Cannabinoid receptors in rat brain areas: sexual differences, fluctuations during estrous cycle and changes after gonadectomy and sex steroid replacement.
Abstract
Cannabinoid effects on brain dopaminergic activity vary as a function of gonadal status. In this work, we examined whether these variations might be due to sex steroid-dependent differences in brain cannabinoid receptors (CNr). Four experiments were done: (i) male versus females; (ii) females at each stage of the ovarian cycle; (iii) estradiol (E2) and/or progesterone (P)-replaced ovariectomized (OVX) females; and (iv) testosterone (T)-replaced orchidectomized males. The density of CNr in the medial basal hypothalamus fluctuated in females during the estrous cycle. The density was higher in diestrus and decreased in estrus. This parameter did not change after ovariectomy and E2 replacement. However, P increased the density of CNr when administered to OVX rats acutely treated with E2, but not administered alone or after chronic E2 treatment. In the striatum, the affinity of CNr was slightly higher in males than females, with no changes in density. Ovariectomy increased the affinity of CNr, which normalized only after administration of acute E2. Interestingly, the high affinity values observed in this area after P alone or combined with E2, corresponded to low densities as compared with intact females. In the limbic forebrain, the affinity for the cannabinoid ligand was also higher in males than females with no changes in density. Affinity was also higher in diestrus and lower in estrus, whereas density was unchanged. Ovariectomy decreased CNr density. A normal situation was found after administration of acute E2 or P alone, whereas chronic E2 markedly increased the density of CNr as compared with both intact and OVX females. Interestingly, this latter increase was prevented by coadministration of P. Orchidectomy did not affect CNr density, but administration of T produced a marked decrease. In the mesencephalon, the density and affinity of CNr was higher in males than females. Administration of P to OVX rats produced opposite effects, increasing the density when administered alone and decreasing it when administered to acute E2-replaced OVX rats. In summary, these results reveal the existence of subtle, sometimes more pronounced, sex dimorphisms, fluctuations along the ovarian cycle and changes after gonadectomy and sex steroid replacement in CNr density and affinity in certain brain areas. This supports the hypothesis of possible sex steroid-dependent differences in the sensitivity of certain neuronal processes to cannabinoid treatment.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Ovarian cyclical changes in cannabinoid receptor density or endocannabinoid content occur in brain areas potentially associated with nociception.
“both studies observed ovarian cyclical changes in cannabinoid receptor density or endocannabinoid content in brain areas potentially associated with nociception, [8,44].”
From Endocannabinoid involvement in endometriosis. (2010) · cites this paper as [44]
Cites
PROTEIN MEASUREMENT WITH THE FOLIN PHENOL REAGENT
Lowry, O. H., Rosebrough, N., Farr, A. L., & Randall, R. (1951) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)52451-6 · Cited by 315,771 · see citing works
Isolation and Structure of a Brain Constituent That Binds to the Cannabinoid Receptor
Devane, W. A., Hanuš, L., Breuer, A., Pertwee, R. G., Stevenson, L. A., Griffin, G., Gibson, D., Mandelbaum, A., Etinger, A., & Mechoulam, R. (1992) · Science · doi:10.1126/science.1470919 · Cited by 5,633 · see citing works
REGIONAL STUDIES OF CATECHOLAMINES IN THE RAT BRAIN‐I
Glowinski, J., & Iversen, L. L. (1966) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1966.tb09873.x · Cited by 5,436 · see citing works
Structure of a cannabinoid receptor and functional expression of the cloned cDNA
Matsuda, L. A., Lolait, S. J., Brownstein, M. J., Young, A. C., & Bonner, T. I. (1990) · Nature · doi:10.1038/346561a0 · Cited by 5,011 · see citing works
Determination and characterization of a cannabinoid receptor in rat brain
Devane, W. A., Dysarz, F. A., Johnson, M. R., Melvin, L. S., & Howlett, A. C. (1988) · Molecular Pharmacology · doi:10.1016/s0026-895x(25)09876-1 · Cited by 2,443 · 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
Neuronal localization of cannabinoid receptors in the basal ganglia of the rat
Herkenham, M. A., Lynn, A. B., de Costa, B. R., & Richfield, E. K. (1991) · Brain Research · doi:10.1016/0006-8993(91)90970-7 · Cited by 515 · see citing works
Involvement of Gi in the inhibition of adenylate cyclase by cannabimimetic drugs.
Howlett, A. C., Qualy, J. M., & Khachatrian, L. (1986) · Molecular Pharmacology · doi:10.1016/s0026-895x(25)10219-8 · Cited by 470 · see citing works
Chen, J., Paredes, W. M., Li, J., Smith, D. M., Lowinson, J. H., & Gardner, E. L. (1990) · Psychopharmacology · doi:10.1007/bf02245916 · Cited by 329 · see citing works
Howlett, A. C., Johnson, M. R., Melvin, L. S., & Milne, G. M. (1988) · Molecular Pharmacology · doi:10.1016/s0026-895x(25)13196-9 · Cited by 253 · see citing works
Cannabinoid Receptors and Modulation of Cyclic AMP Accumulation in the Rat Brain
Bidaut‐Russell, M., Devane, W. A., & Howlett, A. C. (1990) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1990.tb08815.x · Cited by 208 · see citing works
Facilitation of brain stimulation reward byΔ 9-tetrahydrocannabinol
Gardner, E. L., Paredes, W. M., Smith, D. M., Donner, A., Milling, C., Cohen, D., & Morrison, D. (1988) · Psychopharmacology · doi:10.1007/bf02431546 · Cited by 204 · see citing works
Biochemistry and Physiology of Substance Abuse
WATSON, R. R. (1990) · Medical Entomology and Zoology · Cited by 202 · see citing works
17β-estradiol at a physiological dose acutely increases dopamine turnover in rat brain
Paolo, T. D., Rouillard, C., & Bédard, P. J. (1985) · European Journal of Pharmacology · doi:10.1016/0014-2999(85)90604-1 · Cited by 195 · see citing works
The Cannabinoids: Chemical, Pharmacologic, and Therapeutic Aspects
(1984) · Elsevier eBooks · doi:10.1016/b978-0-12-044620-9.x5001-5 · Cited by 189 · see citing works
de Fonseca, F. R., Cebeira, M., Fernández‐Ruíz, J., Navarro, M. A., & Ramos, J. A. (1991) · Neuroscience · doi:10.1016/0306-4522(91)90329-m · Cited by 126 · see citing works
Self-citationStriatal D1 dopamine receptor density fluctuates during the rat estrous cycle
Lévesque, D., Gagnon, S., & Paolo, T. D. (1989) · Neuroscience Letters · doi:10.1016/0304-3940(89)90426-6 · Cited by 89 · see citing works
A physiological dose of progesterone affects rat striatum biogenic amine metabolism
Paolo, T. D., Lévesque, D., & Daigle, M. (1986) · European Journal of Pharmacology · doi:10.1016/0014-2999(86)90077-4 · Cited by 74 · see citing works
Regulation of adenylate cyclase by chronic exposure to cannabimimetic drugs.
Dill, J. A., & Howlett, A. C. (1988) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)24581-5 · Cited by 73 · see citing works
Fernández‐Ruíz, J., Amor, J. C., & Ramos, J. A. (1989) · Brain Research · doi:10.1016/0006-8993(89)91266-3 · Cited by 70 · see citing works
Self-citationAcute effects of δ-9-tetrahydrocannabinol on dopaminergic activity in several rat brain areas
de Fonseca, F. R., Fernández‐Ruíz, J., Murphy, L. L., Cebeira, M., Steger, R. W., Artke, J. A., & Ramos, J. A. (1992) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(92)90526-l · Cited by 69 · see citing works
Self-citationFernández‐Ruíz, J., de Miguel, R., Hernández, M., & Ramos, J. A. (1990) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(90)90262-g · Cited by 41 · see citing works
Self-citationde Fonseca, F. R., Hernández, M., de Miguel, R., Fernández‐Ruíz, J., & Ramos, J. A. (1992) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(92)90359-n · Cited by 37 · see citing works
Self-citationChanges in brain dopaminergic indices induced by perinatal exposure to cannabinoids in rats
de Fonseca, F. R., Cebeira, M., Hernández, M., Ramos, J. A., & Fernández‐Ruíz, J. (1990) · Developmental Brain Research · doi:10.1016/0165-3806(90)90280-c · Cited by 34 · see citing works
Self-citationEvidence for a direct anterior pituitary site of delta-9-tetrahydrocannabinol action
Murphy, L. L., Newton, S. C., Dhali, J., & Chávez, D. (1991) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(91)90370-h · Cited by 31 · see citing works
Murphy, L. L., de Fonseca, F. R., & Steger, R. W. (1991) · Steroids · doi:10.1016/0039-128x(91)90131-e · Cited by 24 · see citing works
Role of estrogens on striatal dopaminergic activity
Ramos, J. A., Pais, J., Cebeira, M., & Fernández‐Ruíz, J. (1987) · Journal of Steroid Biochemistry · doi:10.1016/0022-4731(87)90137-3 · Cited by 20 · see citing works
Self-citationInfluence of Estradiol and Progesterone on Pulsatile LH Secretion in 8-Day Ovariectomized Rats
Leipheimer, R. E., Bona‐Gallo, A., & Gallo, R. V. (2008) · Neuroendocrinology · doi:10.1159/000124544 · Cited by 15 · see citing works
Bonnin, A., Fern�ndez-Ruiz, J. J., Martı́n, M. I., de Fonseca, F. R., de Miguel, R., & Ramos, J. A. (1992) · Molecular and Cellular Neuroscience · doi:10.1016/1044-7431(92)90028-z · Cited by 11 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
The Emerging Role of the Endocannabinoid System in Endocrine Regulation and Energy Balance
Pagotto, U., Marsicano, G., Cota, D., Lutz, B., & Pasquali, R. (2005) · Endocrine Reviews · doi:10.1210/er.2005-0009 · Cited by 856 · 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
Puberty as a highly vulnerable developmental period for the consequences of cannabis exposure
Schneider, M. (2008) · Addiction Biology · doi:10.1111/j.1369-1600.2008.00110.x · Cited by 330 · see citing works
Bisogno, T., Berrendero, F., Ambrosino, G., Cebeira, M., Ramos, J. A., Fernández‐Ruíz, J., & Marzo, V. D. (1999) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1999.0254 · Cited by 313 · see citing works
Self-citationCrane, 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
Craft, R. M., Marusich, J. A., & Wiley, J. L. (2012) · Life Sciences · doi:10.1016/j.lfs.2012.06.009 · Cited by 301 · see citing works
The Influence of Marijuana Use on Neurocognitive Functioning in Adolescents
Tapert, S. F., Schweinsburg, A. D., & Brown, S. A. (2008) · Current Drug Abuse Reviews · doi:10.2174/1874473710801010099 · Cited by 252 · see citing works
The Role of the Endocannabinoid System and Genetic Variation in Adolescent Brain Development
Meyer, H. C., Lee, F. S., & Gee, D. G. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2017.143 · Cited by 222 · see citing works
Bradshaw, H. B., Rimmerman, N., Krey, J. F., & Walker, J. M. (2006) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00933.2005 · Cited by 202 · see citing works
Cannabinoid self‐administration in rats: sex differences and the influence of ovarian function
Fattore, L., Spano, M. S., Altea, S., Angius, F., Fadda, P., & Fratta, W. (2007) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0707465 · Cited by 200 · see citing works
How important are sex differences in cannabinoid action?
Fattore, L., & Fratta, W. (2010) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2010.00776.x · Cited by 196 · see citing works
González, S. R., Bisogno, T., Wenger, T., Manzanares, J., Milone, A., Berrendero, F., Marzo, V. D., Ramos, J. A., & Fernández‐Ruíz, J. (2000) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.2000.2406 · Cited by 196 · see citing works
Self-citationAbstinent adolescent marijuana users show altered fMRI response during spatial working memory
Schweinsburg, A. D., Nagel, B. J., Schweinsburg, B. C., Park, A., Theilmann, R. J., & Tapert, S. F. (2008) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2007.04.018 · Cited by 187 · see citing works
Function of Cannabinoid Receptors in the Neuroendocrine Regulation of Hormone Secretion
Murphy, L. L., Muñoz, R. M., Adrian, B., & Villanúa, M. Á. (1998) · Neurobiology of Disease · doi:10.1006/nbdi.1998.0224 · Cited by 175 · see citing works
Vela, G., Martı́n, S., Garcı́a-Gil, L., Crespo, J. A., Ruiz‐Gayo, M., Fernández-Ruiz, J. J., Garcı́a-Lecumberri, C., Pélaprat, D., Fuentes, J. A., Ramos, J. A., et al. (1998) · Brain Research · doi:10.1016/s0006-8993(98)00766-5 · Cited by 172 · see citing works
Self-citationPreferential limbic expression of the cannabinoid receptor mRNA in the human fetal brain
Wang, X., Dow-Edwards, D. L., Keller, É., & Hurd, Y. L. (2003) · Neuroscience · doi:10.1016/s0306-4522(03)00020-4 · Cited by 154 · 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
Sex-dependent effects of in utero cannabinoid exposure on cortical function
Bara, A., Manduca, A., Bernabeu, A., Borsoï, M., Serviado, M., Lassalle, O., Murphy, M. N., Wager‐Miller, J., Mackie, K., Pélissier‐Alicot, A., et al. (2018) · eLife · doi:10.7554/elife.36234 · Cited by 146 · 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
Van Laere, K., Goffin, K., Casteels, C., Dupont, P., Mortelmans, L., de Hoon, J., & Bormans, G. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2007.10.053 · Cited by 142 · see citing works
Suárez, J., Llorente, R., Romero‐Zerbo, S., Mateos, B., Bermúdez‐Silva, F. J., de Fonseca, F. R., & Viveros, M. (2008) · Hippocampus · doi:10.1002/hipo.20537 · Cited by 142 · see citing works
Gender effects on amygdala morphometry in adolescent marijuana users
McQueeny, T. M., Padula, C. B., Price, J. S., Lisdahl, K. M., Logan, P., & Tapert, S. F. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.05.031 · Cited by 139 · see citing works
Gorzalka, B. B., & Dang, S. S. (2011) · Endocrinology · doi:10.1210/en.2011-1643 · Cited by 139 · 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
Tseng, A. H., Harding, J. W., & Craft, R. M. (2004) · Behavioural Brain Research · doi:10.1016/j.bbr.2004.01.029 · Cited by 132 · see citing works
Krebs-Kraft, D. L., Hill, M. N., Hillard, C. J., & McCarthy, M. M. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1005003107 · Cited by 130 · see citing works
Estrogenic regulation of limbic cannabinoid receptor binding
Riebe, C. J. N., Hill, M. N., Lee, T. T. Y., Hillard, C. J., & Gorzalka, B. B. (2010) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2010.02.008 · Cited by 128 · see citing works
Viveros, M., Llorente, R., Suárez, J., Llorente‐Berzal, A., López‐Gallardo, M., & de Fonseca, F. R. (2011) · Journal of Psychopharmacology · doi:10.1177/0269881111408956 · Cited by 124 · see citing works
Mechanisms 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
Krolick, K. N., Zhu, Q., & Shi, H. (2018) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2018.07.008 · Cited by 121 · see citing works
Sex differences in cannabis withdrawal symptoms among treatment-seeking cannabis users.
Herrmann, E. S., Weerts, E. M., & Vandrey, R. G. (2015) · Experimental and Clinical Psychopharmacology · doi:10.1037/pha0000053 · Cited by 115 · 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
Behavioural consequences of maternal exposure to natural cannabinoids in rats
Navarro, M. A., & Rubio, P. (1995) · Psychopharmacology · doi:10.1007/bf02246436 · Cited by 110 · see citing works
Neurochemical basis of cannabis addiction
Maldonado, R. J., Berrendero, F., Ozaita, A., & Robledo, P. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.02.035 · Cited by 110 · see citing works
Sexually 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
Sex differences in the subjective effects of oral Δ9-THC in cannabis users
Fogel, J. S., Kelly, T. H., Westgate, P. M., & Lile, J. A. (2016) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2016.01.007 · Cited by 107 · see citing works
Craft, R. M., Wakley, A. A., Tsutsui, K. T., & Laggart, J. D. (2011) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.111.188540 · Cited by 105 · see citing works
Romero, J., García‐García, L., Fernández‐Ruíz, J., Cebeira, M., & Ramos, J. A. (1995) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(95)00023-p · Cited by 101 · see citing works
Self-citationMarco, E. M., Echeverry‐Alzate, V., López‐Moreno, J. A., Giné, E., Peñasco, S., & Viveros, M. (2014) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000068 · Cited by 95 · see citing works
Endocannabinoid signaling and the hypothalamic-Pituitary-Adrenal axis
Hillard, C. J., Beatka, M., & Sarvaideo, J. (2016) · Comprehensive physiology · doi:10.1002/cphy.c160005 · Cited by 93 · see citing works
Mize, A. L., & Alper, R. H. (2000) · Brain Research · doi:10.1016/s0006-8993(00)01998-3 · Cited by 92 · 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
Bushlin, I., Gupta, A., Stockton, S. D., Miller, L. K., & Devi, L. A. (2012) · PLoS ONE · doi:10.1371/journal.pone.0049789 · Cited by 90 · see citing works
Sex differences in antinociceptive tolerance to delta-9-tetrahydrocannabinol in the rat
Wakley, A. A., Wiley, J. L., & Craft, R. M. (2014) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2014.07.029 · Cited by 90 · see citing works
Effects of Δ9-THC and cannabidiol vapor inhalation in male and female rats
Paydar, M. J., Nguyen, J. D., Kerr, T. M., Grant, Y., Vandewater, S. A., Cole, M., & Taffe, M. A. (2018) · Psychopharmacology · doi:10.1007/s00213-018-4946-0 · Cited by 82 · see citing works
Keeney, 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 in brain plasticity: Cortical maturation, HPA axis function and behavior
Dow-Edwards, D. L., & Silva, L. (2016) · Brain Research · doi:10.1016/j.brainres.2016.08.037 · Cited by 84 · see citing works
Brain CB2 Receptors: Implications for Neuropsychiatric Disorders
Roche, M., & Finn, D. P. (2010) · Pharmaceuticals · doi:10.3390/ph3082517 · Cited by 87 · see citing works
Wenger, T., Jamali, K. A., Juanéda, C., Léonardelli, J., & Tramu, G. (1997) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1997.7222 · Cited by 85 · see citing works
Wiley, J. L., O’Connell, M. M., Tokarz, M. E., & Wright, M. J. (2006) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.106.108126 · Cited by 83 · see citing works
FemándeZ-Ruiz, J. J., Muñoz, R. M., Romero, J., Villanúa, M. A., Makriyannis, A., & Ramos, J. A. (1997) · Biochemical Pharmacology · doi:10.1016/s0006-2952(97)00168-8 · Cited by 82 · see citing works
Self-citationManduca, A., Servadio, M., Melancia, F., Schiavi, S., Manzoni, O. J., & Trezza, V. (2019) · British Journal of Pharmacology · doi:10.1111/bph.14879 · Cited by 77 · see citing works
Martı́n-Calderón, J. L., Muñoz, R. M., Villanúa, M. Á., del Arco, I., Moreno, J. L., de Fonseca, F. R., & Navarro, M. A. (1998) · European Journal of Pharmacology · doi:10.1016/s0014-2999(97)01560-4 · Cited by 74 · see citing works
Withdrawal from THC during adolescence: Sex differences in locomotor activity and anxiety
Harte‐Hargrove, L. C., & Dow-Edwards, D. L. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.02.048 · Cited by 73 · see citing works
Sex‐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
Craft, R. M., & Leitl, M. D. (2008) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2007.09.004 · Cited by 70 · see citing works
Sex, Drugs, and Cognition: Effects of Marijuana
Anderson, B. M., Rizzo, M., Block, R. I., Pearlson, G. D., & OʼLeary, D. S. (2010) · Journal of Psychoactive Drugs · doi:10.1080/02791072.2010.10400704 · Cited by 69 · see citing works
Cannabinoid–hormone interactions in the regulation of motivational processes
López, H. H. (2009) · Hormones and Behavior · doi:10.1016/j.yhbeh.2009.10.005 · Cited by 67 · see citing works
Lee, T. T. Y., & Hill, M. N. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.11.017 · Cited by 67 · see citing works
Sex, THC, and hormones: Effects on density and sensitivity of CB1 cannabinoid receptors in rats
Farquhar, C. E., Breivogel, C. S., Gamage, T. F., Gay, E. A., Thomas, B. F., Craft, R. M., & Wiley, J. L. (2018) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2018.09.018 · Cited by 69 · see citing works
Ney, 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
Endocannabinoid involvement in endometriosis.
Dmitrieva, N., Nagabukuro, H., Resuehr, D., Zhang, G., McAllister, S. L., McGinty, K. A., Mackie, K., & Berkley, K. J. (2010) · Pain · doi:10.1016/j.pain.2010.08.037 · Cited by 64 · see citing works
“In contrast, two other rodent studies suggest that hormonal therapies in endometriosis might affect how cannabinoids influence central pain mechanisms; both studies observed ovarian cyclical changes in cannabinoid receptor density or endocannabinoid content in brain areas potentially associated with nociception [8,44].”
ResultDrzewiecki, C. M., & Juraska, J. M. (2020) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2020.173044 · Cited by 67 · see citing works
CB 1 receptor mediation of cannabinoid behavioral effects in male and female rats
Tseng, A. H., & Craft, R. M. (2004) · Psychopharmacology · doi:10.1007/s00213-003-1620-x · 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
Kruse, L. C., Cao, J. K., Viray, K., Stella, N., & Clark, J. J. (2019) · Neuropsychopharmacology · doi:10.1038/s41386-019-0387-7 · Cited by 61 · see citing works
Sex-dependent effects of Δ9-tetrahydrocannabinol on locomotor activity in mice
Wiley, J. L. (2003) · Neuroscience Letters · doi:10.1016/j.neulet.2003.08.050 · Cited by 59 · see citing works
Melis, M., Felice, M. D., Lecca, S., Fattore, L., & Pistis, M. (2013) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2013.00093 · Cited by 58 · see citing works
Sex-Dependent Vulnerability to Cannabis Abuse in Adolescence
Rubino, T., & Parolaro, D. (2015) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2015.00056 · Cited by 58 · see citing works
Framework for sex differences in adolescent neurobiology: A focus on cannabinoids
Viveros, M., Marco, E. M., López‐Gallardo, M., García‐Segura, L. M., & Wagner, E. J. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.09.005 · Cited by 58 · see citing works
Sex differences in hippocampal response to endocannabinoids after exposure to severe stress
Zer‐Aviv, T. M., & Akirav, I. (2016) · Hippocampus · doi:10.1002/hipo.22577 · Cited by 58 · see citing works
Sex differences in behavioral effects of cannabinoids
Craft, R. M. (2005) · Life Sciences · doi:10.1016/j.lfs.2005.04.019 · Cited by 58 · see citing works
Atkinson, H. C., Leggett, J. D., Wood, S. A., Castrique, E. S., Kershaw, Y. M., & Lightman, S. L. (2010) · Endocrinology · doi:10.1210/en.2010-0101 · Cited by 57 · see citing works
Effects of Cannabinoids on Hypothalamic and Reproductive Function
Maccarrone, M., & Wenger, T. (2005) · Springer eBooks · doi:10.1007/3-540-26573-2_18 · Cited by 57 · see citing works
The effect of cannabis use and gender on the visual steady state evoked potential
Skosnik, P. D., Krishnan, G. P., Vohs, J. L., & O’Donnell, B. F. (2005) · Clinical Neurophysiology · doi:10.1016/j.clinph.2005.09.024 · Cited by 57 · see citing works
Keeney, B. K., Meek, T. H., Middleton, K. M., Holness, L. F., & Garland, T. (2012) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2012.02.017 · Cited by 56 · see citing works
Roberts, C. J., Stuhr, K. L., Hutz, M. J., Raff, H., & Hillard, C. J. (2013) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2013.11.026 · Cited by 55 · see citing works
Winsauer, P. J., Daniel, J. M., Filipeanu, C. M., Leonard, S. T., Hulst, J. L., Rodgers, S. P., Lassen-Greene, C. L., & Sutton, J. L. (2010) · Addiction Biology · doi:10.1111/j.1369-1600.2010.00227.x · Cited by 55 · see citing works
Peterson, B. M., Martinez, L. A., Meisel, R. L., & Mermelstein, P. G. (2016) · Neuropharmacology · doi:10.1016/j.neuropharm.2016.06.002 · Cited by 54 · see citing works
The endocannabinoid system expression in the female reproductive tract is modulated by estrogen
Maia, J. C., Almada, M., Silva, A. C., Correia‐da‐Silva, G., Teixeira, N. A. A., Sá, S. I., & Fonseca, B. M. (2017) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2017.07.023 · Cited by 54 · see citing works
Harte, L. C., & Dow-Edwards, D. (2010) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2010.05.001 · Cited by 51 · see citing works
Navarro, M. A., Rubio, P., & de Fonseca, F. R. (1994) · Psychopharmacology · doi:10.1007/bf02247471 · Cited by 51 · see citing works
Best, L. M., Williams, B., Foll, B. L., Mansouri, E., Bazinet, R. P., Lin, L., Luca, V. D., Lagzdins, D., Rusjan, P., Tyndale, R. F., et al. (2020) · Neuropsychopharmacology · doi:10.1038/s41386-020-0606-2 · Cited by 48 · see citing works
Changes in the Mucus Barrier during Cisplatin-Induced Intestinal Mucositis in Rats
Yamamoto, H., Ishihara, K., Takeda, Y., Koizumi, W., & Ichikawa, T. (2013) · BioMed Research International · doi:10.1155/2013/276186 · Cited by 48 · see citing works
The impact of gonadal hormones on cannabinoid dependence.
Marusich, J. A., Craft, R. M., Lefever, T. W., & Wiley, J. L. (2015) · Experimental and Clinical Psychopharmacology · doi:10.1037/pha0000027 · Cited by 46 · see citing works
Sex, Species and Age: Effects of Rodent Demographics on the Pharmacology of Δ9-Tetrahydrocanabinol
Wiley, J., Barrus, D., Farquhar, C., Lefever, T., & Gamage, T. (2020) · Progress in Neuro-psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2020.110064 · Cited by 38 · see citing works
Sex, stress, and prefrontal cortex: influence of biological sex on stress-promoted cocaine seeking
Doncheck, E. M., Liddiard, G. T., Konrath, C. D., Liu, X., Yu, L., Urbanik, L. A., Herbst, M. R., DeBaker, M. C., Raddatz, N. J., Newenhizen, E. C. V., et al. (2020) · Neuropsychopharmacology · doi:10.1038/s41386-020-0674-3 · Cited by 45 · see citing works
Endocannabinoids and the Endocrine System in Health and Disease
Hillard, C. J. (2015) · Handbook of experimental pharmacology · doi:10.1007/978-3-319-20825-1_11 · Cited by 45 · see citing works
Wakley, A. A., & Craft, R. M. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.07.037 · Cited by 45 · see citing works
Influence of the anabolic-androgenic steroid nandrolone on cannabinoid dependence
Célèrier, E., Ahdepil, T., Wikander, H., Berrendero, F., Nyberg, F., & Maldonado, R. J. (2006) · Neuropharmacology · doi:10.1016/j.neuropharm.2005.11.017 · Cited by 43 · see citing works
Casteels, C., Lauwers, E., Baitar, A., Bormans, G. M., Baekelandt, V., & Laere, K. V. (2009) · Brain Research · doi:10.1016/j.brainres.2009.12.026 · Cited by 42 · see citing works
López-Rodríguez, A. B., Vicente, B. M., Romero‐Zerbo, S., Rodríguez‐Rodríguez, N., Bellini, M. J., de Fonseca, F. R., Bermúdez‐Silva, F. J., Azcoitia, Í., García‐Segura, L. M., & Viveros, M. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhq277 · Cited by 42 · 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
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
Doncheck, E. M., Urbanik, L. A., DeBaker, M. C., Barron, L. M., Liddiard, G. T., Tuscher, J. J., Frick, K. M., Hillard, C. J., & Mantsch, J. R. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2017.170 · Cited by 41 · see citing works
The effect of anandamide on prolactin secretion is modulated by estrogen
Scorticati, C., Mohn, C. E., Laurentiis, A. D., Vissio, P. G., Fernández‐Solari, J., Seilicovich, A., McCann, S. M., & Rettori, V. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0437924100 · Cited by 41 · see citing works
Sex-dependence of anxiety-like behavior in cannabinoid receptor 1 (Cnr1) knockout mice
Bowers, M. E., & Ressler, K. J. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.12.005 · Cited by 40 · see citing works
Effects of ∆9-tetrahydrocannabinol on aversive memories and anxiety: a review from human studies
Raymundi, A. M., da Silva, T. R., Sohn, J. M. B., Bertoglio, L. J., & Stern, C. A. J. (2020) · BMC Psychiatry · doi:10.1186/s12888-020-02813-8 · Cited by 40 · see citing works
Goffin, K. E., Bormans, G. M., Casteels, C., Bosier, B., Lambert, D. M., Grachev, I. D., Paesschen, W. V., & Laere, K. V. (2008) · Neuropharmacology · doi:10.1016/j.neuropharm.2008.02.018 · Cited by 39 · see citing works
- Authors
- de Fonseca, F. R., Cebeira, M., Ramos, J. A., Martín, M., & Fernández-Ruiz, J. J.
- Affiliations
- Universidad Complutense de Madrid (ES)
- ORCID
- Martín, M.
- Venue
- Life Sciences
- Publisher
- Elsevier BV
- Published
- 1994-01
- Volume
- 54
- Issue
- 3
- Pages
- 159-170
- ISSN
- 0024-3205 (ISSN-L)
- OpenAlex
- W2056795643
- Cited by
- 243
- References
- 29
- Citations by year
- 2026: 6 · 2025: 9 · 2024: 11 · 2023: 18 · 2022: 12 · 2021: 18 · 2020: 14 · 2019: 4 · 2018: 10 · 2017: 12 · 2016: 8 · 2015: 11 · 2014: 9 · 2013: 9 · 2012: 9
- FWCI
- 2.09
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Life Sciences (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Pharmacology › Cannabis and Cannabinoid Research
- Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Estrogen and related hormone effects
- Keywords
- cannabinoid receptors, sex differences, estrous cycle, gonadectomy, estradiol, progesterone, testosterone, ovariectomy, orchiectomy, receptor density, receptor binding affinity, medial basal hypothalamus, striatum, limbic forebrain, midbrain, dopaminergic activity, gonadal status
- MeSH terms
- Animals, Brain, Cannabinoids, Cyclohexanols, Dopamine, Estradiol, Estrus, Female, Kinetics, Male, Neurons, Orchiectomy, Ovariectomy, Ovary, Progesterone, Receptors, Drug, Sex Characteristics, Testis, Testosterone, Dronabinol, Tritium, Rats, Wistar, Receptors, Cannabinoid, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review