelmans, L., de Hoon, J., & Bormans, G.
- Affiliations
- Universitair Ziekenhuis Leuven (BE)
- KU Leuven (BE)
- Venue
- NeuroImage
- Publisher
- Elsevier BV
- Published
- 2008-02
- Volume
- 39
- Issue
- 4
- Pages
- 1533-1541
- ISSN
- 1053-8119 (ISSN-L)
- OpenAlex
- W2088851718
- Cited by
- 142
- References
- 53
- Citations by year
- 2026: 7 · 2025: 6 · 2024: 9 · 2023: 8 · 2022: 14 · 2021: 8 · 2020: 10 · 2019: 8 · 2018: 7 · 2017: 3 · 2016: 4 · 2015: 4 · 2014: 11 · 2013: 11 · 2012: 6
- FWCI
- 3.72
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- NeuroImage (publishedVersion)
- PubMed (publishedVersion)
- Lirias (submittedVersion)
- Topics
- Health Sciences › Medicine › Pharmacology › Cannabis and Cannabinoid Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- cannabinoid type 1 receptor, CB1R, endocannabinoid system, healthy aging, sex differences, positron emission tomography, hippocampus, basal ganglia, limbic system, sex hormones, receptor binding
- MeSH terms
- Adolescent, Adult, Aged, Aging, Brain, Brain Chemistry, Female, Humans, Image Processing, Computer-Assisted, Magnetic Resonance Imaging, Male, Middle Aged, Pyridines, Reference Values, Sex Characteristics, Radiopharmaceuticals, Area Under Curve, Receptor, Cannabinoid, CB1, Positron-Emission Tomography
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