Activation of Both CB1 and CB2 Endocannabinoid Receptors Is Critical for Masculinization of the Developing Medial Amygdala and Juvenile Social Play Behavior
Open accessAbstract
Juvenile social play behavior is a shared trait across a wide variety of mammalian species. When play is characterized by the frequency or duration of physical contact, males usually display more play relative to females. The endocannabinoid system contributes to the development of the sex difference in social play behavior in rats. Treating newborn pups with a nonspecific endocannabinoid agonist, WIN55,212-2, masculinizes subsequent juvenile rough-and-tumble play behavior by females. Here we use specific drugs to target signaling through either the CB1 or CB2 endocannabinoid receptor (CB1R or CB2R) to determine which modulates the development of sex differences in play. Our data reveal that signaling through both CB1R and CB2R must be altered neonatally to modify development of neural circuitry regulating sex differences in play. Neonatal co-agonism of CB1R and CB2R masculinized play by females, whereas co-antagonism of these receptors feminized rates of male play. Because of a known role for the medial amygdala in the sexual differentiation of play, we reconstructed Golgi-impregnated neurons in the juvenile medial amygdala and used factor analysis to identify morphological parameters that were sexually differentiated and responsive to dual agonism of CB1R and CB2R during the early postnatal period. Our results suggest that sex differences in the medial amygdala are modulated by the endocannabinoid system during early development. Sex differences in play behavior are loosely correlated with differences in neuronal morphology.
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If females are treated with CB1 and CB2 receptor agonists to mimic higher endocannabinoid levels, their newborn cell number and eventual play behavior is masculinized, even in the absence of testosterone.
“If females are treated with CB1 and CB2 receptor agonists to “mimic” the higher endocannabinoid levels, their newborn cell number and eventual play behavior is masculinized, even in the absence of testosterone (Argue et al., 2017; VanRyzin et al., 2019).”
From Developmental origins of sex differences in the neural circuitry of play (2020) · cites this paper as Argue et al., 2017
The Results (Fig. 2; page not provided) show that neonatal coadministration of CB1 and CB2 agonists increased females’ juvenile play to male levels. The paper does not report that this combined treatment masculinized newborn cell number; its Discussion instead describes a prior finding involving a nonspecific agonist. It also does not test whether the effect occurs independently of testosterone. (LLM, conf=0.88)
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Cites
Molecular characterization of a peripheral receptor for cannabinoids
Munro, S., Thomas, K. L., & Abu-Shaar, M. (1993) · Nature · doi:10.1038/365061a0 · Cited by 5,092 · 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
Galiègue, S., Mary, S., Marchand, J., Dussossoy, D., Carrière, D., Carayon, P., Bouaboula, M., Shire, D. J., Fur, G. L., & Casellas, P. (1995) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1995.tb20780.x · Cited by 1,751 · see citing works
An Introduction to the Endogenous Cannabinoid System
Lu, H.-C., & Mackie, K. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.07.028 · Cited by 1,234 · see citing works
Cannabinoid CB2 receptors: immunohistochemical localization in rat brain
Gong, J.-P., Onaivi, E. S., Ishiguro, H., Liu, Q.-R., Tagliaferro, P. A., Brusco, A., & Uhl, G. R. (2006) · Brain Research · doi:10.1016/j.brainres.2005.11.035 · Cited by 820 · see citing works
Mammalian Play: Training for the Unexpected
Spinka, M., Newberry, R. C., & Bekoff, M. (2001) · The Quarterly Review of Biology · doi:10.1086/393866 · Cited by 817 · see citing works
Hardwiring the Brain: Endocannabinoids Shape Neuronal Connectivity
Berghuis, P., Rajnicek, A. M., Morozov, Y. M., Ross, R. A., Mulder, J., Urbán, G. M., Monory, K., Marsicano, G., Matteoli, M., Canty, A. J., et al. (2007) · Science · doi:10.1126/science.1137406 · Cited by 551 · see citing works
Discovery of the Presence and Functional Expression of Cannabinoid CB2 Receptors in Brain
Onaivi, E. S., Ishiguro, H., GONG, J., Sejal, P., Perchuk, A., Meozzi, P. A., MYERS, L., Mora, Z., Tagliaferro, P. A., Gardner, E., et al. (2006) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1369.052 · Cited by 546 · see citing works
Cannabinoid and cannabinoid‐like receptors in microglia, astrocytes, and astrocytomas
Stella, N. (2010) · Glia · doi:10.1002/glia.20983 · Cited by 529 · see citing works
Jiang, W. (2005) · Journal of Clinical Investigation · doi:10.1172/jci25509 · Cited by 527 · see citing works
Modulation of the cannabinoid CB 2 receptor in microglial cells in response to inflammatory stimuli
Maresz, K., Carrier, E. J., Ponomarev, E. D., Hillard, C. J., & Dittel, B. N. (2005) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2005.03380.x · Cited by 483 · see citing works
Moller, P., & Husby, R. (2000) · Schizophrenia Bulletin · doi:10.1093/oxfordjournals.schbul.a033442 · Cited by 464 · see citing works
The neurobiology and evolution of cannabinoid signalling
Elphick, M. R., & Egertová, M. (2001) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2000.0787 · Cited by 416 · see citing works
Development of the blood-brain barrier
Engelhardt, B. (2003) · Cell and Tissue Research · doi:10.1007/s00441-003-0751-z · Cited by 377 · see citing works
Endocannabinoids and the control of energy balance
Matias, I., & Marzo, V. D. (2006) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2006.11.006 · Cited by 367 · see citing works
Induction of PGE2 by estradiol mediates developmental masculinization of sex behavior
Amateau, S. K., & McCarthy, M. M. (2004) · Nature Neuroscience · doi:10.1038/nn1254 · Cited by 340 · see citing works
Self-citationNúñez, E., Benito, C., Pazos, M. R., Barbáchano, A., Fajardo, O., González, S. R., Tolón, R. M., & Romero, J. (2004) · Synapse · doi:10.1002/syn.20050 · Cited by 334 · see citing works
Zhang, H.-Y., Gao, M., Liu, Q.-R., Bi, G.-H., Li, X., Yang, H.-J., Gardner, E. L., Wu, J., & Xi, Z.-X. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1413210111 · Cited by 334 · see citing works
Endocannabinoid signaling controls pyramidal cell specification and long-range axon patterning
Mulder, J., Aguado, T., Keimpema, E., Barabás, K., Rosado, C. J. B., Nguyen, L., Monory, K., Marsicano, G., Marzo, V. D., Hurd, Y. L., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0803545105 · Cited by 328 · see citing works
The endocannabinoid system drives neural progenitor proliferation
Aguado, T., Monory, K., Palazuelos, J., Stella, N., Cravatt, B. F., Lutz, B., Marsicano, G., Kokaia, Z., Guzmán, M., & Galve‐Roperh, I. (2005) · The FASEB Journal · doi:10.1096/fj.05-3995fje · Cited by 327 · see citing works
Ständer, S., Schmelz, M., Metze, D., Luger, T. A., & Rukwied, R. (2005) · Journal of Dermatological Science · doi:10.1016/j.jdermsci.2005.01.007 · Cited by 300 · see citing works
Cannabinoid CB 2 receptors in human brain inflammation
Benito, C., Tolón, R. M., Pazos, M. R., Núñez, E., Castillo, A. I., & Romero, J. (2007) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0707505 · Cited by 293 · see citing works
Refining the Motor Training Hypothesis for the Evolution of Play
Byers, J. A., & Walker, C. (1995) · The American Naturalist · doi:10.1086/285785 · Cited by 286 · see citing works
Repeated Social Defeat, Neuroinflammation, and Behavior: Monocytes Carry the Signal
Weber, M. D., Godbout, J. P., & Sheridan, J. F. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2016.102 · Cited by 283 · see citing works
Cannabinoid receptor signaling in progenitor/stem cell proliferation and differentiation
Galve‐Roperh, I., Chiurchiù, V., Díaz-Alonso, J., Bari, M., Guzmán, M., & Maccarrone, M. (2013) · Progress in Lipid Research · doi:10.1016/j.plipres.2013.05.004 · Cited by 280 · see citing works
Cannabinoid Type 2 Receptors Mediate a Cell Type-Specific Plasticity in the Hippocampus
Stempel, A. V., Stumpf, A., Zhang, H.-Y., Özdoğan, T., Pannasch, U., Theis, A.-K., Otte, D., Wojtalla, A., Rácz, I., Ponomarenko, A., et al. (2016) · Neuron · doi:10.1016/j.neuron.2016.03.034 · Cited by 274 · see citing works
The Endocannabinoid System Promotes Astroglial Differentiation by Acting on Neural Progenitor Cells
Aguado, T., Palazuelos, J., Monory, K., Stella, N., Cravatt, B. F., Lutz, B., Marsicano, G., Kokaia, Z., Guzmán, M., & Galve‐Roperh, I. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.3101-05.2006 · Cited by 269 · see citing works
Expression of the CB1 and CB2 receptor messenger RNAs during embryonic development in the rat
Buckley, N. E., Hansson, S. R., Harta, G., & Mezey, É. (1997) · Neuroscience · doi:10.1016/s0306-4522(97)00348-5 · Cited by 265 · see citing works
Brain neuronal CB2 cannabinoid receptors in drug abuse and depression: from mice to human subjects
Onaivi, E. S., Ishiguro, H., Gong, J.-P., Patel, S., Meozzi, P. A., Myers, L., Perchuk, A., Mora, Z., Tagliaferro, P. A., Gardner, E., et al. (2008) · PLoS ONE · doi:10.1371/journal.pone.0001640 · Cited by 257 · see citing works
Tortoriello, G., Morris, C. V., Alpár, A., Fuzik, J., Shirran, S. L., Calvigioni, D., Keimpema, E., Botting, C. H., Reinecke, K., Herdegen, T., et al. (2014) · The EMBO Journal · doi:10.1002/embj.201386035 · Cited by 255 · see citing works
Rueda, D., Navarro, B., Martı́nez-Serrano, A., Guzmán, M., & Galve‐Roperh, I. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m206590200 · Cited by 254 · see citing works
Jordan, R. (2003) · Autism · doi:10.1177/1362361303007004002 · Cited by 248 · see citing works
PELLIS, S. M., FIELD, E. F., SMITH, L. K., & PELLIS, V. C. (1997) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(95)00060-7 · Cited by 234 · see citing works
The FGF receptor uses the endocannabinoid signaling system to couple to an axonal growth response
Williams, E., Walsh, F. S., & Doherty, P. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200210164 · Cited by 230 · see citing works
Current Perspectives on the Biological Study of Play: Signs of Progress
Graham, K. L., & Burghardt, G. M. (2010) · The Quarterly Review of Biology · doi:10.1086/656903 · Cited by 229 · see citing works
Mong, J. A., Glaser, E. M., & McCarthy, M. M. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-04-01464.1999 · Cited by 226 · see citing works
Self-citationNon‐psychoactive CB 2 cannabinoid agonists stimulate neural progenitor proliferation
Palazuelos, J., Aguado, T., Egia, A., Mechoulam, R., Guzmán, M., & Galve‐Roperh, I. (2006) · The FASEB Journal · doi:10.1096/fj.06-6164fje · Cited by 222 · see citing works
Play fighting of rats in comparative perspective: a schema for neurobehavioral analyses
Pellis, S. M., & Pellis, V. C. (1998) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(97)00071-7 · Cited by 210 · see citing works
Racz, I., Nadal, X., Alferink, J., Baños, J. E., Rehnelt, J., Martín, M., Pintado, B., Gutierrez-Adan, A., Sanguino, E., Manzanares, J., et al. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.3400-08.2008 · Cited by 195 · see citing works
The play partners of immature baboons
Cheney, D. L. (1978) · Animal Behaviour · doi:10.1016/0003-3472(78)90093-3 · Cited by 189 · see citing works
Goncalves, M. B. C. V., Suetterlin, P., Yip, P. K., Molina‐Holgado, F., Walker, D. J., Oudin, M. J., Zentar, M. P., Pollard, S. M., Yáñez‐Muñoz, R. J., Williams, G. H., et al. (2008) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2008.05.001 · Cited by 177 · see citing works
The influence of natural variations in maternal care on play fighting in the rat
Parent, C. I., & Meaney, M. J. (2008) · Developmental Psychobiology · doi:10.1002/dev.20342 · Cited by 175 · see citing works
CB2 Cannabinoid Receptors Promote Neural Progenitor Cell Proliferation via mTORC1 Signaling
Palazuelos, J., Ortega, Z., Díaz-Alonso, J., Guzmán, M., & Galve‐Roperh, I. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.291294 · Cited by 173 · see citing works
Berrendero, F., Garcı́a-Gil, L., Hernández, M., Romero, J., Cebeira, M., de Miguel, R., Ramos, J. A., & Fernández‐Ruíz, J. (1998) · Development · doi:10.1242/dev.125.16.3179 · Cited by 171 · see citing works
Sex differences in the play behavior of prepubescent rats
Olioff, M., & Stewart, J. (1978) · Physiology & Behavior · doi:10.1016/0031-9384(78)90060-4 · Cited by 145 · see citing works
HENRY, J. D., & Herrero, S. (1974) · American Zoologist · doi:10.1093/icb/14.1.371 · Cited by 142 · see citing works
Brain Sex Differences and the Organisation of Juvenile Social Play Behaviour
Auger, A. P., & Olesen, K. M. (2009) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2009.01871.x · Cited by 142 · see citing works
Wu, C., Zhu, J., Wager‐Miller, J., Wang, S., O’Leary, D. D. M., Monory, K., Lutz, B., Mackie, K., & Lu, H. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07337.x · Cited by 138 · see citing works
Interferon-γ Is a Critical Modulator of CB2Cannabinoid Receptor Signaling during Neuropathic Pain
Rácz, I., Nadal, X., Alferink, J., Baños, J.-E., Rehnelt, J., Martín, M., Pintado, B., Gutiérrez‐Adán, A., Sanguino, E., Bellora, N., et al. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.3402-08.2008 · Cited by 134 · 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
Self-citationPsychomotor stimulants, social deprivation and play in juvenile rats
Beatty, W. W., Dodge, A. M., Dodge, L. J., White, K., & Panksepp, A. (1982) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(82)90445-2 · Cited by 126 · see citing works
Pellis, S. M. (2002) · Archives of Sexual Behavior · doi:10.1023/a:1014070916047 · Cited by 124 · see citing works
Staiano, R. I., Loffredo, S., Borriello, F., Iannotti, F. A., Piscitelli, F., Orlando, P., Secondo, A., Granata, F., Lepore, M. T., Fiorelli, A., et al. (2015) · Journal of Leukocyte Biology · doi:10.1189/jlb.3hi1214-584r · Cited by 123 · see citing works
Meaney, M. J., & McEwen, B. S. (1986) · Brain Research · doi:10.1016/0006-8993(86)91492-7 · Cited by 122 · see citing works
A brain motivated to play: insights into the neurobiology of playfulness
Siviy, S. M. (2016) · Behaviour · doi:10.1163/1568539x-00003349 · Cited by 113 · see citing works
Morris, J. A., Jordan, C. L., & Breedlove, S. M. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21536 · Cited by 109 · see citing works
Morphological sex differences and laterality in the prepubertal medial amygdala
Cooke, B. M., Stokas, M. R., & Woolley, C. S. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21281 · Cited by 103 · see citing works
Iannotti, F. A., Silvestri, C., Mazzarella, E., Martella, A., Calvigioni, D., Piscitelli, F., Ambrosino, P., Petrosino, S., Czifra, G., Bı́ró, T., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1406728111 · Cited by 96 · see citing works
Mechanisms of Biased β-Arrestin-Mediated Signaling Downstream from the Cannabinoid 1 Receptor
Delgado‐Peraza, F., Ahn, K. H., Nogueras‐Ortiz, C. J., Mungrue, I. N., Mackie, K., Kendall, D. A., & Yudowski, G. A. (2016) · Molecular Pharmacology · doi:10.1124/mol.115.103176 · Cited by 95 · see citing works
Gómez, O., Arévalo‐Martín, Á., García‐Ovejero, D., Ortega‐Gutiérrez, S., Cisneros, J. A., Almazán, G., Sanchez-Rodriguez, M. A., Molina‐Holgado, F., & Molina‐Holgado, E. (2010) · Glia · doi:10.1002/glia.21061 · Cited by 90 · see citing works
Functional Selectivity of CB2 Cannabinoid Receptor Ligands at a Canonical and Noncanonical Pathway
Dhopeshwarkar, A., & Mackie, K. (2016) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.116.232561 · Cited by 88 · see citing works
Fine‐tuning of social play in juvenile lowland gorillas (gorilla gorilla gorilla)
Palagi, E., Antonacci, D., & Cordoni, G. (2007) · Developmental Psychobiology · doi:10.1002/dev.20219 · Cited by 86 · see citing works
Strous, R. D., Alvir, J. M. J., Robinson, D. G., Gal, G., Sheitman, B., Chakos, M., & Lieberman, J. A. (2004) · Schizophrenia Bulletin · doi:10.1093/oxfordjournals.schbul.a007077 · Cited by 86 · see citing works
Social play in captive wolves (Canis lupus): not only an immature affair
Cordoni, G. (2009) · Behaviour · doi:10.1163/156853909x427722 · Cited by 84 · see citing works
Himmler, B. T., Stryjek, R., Modlinska, K., Derksen, S. M., Pisula, W., & Pellis, S. M. (2013) · Journal of Comparative Psychology · doi:10.1037/a0032187 · Cited by 82 · see citing works
Effects of early social deprivation on reproductive behavior of male rats
Gruendel, A. D., & Arnold, W. J. (1969) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0026667 · Cited by 76 · see citing works
Dyadic Play in Hamadryas Baboons
LeResche, L. (1976) · Behaviour · doi:10.1163/156853976x00514 · Cited by 73 · see citing works
Thor, D. H., & Holloway, W. R. (1986) · Behavioral Neuroscience · doi:10.1037//0735-7044.100.2.275 · Cited by 73 · see citing works
Thor, D. H., & Holloway, W. R. (1986) · Behavioral Neuroscience · doi:10.1037/0735-7044.100.2.275 · Cited by 73 · see citing works
Characterization of juvenile play in rats: importance of sex of self and sex of partner
Argue, K. J., & McCarthy, M. M. (2015) · Biology of Sex Differences · doi:10.1186/s13293-015-0034-x · Cited by 71 · see citing works
Self-citationRom, S., Zuluaga‐Ramirez, V., Dykstra, H., Reichenbach, N. L., Pacher, P., & Persidsky, Y. (2013) · American Journal Of Pathology · doi:10.1016/j.ajpath.2013.07.033 · Cited by 71 · see citing works
Himmler, S. M., Modlinska, K., Stryjek, R., Himmler, B. T., Pisula, W., & Pellis, S. M. (2014) · Journal of Comparative Psychology · doi:10.1037/a0036104 · Cited by 67 · see citing works
Functions of the CB1 and CB2 Receptors in Neuroprotection at the Level of the Blood–Brain Barrier
Vendel, E., & de Lange, E. C. M. (2014) · NeuroMolecular Medicine · doi:10.1007/s12017-014-8314-x · Cited by 64 · see citing works
Environmental influences on play behaviour in immature gelada baboons
Barrett, L., Dunbar, R., & Dunbar, P. (1992) · Animal Behaviour · doi:10.1016/s0003-3472(05)80760-2 · Cited by 60 · see citing works
Empathy in the Play of Children with Attention Deficit Hyperactivity Disorder
Cordier, R., Bundy, A. C., Hocking, C. S., & Einfeld, S. (2010) · OTJR Occupational Therapy Journal of Research · doi:10.3928/15394492-20090518-02 · Cited by 57 · see citing works
Comparison of the play of children with attention deficit hyperactivity disorder by subtypes
Cordier, R., Bundy, A. C., Hocking, C. S., & Einfeld, S. (2010) · Australian Occupational Therapy Journal · doi:10.1111/j.1440-1630.2009.00821.x · Cited by 51 · see citing works
Rubio‐Araiz, A., Arévalo‐Martín, Á., Gómez, O., Navarro‐Galve, B., García‐Ovejero, D., Suetterlin, P., Sánchez-Heras, E., Molina‐Holgado, E., & Molina‐Holgado, F. (2008) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2008.03.010 · Cited by 50 · see citing works
Rivera, P., Bîndilă, L., Pastor, A., Pérez‐Martín, M., Pavón, F. J., Serrano, A., de la Torre, R., Lutz, B., de Fonseca, F. R., & Suárez, J. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00098 · Cited by 49 · see citing works
Endocannabinoid synthesis and degradation, and their regulation in the framework of energy balance.
Matias, I., & Marzo, V. D. (2006) · PubMed · Cited by 49 · see citing works
Cannabinoids and intestinal motility: welcome to CB2 receptors
Izzo, A. A. (2004) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0705890 · Cited by 43 · see citing works
Sun, J., Fang, Y., Chen, T., Guo, J., Yan, J., Song, S., Zhang, L., & Liao, H. (2012) · Brain Research · doi:10.1016/j.brainres.2012.11.006 · Cited by 37 · see citing works
Díaz-Alonso, J., Aguado, T., de Salas-Quiroga, A., Ortega, Z., Guzmán, M., & Galve‐Roperh, I. (2014) · Cerebral Cortex · doi:10.1093/cercor/bhu039 · Cited by 33 · see citing works
Enhancing Peer Interactions Within the Context of Play
Arthur, M., Bochner, S., & Butterfield, N. (1999) · International Journal of Disability Development and Education · doi:10.1080/103491299100551 · Cited by 28 · see citing works
Regulation of neural progenitor cell fate by anandamide
Soltys, J. N., Yushak, M. L., & Mao‐Draayer, Y. (2010) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2010.07.129 · Cited by 28 · see citing works
Playfighting in Captive Red-Necked Wallabies, Macropus Rufogriseus Banksianus
Watson, D. M., & Croft, D. B. (1993) · Behaviour · doi:10.1163/156853993x00128 · Cited by 24 · see citing works
Play soliciting behavior in prepubertal and postpubertal male rats
Thor, D. H., & Holloway, W. R. (1985) · Animal Learning & Behavior · doi:10.3758/bf03200028 · Cited by 20 · see citing works
Pinning in the Play Fighting of Rats: A Comparative Perspective With Methodological Recommendations
Himmler, S. M., Himmler, B. T., Stryjek, R., Modlińska, K., Pisula, W., & Pellis, S. M. (2016) · International Journal of Comparative Psychology · doi:10.46867/ijcp.2016.29.00.06 · Cited by 19 · see citing works
Argue, K. J., & McCarthy, M. M. (2015) · PubMed · doi:10.4172/0975-9042.000117 · Cited by 16 · see citing works
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VanRyzin, J. W., Marquardt, A. E., Argue, K. J., Vecchiarelli, H. A., Ashton, S. E., Arambula, S. E., Hill, M. N., & McCarthy, M. M. (2019) · Neuron · doi:10.1016/j.neuron.2019.02.006 · Cited by 272 · see citing works
Self-citationLiu, Q.-R., Canseco-Alba, A., Zhang, H.-Y., Tagliaferro, P., Chung, M., Dennis, E., Sanabria, B., Schanz, N., Escosteguy-Neto, J. C., Ishiguro, H., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-17796-y · Cited by 147 · see citing works
Netser, S., Meyer, A., Magalnik, H., Zylbertal, A., Haskal, S., Briller, M., Bizer, A., Grinevich, V., & Wagner, S. (2020) · Nature Communications · doi:10.1038/s41467-020-19569-0 · Cited by 115 · see citing works
Neuro-Immune Mechanisms Regulating Social Behavior: Dopamine as Mediator?
Kopec, A. M., Smith, C. J. W., & Bilbo, S. D. (2019) · Trends in Neurosciences · doi:10.1016/j.tins.2019.02.005 · Cited by 68 · see citing works
Neuroinflammation, Early-Life Adversity, and Brain Development
Andersen, S. L. (2022) · Harvard Review of Psychiatry · doi:10.1097/hrp.0000000000000325 · Cited by 70 · see citing works
The neurobiology of social play behaviour: Past, present and future
Achterberg, E. J. M., & Vanderschuren, L. J. M. J. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105319 · Cited by 56 · see citing works
Kougias, D. G., Cortes, L. R., Moody, L., Rhoads, S., Pan, Y., & Juraska, J. M. (2017) · Endocrinology · doi:10.1210/en.2017-03047 · Cited by 51 · see citing works
Molecular and neurocircuitry mechanisms of social avoidance
Gellner, A., Voelter, J., Schmidt, U., Beins, E. C., Stein, V., Philipsen, A., & Hurlemann, R. (2020) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-020-03649-x · Cited by 51 · see citing works
Todd, S. W., Lumsden, E. W., Aracava, Y., Mamczarz, J., Albuquerque, E. X., & Pereira, E. F. R. (2020) · Neuropharmacology · doi:10.1016/j.neuropharm.2020.108271 · Cited by 41 · see citing works
Borsoï, M., Manduca, A., Bara, A., Lassalle, O., Pélissier‐Alicot, A., & Manzoni, O. J. (2019) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2019.00023 · Cited by 39 · see citing works
Baglot, S. L., VanRyzin, J. W., Marquardt, A. E., Aukema, R. J., Petrie, G. N., Hume, C., Reinl, E. L., Bieber, J. B., McLaughlin, R. J., McCarthy, M. M., et al. (2021) · Journal of Neuroscience Research · doi:10.1002/jnr.24992 · Cited by 37 · see citing works
Self-citationDevelopmental origins of sex differences in the neural circuitry of play
VanRyzin, J. W., Marquardt, A. E., & McCarthy, M. M. (2020) · International Journal of Play · doi:10.1080/21594937.2020.1723370 · Cited by 34 · see citing works
“If females are treated with CB1 and CB2 receptor agonists to ‘mimic’ the higher endocannabinoid levels, their newborn cell number and eventual play behavior is masculinized, even in the absence of testosterone (Argue et al., 2017; VanRyzin et al., 2019).”
BackgroundSelf-citationCutuli, D., Berretta, E., Caporali, P., Sampedro-Piquero, P., De Bartolo, P., Laricchiuta, D., Gelfo, F., Pesoli, M., Foti, F., Farioli Vecchioli, S., et al. (2019) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.02.015 · Cited by 30 · see citing works
Structure and function of the medial amygdala
(2020) · Handbook of Behavioral Neuroscience · doi:10.1016/b978-0-12-815134-1.00002-7 · Cited by 29 · see citing works
Lipid 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
Brain endocannabinoid signaling exhibits remarkable complexity
Gorzkiewicz, A., & Szemraj, J. (2018) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2018.06.012 · Cited by 24 · see citing works
Pietropaolo, S., & Marsicano, G. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.11.031 · Cited by 23 · see citing works
Sex differences in juvenile play behavior differ among rat strains
Northcutt, K. V., & Nwankwo, V. C. (2018) · Developmental Psychobiology · doi:10.1002/dev.21760 · Cited by 20 · see citing works
Walker, D. M., Zhou, X., Cunningham, A. M., Ramakrishnan, A., Cates, H. M., Lardner, C. K., Peña, C. J., Bagot, R. C., Issler, O., Van der Zee, Y., et al. (2022) · Biological Psychiatry · doi:10.1016/j.biopsych.2022.06.026 · Cited by 20 · see citing works
Fyke, W., Alarcón, J. M., Velinov, M. T., & Chadman, K. K. (2021) · Autism Research · doi:10.1002/aur.2520 · Cited by 19 · see citing works
Social behavior in prepubertal neurexin 1α deficient rats: A model of neurodevelopmental disorders.
Kight, K. E., Argue, K. J., Bumgardner, J. G., Bardhi, K., Waddell, J., & McCarthy, M. M. (2021) · Behavioral Neuroscience · doi:10.1037/bne0000482 · Cited by 17 · see citing works
Self-citationJohn, S. R., Dagash, W., Mohapatra, A. N., Netser, S., & Wagner, S. (2022) · Neuroscience · doi:10.1016/j.neuroscience.2022.04.020 · Cited by 16 · see citing works
The development of sex differences in the nervous system and behavior of flies, worms, and rodents
Meeh, K. L., Rickel, C. T., Sansano, A. J., & Shirangi, T. R. (2021) · Developmental Biology · doi:10.1016/j.ydbio.2021.01.010 · Cited by 13 · see citing works
Ahmed, M., Best, L. M., Pereira, C. F., Boileau, I., & Kloiber, S. M. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104680 · Cited by 14 · see citing works
Walker, D. M., Zhou, X., Ramakrishnan, A., Cates, H. M., Cunningham, A. M., Peña, C. J., Bagot, R. C., Issler, O., van der Zee, Y. Y., Lipschultz, A. P., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.02.18.955187 · Cited by 15 · see citing works
Lee, J., Reppucci, C. J., Bowden, S. M., Huez, E. D. M., Bredewold, R., & Veenema, A. H. (2021) · Hormones and Behavior · doi:10.1016/j.yhbeh.2024.105563 · Cited by 10 · see citing works
Trujillo-Villarreal, L. A., Cárdenas‐Tueme, M., Maldonado‐Ruiz, R., Reséndez‐Pérez, D., & Camacho‐Morales, A. (2020) · Journal of Neurochemistry · doi:10.1111/jnc.15141 · Cited by 12 · see citing works
Turano, A., McAuley, E. M., Muench, M. C., & Schwarz, J. M. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113449 · Cited by 11 · see citing works
Breach, M. R., Akouri, H. E., Costantine, S., Dodson, C. M., McGovern, N., & Lenz, K. M. (2023) · Hormones and Behavior · doi:10.1016/j.yhbeh.2023.105427 · Cited by 10 · see citing works
DeRosa, H., Caradonna, S. G., Tran, H., Marrocco, J., & Kentner, A. C. (2022) · eNeuro · doi:10.1523/eneuro.0148-22.2022 · Cited by 10 · see citing works
Kopec, A. M., Smith, C. J. W., Ayre, N. R., Sweat, S. C., & Bilbo, S. D. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/211029 · Cited by 6 · see citing works
Cannabis, Cannabinoide und das Endocannabinoidsystem
Schneider, M., Hoch, E., Simon, R., Pfeiffer-Gerschel, T., Kraus, L., Häuser, W., & Lutz, B. (2018) · Springer eBooks · doi:10.1007/978-3-662-57291-7_1 · Cited by 4 · see citing works
Rosario-Rodríguez, L. J., Cantres-Rosario, Y. M., Jesús, A. E. R. D., Mera-Pérez, A. M., Tosado-Rodríguez, E. L., Roche-Lima, A., & Meléndez, L. M. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms262110596 · Cited by 3 · see citing works
Bombardi, C., Salamanca, G., Tagliavia, C., Grandis, A., Cunha, R. Z., Gramenzi, A., Silva, M. D., Zannoni, A., & Chiocchetti, R. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26157613 · Cited by 3 · see citing works
Neurological Disorders and Women's Health: Contribution of Molecular Neuroimaging Techniques
Ekmekçioğlu, Ö., Albert, N. L., Heinrich, K., Tolboom, N., Weehaeghe, D. V., Traub‐Weidinger, T., Atay, L. Ö., Garibotto, V., & Morbelli, S. D. (2024) · Seminars in Nuclear Medicine · doi:10.1053/j.semnuclmed.2024.01.010 · Cited by 3 · see citing works
Sex and the Developing Brain Second Edition
McCarthy, M. M. (2017) · Colloquium Series on The Developing Brain · doi:10.4199/c00152ed1v01y201703dbr014 · Cited by 2 · see citing works
Self-citationDelage, C. I., Nys, G., Fillet, M., & Cornil, C. A. (2021) · Hormones and Behavior · doi:10.1016/j.yhbeh.2021.105024 · Cited by 2 · see citing works
Feminization of social play behavior depends on microgliaPreprint
VanRyzin, J. W., Marquardt, A. E., & McCarthy, M. M. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.08.19.608675 · Cited by 2 · see citing works
Self-citationDevelopmental Shifts in Amygdala Function
Rosenkranz, J. A. (2024) · Current topics in behavioral neurosciences · doi:10.1007/7854_2024_538 · Cited by 1 · see citing works
Endocannabinoids and social behavior
Trezza, V., Rava, A., & Feo, A. (2025) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-443-13908-6.00019-0 · Cited by 1 · see citing works
Breach, M. R., Schatz, B., Akouri, H. E., Tapp, Z. M., Lastra, A. Z., Weinstein, A. E., Mohamed, M., Walters, A. E., Mohamed, R., Toirov, O., et al. (2026) · Scientific Reports · doi:10.1038/s41598-026-41521-3 · Cited by 1 · see citing works
Kougias, D. G. (2018) · Illinois Digital Environment for Access to Learning and Scholarship (University of Illinois at Urbana-Champaign)
Endocannabinoids and sex differences in the developing social behavior network
McCarthy, M. M., Marquardt, A. E., & VanRyzin, J. W. (2022) · Elsevier eBooks · doi:10.1016/b978-0-12-823490-7.00006-x
Self-citationThe endocannabinoid system: Signaling and social motivation
Cysneiros, R. M., & Ribeiro, F. T. (2023) · Elsevier eBooks · doi:10.1016/b978-0-323-90877-1.00012-7
Endocannabinoid regulation of cortical functions
Dudok, B. (2025) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-443-13908-6.00012-8
Ahmed, M., Pereira, C. F., Best, L. M., Mahmood, R., George, T. P., Foll, B. L., Boileau, I., & Kloiber, S. (2026) · Journal of Psychopharmacology · doi:10.1177/02698811261478615
- Authors
- Argue, K. J., VanRyzin, J. W., Falvo, D. J., Whitaker, A. R., Yu, S. J., & McCarthy, M. M.
- Affiliations
- University of Maryland, Baltimore (US)
- Corresponding author
- Argue, Kathryn J
- ORCID
- Venue
- eneuro
- Publisher
- Society for Neuroscience
- Published
- 2017-01
- Volume
- 4
- Issue
- 1
- Pages
- ENEURO.0344-16.2017
- ISSN
- 2373-2822 (ISSN-L)
- PMC
- PMC5272923
- OpenAlex
- W2573093185
- Cited by
- 47
- References
- 91
- Citations by year
- 2026: 2 · 2025: 4 · 2024: 3 · 2023: 3 · 2022: 6 · 2021: 10 · 2020: 7 · 2019: 3 · 2018: 5 · 2017: 4
- FWCI
- 3.63
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- eNeuro (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- HHS | NIH | National Institute of Mental Health (100000025, RO1MH52716-020)
- HHS | NIH | National Institute on Drug Abuse (100000026, RO1DA039062-01)
- Topics
- Health Sciences › Medicine › Pharmacology › Cannabis and Cannabinoid Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Sexual Differentiation and Disorders
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Keywords
- endocannabinoid system, CB1 receptor, CB2 receptor, sex differences, social play, rough-and-tumble play, medial amygdala, masculinization, neuronal morphology, neonatal development, WIN 55,212-2
- MeSH terms
- Amygdala, Animals, Animals, Newborn, Female, Male, Neural Pathways, Neurons, Sex Characteristics, Social Behavior, Rats, Sprague-Dawley, Receptor, Cannabinoid, CB1, Receptor, Cannabinoid, CB2, Cannabinoid Receptor Modulators
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