Age and sex differences in oxytocin and vasopressin V1a receptor binding densities in the rat brain: focus on the social decision-making network
Open accessAbstract
Oxytocin (OT) and vasopressin (AVP) regulate various social behaviors via activation of the OT receptor (OTR) and the AVP V1a receptor (V1aR) in the brain. Social behavior often differs across development and between the sexes, yet our understanding of age and sex differences in brain OTR and V1aR binding remains incomplete. Here, we provide an extensive analysis of OTR and V1aR binding density throughout the brain in juvenile and adult male and female rats, with a focus on regions within the social decision-making network. OTR and V1aR binding density were higher in juveniles than in adults in regions associated with reward and socio-spatial memory and higher in adults than in juveniles in key regions of the social decision-making network and in cortical regions. We discuss possible implications of these shifts in OTR and V1aR binding density for the age-specific regulation of social behavior. Furthermore, sex differences in OTR and V1aR binding density were less numerous than age differences. The direction of these sex differences was region-specific for OTR but consistently higher in females than in males for V1aR. Finally, almost all sex differences in OTR and V1aR binding density were already present in juveniles and occurred in regions with denser binding in adults compared to juveniles. Possible implications of these sex differences for the sex-specific regulation of behavior, as well potential underlying mechanisms, are discussed. Overall, these findings provide an important framework for testing age- and sex-specific roles of OTR and V1aR in the regulation of social behavior.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
AVP-ir fibers, and to a lesser extent OT-ir fibers and their receptors, have been observed in several forebrain constituents of the SBNN in rodents.
“AVP-ir fibers, and, to a lesser extent, OT-ir fibers and their receptors have been observed in several forebrain constituents of the “social behavior neural network” (SBNN) in rodents”
From Quantitative mapping reveals age and sex differences in vasopressin, but not oxytocin, immunoreactivity in the rat social behavior neural network (2017) · cites this paper as Smith et al., 2017
The Introduction (page unavailable) says OT- and AVP-producing nuclei project fibers to many brain regions and that both receptors are widely distributed. The Discussion (page unavailable) identifies several receptor-bearing regions as nodes of the social behavior network. However, the paper does not establish that OT-immunoreactive fibers or their receptors occur there to a lesser extent than AVP-immunoreactive fibers; its measurements concern receptor binding, not that comparison of fibers. (LLM, conf=0.84)
Experimental — accuracy not yet measuredAdult rats expressed higher OTR binding density than juvenile rats in the pBNST, MePD, MPOA, and VMH; juveniles had higher OTR binding in the ventral LS; and males had higher OTR binding in these regions than females.
“adult rats expressed higher OTR binding density compared to juvenile rats in the pBNST, MePD, MPOA, and VMH, while juveniles had higher OTR binding in the ventral portion of the LS and males had higher levels of OTR binding in these regions compared to females (Smith et al., 2017)”
From Quantitative mapping reveals age and sex differences in vasopressin, but not oxytocin, immunoreactivity in the rat social behavior neural network (2017) · cites this paper as Smith et al., 2017
The Results section on age differences reports higher OTR binding in adults in the pBNST, MePD, MPOA, and VMH, and higher binding in juveniles in the ventral lateral septum (page unavailable). The sex-differences Results report higher binding in males in the pBNST, MePD, and VMH, but do not list the MPOA or ventral lateral septum; the Discussion does describe higher binding in males in the MPOA. Thus, the claim that males had higher binding in all the named regions is not supported for the ventral lateral septum. (LLM, conf=0.84)
Experimental — accuracy not yet measuredMale and female rats show very dense V1aR binding in the dorsal and intermediate LS, with females having even denser binding than males.
“Male and female rats show very dense V1aR binding in the dorsal and intermediate LS, with females having even denser binding than males [39,40].”
From Involvement of dopamine, but not norepinephrine, in the sex-specific regulation of juvenile socially rewarding behavior by vasopressin (2018) · cites this paper as [39]
The Results section, “Sex differences in V1aR binding density” (page unavailable), reports higher V1aR binding in females than males in the dorsal lateral septum. The paper does not establish the claim of very dense V1aR binding in both dorsal and intermediate lateral septum: its Table 1 identifies intermediate lateral septum binding as OTR, not V1aR. (LLM, conf=0.88)
Experimental — accuracy not yet measuredThe MPOA contains oxytocin receptors in both sexes and at both juvenile and adult ages.
“the MPOA contains oxytocin receptors in both sexes and at both juvenile and adult ages (Smith et al., 2017)”
From Quantitative mapping reveals age and sex differences in vasopressin, but not oxytocin, immunoreactivity in the rat social behavior neural network (2017) · cites this paper as Smith et al., 2017
Robust age and sex differences were found for the oxytocin receptor (OTR) across multiple nodes of the rat SBNN.
“robust age and sex differences were found for the OTR across multiple nodes of the rat SBNN (Smith et al., 2017)”
From Quantitative mapping reveals age and sex differences in vasopressin, but not oxytocin, immunoreactivity in the rat social behavior neural network (2017) · cites this paper as Smith et al., 2017
The MPOA is one of a few regions that show abundant AVP fibers but virtually no V1AR.
“the MPOA is one of a few regions that show abundant AVP fibers, but virtually no V1AR (Smith et al., 2017)”
From Quantitative mapping reveals age and sex differences in vasopressin, but not oxytocin, immunoreactivity in the rat social behavior neural network (2017) · cites this paper as Smith et al., 2017
The Methods table lists OTR binding in the MPOA, but gives no MPOA V1aR measurement. The Introduction describes AVP fiber projections broadly, not abundant fibers in the MPOA. Searches for MPOA, AVP fibers, and absent V1aR found no passage establishing the claimed combination. (LLM, conf=0.72)
Experimental — accuracy not yet measuredIn the mammalian brain, OTRs and V1aRs are robustly expressed in many regions, but their distributions often differ.
“In mammalian brain OTRs and V1aRs are robustly expressed in many regions but their distributions often differ [9; 21; 22] (Figure 3).”
From Cross-talk among oxytocin and arginine-vasopressin receptors: Relevance for basic and clinical studies of the brain and periphery (2018) · cites this paper as [22]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The adolescent brain and age-related behavioral manifestations
Spear, L. P. (2000) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(00)00014-2 · Cited by 5,433 · see citing works
The oxytocin receptor system: structure, function, and regulation
Gimpl, G., & Fahrenholz, F. (2001) · Physiological Reviews · doi:10.1152/physrev.2001.81.2.629 · Cited by 3,089 · see citing works
More powerful procedures for multiple significance testing
Hochberg, Y., & Benjamini, Y. (1990) · Statistics in Medicine · doi:10.1002/sim.4780090710 · Cited by 2,715 · see citing works
Understanding adolescence as a period of social–affective engagement and goal flexibility
Crone, E. A., & Dahl, R. E. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3313 · Cited by 2,507 · see citing works
Is Adolescence a Sensitive Period for Sociocultural Processing?
Blakemore, S.-J., & Mills, K. L. (2014) · Annual Review of Psychology · doi:10.1146/annurev-psych-010213-115202 · Cited by 2,264 · cited 3× · see citing works
“The juvenile period (here synonymous with the peri-pubertal or early adolescent period and spanning postnatal days 28–42 in rats (Spear 2000) is characterized by increased time spent engaging in peer interactions, novelty-seeking, and risk-taking behavior than at younger or older ages (Doremus-Fitzwater et al. 2010; B…”
BackgroundSteinberg, L., Albert, D., Cauffman, E., Banich, M., Graham, S., & Woolard, J. (2008) · Developmental Psychology · doi:10.1037/a0012955 · Cited by 1,542 · see citing works
Oxytocin shapes the neural circuitry of trust and trust adaptation in humans
Baumgartner, T., Heinrichs, M., Vonlanthen, A., Fischbacher, U., & Fehr, E. (2008) · Neuron · doi:10.1016/j.neuron.2008.04.009 · Cited by 1,258 · see citing works
NEWMAN, S. W. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb09271.x · Cited by 1,189 · see citing works
Peers increase adolescent risk taking by enhancing activity in the brain’s reward circuitry
Chein, J., Albert, D., O’Brien, L., Uckert, K., & Steinberg, L. (2011) · Developmental Science · doi:10.1111/j.1467-7687.2010.01035.x · Cited by 1,180 · cited 1× · see citing works
“…of peers can increase alcohol intake and risk-taking behavior in adolescent rats, mice and humans (Varlinskaya et al. 2015; Logue et al. 2014; Chein et al. 2011, Smith et al. 2015), while strong social attachments can reduce the risk of developing a drug addiction in humans (Tops et al.…”
BackgroundSocial reward requires coordinated activity of nucleus accumbens oxytocin and serotonin
Dölen, G., Darvishzadeh, A., Huang, K. W., & Malenka, R. C. (2013) · Nature · doi:10.1038/nature12518 · Cited by 1,161 · see citing works
Evoked axonal oxytocin release in the central amygdala attenuates fear response
Knobloch, H. S., Charlet, A., Hoffmann, L. C., Eliava, M., Khrulev, S., Cetin, A. H., Osten, P., Schwarz, M. K., Seeburg, P. H., Stoop, R., et al. (2012) · Neuron · doi:10.1016/j.neuron.2011.11.030 · Cited by 1,049 · see citing works
Intra- and extrahypothalamic vasopressin and oxytocin pathways in the rat
Buijs, R. M., Swaab, D. F., Dogterom, J., & van Leeuwen, F. W. (1978) · Cell and Tissue Research · doi:10.1007/bf00224932 · Cited by 1,029 · see citing works
The Vertebrate mesolimbic reward system and social behavior network: A comparative synthesis
O'Connell, L. A., & Hofmann, H. A. (2011) · Journal of Comparative Neurology · doi:10.1002/cne.22735 · Cited by 986 · see citing works
Dendritic peptide release and peptide-dependent behaviours
Ludwig, M., & Leng, G. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn1845 · Cited by 945 · see citing works
Intra- and extrahypothalamic vasopressin and oxytocin pathways in the rat
Buijs, R. M. (1978) · Cell and Tissue Research · doi:10.1007/bf00212323 · Cited by 830 · see citing works
Vasopressin and Oxytocin Excite Distinct Neuronal Populations in the Central Amygdala
Huber, D., Veinante, P., & Stoop, R. (2005) · Science · doi:10.1126/science.1105636 · Cited by 804 · see citing works
Oxytocin enables maternal behaviour by balancing cortical inhibition
Marlin, B. J., Mitre, M., D’amour, J. A., Chao, M. V., & Froemke, R. C. (2015) · Nature · doi:10.1038/nature14402 · Cited by 744 · see citing works
Connections of the rat lateral septal complex 1Published on the World Wide Web on 2 June 1997. 1
Risold, P. Y., & Swanson, L. W. (1997) · Brain Research Reviews · doi:10.1016/s0165-0173(97)00009-x · Cited by 671 · see citing works
Lim, M. M., Wang, Z., Olazábal, D. E., Ren, X., Terwilliger, E. F., & Young, L. J. (2004) · Nature · doi:10.1038/nature02539 · Cited by 628 · see citing works
Evolution of a Vertebrate Social Decision-Making Network
O’Connell, L. A., & Hofmann, H. A. (2012) · Science · doi:10.1126/science.1218889 · Cited by 608 · see citing works
Liu, Y., & Wang, Z. X. (2003) · Neuroscience · doi:10.1016/s0306-4522(03)00555-4 · Cited by 580 · cited 1× · see citing works
“…of the OTR in the striatum promotes partner preference formation and alloparental care in adult female prairie voles (Olazábal and Young 2006; Keebaugh et al. 2015; Ross et al. 2009; Liu and Wang 2003) and conditioned place preference for social stimuli in adult male mice (Dölen et al. 2013).”
BackgroundWater associated zero maze: a novel rat test for long term traumatic re-experiencing
Ritov, G., & Richter‐Levin, G. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00001 · Cited by 579 · see citing works
Panksepp, J. (1981) · Developmental Psychobiology · doi:10.1002/dev.420140405 · Cited by 537 · see citing works
de Vries, G. J., & Buijs, R. M. (1983) · Brain Research · doi:10.1016/0006-8993(83)90855-7 · Cited by 524 · cited 1× · see citing works
“AVP is also synthesized in the bed nucleus of the stria terminalis (BNST) and medial amygdala (Sofroniew and Weindl 1978; Sofroniew 1980; Caffé et al. 1987; De Vries et al. 1981; De Vries and Buijs 1983; Rood and De Vries 2011).”
MethodCellular Mechanisms of Social Attachment
Young, L. J., Lim, M. M., Gingrich, B., & Insel, T. R. (2001) · Hormones and Behavior · doi:10.1006/hbeh.2001.1691 · Cited by 523 · see citing works
Dumais, K. M., & Veenema, A. H. (2016) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2015.04.003 · Cited by 520 · cited 10× · see citing works
“…cortex, and perirhinal cortex for the OTR and in the dorsal lateral septum, arcuate nucleus, and ventromedial thalamus for the V1aR) that were either not found or not characterized in previous studies of receptor binding (Dumais et al. 2013; Dumais and Veenema 2016a, b) or mRNA (Szot et al. 1994).”
BackgroundMethodResultInfluentialSelf-citationYoung, L. J., Nilsen, R., Waymire, K. G., MacGregor, G. R., & Insel, T. R. (1999) · Nature · doi:10.1038/23475 · Cited by 488 · see citing works
Pedersen, C. A., Caldwell, J. D., Walker, C., Ayers, G., & Mason, G. A. (1994) · Behavioral Neuroscience · doi:10.1037/0735-7044.108.6.1163 · Cited by 475 · see citing works
The psychobiology of play: Theoretical and methodological perspectives
Panksepp, J., Siviy, S., & Normansell, L. (1984) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(84)90005-8 · Cited by 468 · see citing works
Meibach, R. C., & Siegel, A. (1977) · Brain Research · doi:10.1016/0006-8993(77)90088-9 · Cited by 438 · see citing works
Modulation of social memory in male rats by neurohypophyseal peptides
Dantzer, R., Bluthe, R. M., Koob, G. F., & Le Moal, M. (1987) · Psychopharmacology · doi:10.1007/bf00518192 · Cited by 423 · see citing works
The ins and outs of the striatum: Role in drug addiction
Yager, L. M., Garcia, A. F., Wunsch, A. M., & Ferguson, S. M. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.06.033 · Cited by 421 · see citing works
Doremus-Fitzwater, T. L., Varlinskaya, E. I., & Spear, L. P. (2010) · Brain and Cognition · doi:10.1016/j.bandc.2009.08.008 · Cited by 397 · see citing works
Douglas, L. A., Varlinskaya, E. I., & Spear, L. P. (2004) · Developmental Psychobiology · doi:10.1002/dev.20025 · Cited by 389 · see citing works
Oxytocin Selectively Gates Fear Responses Through Distinct Outputs from the Central Amygdala
Viviani, D., Charlet, A., van den Burg, E., Robinet, C., Hurni, N., Abatis, M., Magara, F., & Stoop, R. (2011) · Science · doi:10.1126/science.1201043 · Cited by 381 · see citing works
Intracellular calcium stores regulate activity-dependent neuropeptide release from dendrites
Ludwig, M., Sabatier, N., Bull, P. M., Landgraf, R., Dayanithi, G., & Leng, G. (2002) · Nature · doi:10.1038/nature00822 · Cited by 346 · see citing works
Oxytocin enhances hippocampal spike transmission by modulating fast-spiking interneurons
Owen, S. F., Tuncdemir, S. N., Bader, P. L., Tirko, N. N., Fishell, G., & Tsien, R. W. (2013) · Nature · doi:10.1038/nature12330 · Cited by 339 · see citing works
Central vasopressin and oxytocin release: regulation of complex social behaviours
VEENEMA, A., & NEUMANN, I. (2008) · Progress in Brain Research · doi:10.1016/s0079-6123(08)00422-6 · Cited by 338 · see citing works
Self-citationVasopressin-dependent neural circuits underlying pair bond formation in the monogamous prairie vole
Lim, M. M., & Young, L. J. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2003.12.008 · Cited by 322 · see citing works
Ross, H. E., Freeman, S. M., Spiegel, L. L., Ren, X., Terwilliger, E. F., & Young, L. J. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.5039-08.2009 · Cited by 322 · see citing works
De Vries, G. J., Buds, R. M., & Swaab, D. F. (1981) · Brain Research · doi:10.1016/0006-8993(81)90989-6 · Cited by 319 · cited 3× · see citing works
“Interestingly, the age difference in V1aR binding density in the lateral septum corresponds with a similar age difference in AVP fiber density in the lateral septum (De Vries et al. 1981), further supporting an age-specific role of the AVP system in the lateral septum.”
BackgroundMethodSofroniew, M. V. (1980) · Journal of Histochemistry & Cytochemistry · doi:10.1177/28.5.7381192 · Cited by 317 · cited 1× · see citing works
“AVP is also synthesized in the bed nucleus of the stria terminalis (BNST) and medial amygdala (Sofroniew and Weindl 1978; Sofroniew 1980; Caffé et al. 1987; De Vries et al. 1981; De Vries and Buijs 1983; Rood and De Vries 2011).”
MethodSofroniew, M. V., & Weindl, A. (1978) · American Journal of Anatomy · doi:10.1002/aja.1001530305 · Cited by 312 · see citing works
Pitkow, L. J., Sharer, C. A., Ren, X., Insel, T. R., Terwilliger, E. F., & Young, L. J. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-18-07392.2001 · Cited by 295 · see citing works
Caffé, A. R., van Leeuwen, F. W., & Luiten, P. G. M. (1987) · Journal of Comparative Neurology · doi:10.1002/cne.902610206 · Cited by 286 · see citing works
Brain vasopressin is an important regulator of maternal behavior independent of dams’ trait anxiety
Bosch, O. J., & Neumann, I. D. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0807412105 · Cited by 280 · see citing works
Nucleus Accumbens μ-Opioid Receptors Mediate Social Reward
Trezza, V., Damsteegt, R., Achterberg, E. J. M., & Vanderschuren, L. J. M. J. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.5492-10.2011 · Cited by 263 · see citing works
Nakajima, M., Görlich, A., & Heintz, N. (2014) · Cell · doi:10.1016/j.cell.2014.09.020 · Cited by 262 · see citing works
Evolution of oxytocin pathways in the brain of vertebrates
Knobloch, H. S., & Grinevich, V. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00031 · Cited by 259 · see citing works
Pellis, S. M., & Pellis, V. C. (1990) · Developmental Psychobiology · doi:10.1002/dev.420230303 · Cited by 255 · see citing works
Charting the maturation of the frontal lobe: An electrophysiological strategy
Segalowitz, S. J., & Davies, P. L. (2004) · Brain and Cognition · doi:10.1016/s0278-2626(03)00283-5 · Cited by 246 · see citing works
Olazábal, D. E., & Young, L. J. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2005.12.010 · Cited by 230 · see citing works
Tribollet, E., Charpak, S., Schmidt, A., Dubois-Dauphin, M., & Dreifuss, J. (1989) · The Journal of Neuroscience · doi:10.1523/jneurosci.09-05-01764.1989 · Cited by 228 · see citing works
Engelmann, M., & Landgraf, R. (1994) · Physiology & Behavior · doi:10.1016/0031-9384(94)90022-1 · Cited by 225 · see citing works
The supramammillary area: its organization, functions and relationship to the hippocampus
Pan, W.-X., & McNaughton, N. (2004) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2004.09.003 · Cited by 223 · see citing works
An intrinsic vasopressin system in the olfactory bulb is involved in social recognition
Tobin, V. A., Hashimoto, H., Wacker, D. W., Takayanagi, Y., Langnaese, K., Caquineau, C., Noack, J., Landgraf, R., Onaka, T., Leng, G., et al. (2010) · Nature · doi:10.1038/nature08826 · Cited by 213 · see citing works
Lukas, M., Toth, I., Veenema, A. H., & Neumann, I. D. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.09.018 · Cited by 211 · see citing works
Goodson, J. L., & Kabelik, D. (2009) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2009.05.007 · Cited by 204 · see citing works
Tribollet, E., Audigier, S., Dubois-Dauphin, M., & Dreifuss, J. J. (1990) · Brain Research · doi:10.1016/0006-8993(90)90232-z · Cited by 203 · see citing works
Dumais, K. M., Bredewold, R., Mayer, T. E., & Veenema, A. H. (2013) · Hormones and Behavior · doi:10.1016/j.yhbeh.2013.08.012 · Cited by 201 · see citing works
Self-citationAlbers, H. E. (2015) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2014.07.001 · Cited by 200 · see citing works
Multisensory Integration of Natural Odors and Sounds in the Auditory Cortex
Cohen, L., Rothschild, G., & Mizrahi, A. (2011) · Neuron · doi:10.1016/j.neuron.2011.08.019 · Cited by 192 · see citing works
Johnson, Z. V., Walum, H., Jamal, Y. A., Xiao, Y., Keebaugh, A. C., Inoue, K., & Young, L. J. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.11.011 · Cited by 190 · see citing works
Curley, J. P. (2009) · Frontiers in Behavioral Neuroscience · doi:10.3389/neuro.08.025.2009 · Cited by 184 · see citing works
Lukas, M., Bredewold, R., Neumann, I. D., & Veenema, A. H. (2010) · Neuropharmacology · doi:10.1016/j.neuropharm.2009.06.020 · Cited by 183 · see citing works
Self-citationVeenema, A. H., Beiderbeck, D. I., Lukas, M., & Neumann, I. D. (2010) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.03.006 · Cited by 180 · see citing works
Self-citationDevelopmental Perspectives on Oxytocin and Vasopressin
Hammock, E. A. D. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.120 · Cited by 177 · see citing works
McGregor, I. S., Callaghan, P. D., & Hunt, G. E. (2008) · British Journal of Pharmacology · doi:10.1038/bjp.2008.132 · Cited by 171 · see citing works
Allen, G. V., & Hopkins, D. A. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902860303 · Cited by 167 · see citing works
Sex-specific modulation of juvenile social play by vasopressin
Veenema, A. H., Bredewold, R., & De Vries, G. J. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.06.002 · Cited by 166 · cited 6× · see citing works
“2016), as well as in juveniles (Veenema et al. 2013; Bredewold et al. 2014), we hypothesize that sex differences in OTR and V1aR binding previously observed in adults (Dumais et al.”
BackgroundInfluentialSelf-citationKondo, Y. (1992) · Physiology & Behavior · doi:10.1016/0031-9384(92)90074-c · Cited by 163 · see citing works
Oxytocin receptor density is associated with male mating tactics and social monogamy
Ophir, A. G., Gessel, A., Zheng, D.-J., & Phelps, S. M. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.01.007 · Cited by 161 · see citing works
Ontogeny of amicable social behavior in the mouse: Gender differences and ongoing isolation outcomes
Terranova, M. L., Laviola, G., & Alleva, E. (1993) · Developmental Psychobiology · doi:10.1002/dev.420260805 · Cited by 160 · see citing works
Bredewold, R., Smith, C. J. W., Dumais, K. M., & Veenema, A. H. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00216 · Cited by 157 · see citing works
Self-citationTRIBOLLET, E., DUBOIS‐DAUPHIN, M., DREIFUSS, J. J., BARBERIS, C., & JARD, S. (1992) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1992.tb34343.x · Cited by 156 · see citing works
Endogenous oxytocin is involved in short-term olfactory memory in female rats
Engelmann, M., Ebner, K., Wotjak, C. T., & Landgraf, R. (1998) · Behavioural Brain Research · doi:10.1016/s0166-4328(97)00084-3 · Cited by 156 · see citing works
Copulatory behavior in male rats with lesions in the bed nucleus of the stria terminalis
Emery, D. E., & Sachs, B. D. (1976) · Physiology & Behavior · doi:10.1016/0031-9384(76)90044-5 · Cited by 151 · see citing works
Keebaugh, A. C., Barrett, C. E., Laprairie, J. L., Jenkins, J. J., & Young, L. J. (2015) · Social Neuroscience · doi:10.1080/17470919.2015.1040893 · Cited by 150 · see citing works
Everts, H. G. J., & Koolhaas, J. M. (1999) · Behavioural Brain Research · doi:10.1016/s0166-4328(98)00004-7 · Cited by 148 · see citing works
Age differences in the impact of peers on adolescents’ and adults’ neural response to reward
Smith, A. R., Steinberg, L., Strang, N., & Chein, J. (2015) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2014.08.010 · Cited by 147 · see citing works
Social recognition does not involve vasopressinergic neurotransmission in female rats
Bluthe´, R.-M., & Dantzer, R. (1990) · Brain Research · doi:10.1016/0006-8993(90)91613-l · Cited by 147 · see citing works
Mattie Tops, A., Koole, S. L., IJzerman, H., & Buisman‐Pijlman, F. T. A. (2013) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2013.07.015 · Cited by 146 · see citing works
Beery, A. K., Lacey, E. A., & Francis, D. D. (2008) · Journal of Comparative Neurology · doi:10.1002/cne.21638 · Cited by 144 · see citing works
Gur, R., Tendler, A., & Wagner, S. (2014) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.03.022 · Cited by 144 · see citing works
Buisman‐Pijlman, F. T. A., Sumracki, N. M., Gordon, J. J., Hull, P. R., Carter, C. S., & Mattie Tops, A. (2013) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2013.09.005 · Cited by 143 · see citing works
Developmental experiences and the oxytocin receptor system
Bales, K. L., & Perkeybile, A. M. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.12.013 · Cited by 142 · see citing works
McCarthy, M. M., Kleopoulos, S. P., Mobbs, C. V., & Pfaff, D. W. (2008) · Neuroendocrinology · doi:10.1159/000126689 · Cited by 142 · see citing works
A Selective Oxytocin Antagonist Attenuates Progesterone Facilitation of Female Sexual Behavior
Witt, D. M., & Insel, T. R. (1991) · Endocrinology · doi:10.1210/endo-128-6-3269 · Cited by 138 · see citing works
Vasopressin innervation of the mouse ( <i>Mus musculus</i> ) brain and spinal cord
Rood, B. D., & De Vries, G. J. (2011) · Journal of Comparative Neurology · doi:10.1002/cne.22635 · Cited by 134 · see citing works
Vasopressin released within the central amygdala promotes maternal aggression
Bosch, O. J., & Neumann, I. D. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07115.x · Cited by 134 · see citing works
Burkett, J. P., Spiegel, L. L., Inoue, K., Murphy, A. Z., & Young, L. J. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.117 · Cited by 133 · see citing works
Ontogeny of oxytocin receptors in rat forebrain: A quantitative study
Shapiro, L. E., & Insel, T. R. (1989) · Synapse · doi:10.1002/syn.890040312 · Cited by 131 · see citing works
Bosch, O. J., Pförtsch, J., Beiderbeck, D. I., Landgraf, R., & Neumann, I. D. (2010) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2010.01984.x · Cited by 130 · see citing works
Veenema, A. H., Bredewold, R., & De Vries, G. J. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.10.002 · Cited by 129 · see citing works
Self-citationCentral vasopressin and oxytocin receptor distributions in two species of singing mice
Polly Campbell, A., Ophir, A. G., & Phelps, S. M. (2009) · The Journal of Comparative Neurology · doi:10.1002/cne.22116 · Cited by 128 · see citing works
Distribution of messenger RNA for the vasopressin V1a receptor in the CNS of male and female rats
Szot, P., Bale, T. L., & Dorsa, D. M. (1994) · Molecular Brain Research · doi:10.1016/0169-328x(94)90111-2 · Cited by 125 · see citing works
Sexually dimorphic expression of oxytocin binding sites in forebrain and spinal cord of the rat
Uhl-Bronner, S., Waltisperger, E., Martínez-Lorenzana, G., Condes Lara, M., & Freund-Mercier, M. J. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.05.025 · Cited by 123 · see citing works
Regulation of activity‐dependent dendritic vasopressin release from rat supraoptic neurones
Ludwig, M., Bull, P. M., Tobin, V. A., Sabatier, N., Landgraf, R., Dayanithi, G., & Leng, G. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2005.083931 · Cited by 122 · see citing works
Lukas, M., Bredewold, R., Landgraf, R., Neumann, I. D., & Veenema, A. H. (2011) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2010.11.007 · Cited by 122 · see citing works
Self-citationThe role of limbic vasopressin and oxytocin in social recognition
van Wimersma Greidanus, T. B., & Maigret, C. (1996) · Brain Research · doi:10.1016/0006-8993(95)01505-1 · Cited by 117 · see citing works
Popik, P., & van Ree, J. M. (1991) · European Neuropsychopharmacology · doi:10.1016/0924-977x(91)90010-r · Cited by 114 · see citing works
Improved cortical entrainment to infant communication calls in mothers compared with virgin mice
Liu, R. C., Linden, J. F., & Schreiner, C. E. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04840.x · Cited by 112 · see citing works
Medial amygdala lesions in male rats reduce aggressive behavior: interference with experience
Vochteloo, J. D., & Koolhaas, J. M. (1987) · Physiology & Behavior · doi:10.1016/0031-9384(87)90137-5 · Cited by 109 · see citing works
Caughey, S. D., Klampfl, S. M., Bishop, V. R., Pfoertsch, J., Neumann, I. D., Bosch, O. J., & Meddle, S. L. (2011) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2011.02224.x · Cited by 107 · see citing works
Consiglio, A. R., Borsoi, A., Pereira, G. A. M., & Lucion, A. B. (2005) · Physiology & Behavior · doi:10.1016/j.physbeh.2005.05.002 · Cited by 106 · see citing works
Sabihi, S., Durosko, N. E., Dong, S. M., & Leuner, B. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.03.009 · Cited by 106 · see citing works
Young, K. A., Liu, Y., Gobrogge, K. L., Wang, H., & Wang, Z. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.4275-13.2014 · Cited by 99 · see citing works
Resendez, S. L., Dome, M., Gormley, G., Franco, D., Nevárez, N., Hamid, A. A., & Aragona, B. J. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.4123-12.2013 · Cited by 93 · see citing works
Kalamatianos, T., Faulkes, C. G., Oosthuizen, M. K., Poorun, R., Bennett, N. C., & Coen, C. W. (2010) · Journal of Comparative Neurology · doi:10.1002/cne.22302 · Cited by 92 · see citing works
Claro, F., Segovia, S., Guillamón, A., & del Abril, A. (1995) · Brain Research Bulletin · doi:10.1016/0361-9230(94)00118-k · Cited by 91 · see citing works
Adolescent mice, unlike adults, consume more alcohol in the presence of peers than alone
Logue, S., Chein, J., Gould, T., Holliday, E., & Steinberg, L. (2014) · Developmental Science · doi:10.1111/desc.12101 · Cited by 88 · see citing works
Young, L. J., Wang, Z., Cooper, T. T., & Albers, H. E. (2000) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2000.00573.x · Cited by 88 · see citing works
Calcagnoli, F., de Boer, S. F., Beiderbeck, D. I., Althaus, M., Koolhaas, J. M., & Neumann, I. D. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.12.050 · Cited by 84 · see citing works
Buijs, R. M. (1980) · Journal of Histochemistry & Cytochemistry · doi:10.1177/28.4.6989899 · Cited by 81 · see citing works
Dumais, K. M., Alonso, A. G., Immormino, M. A., Bredewold, R., & Veenema, A. H. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.11.007 · Cited by 72 · see citing works
Self-citationVarlinskaya, E. I., Truxell, E. M., & SPEAR, L. P. (2015) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.12604 · Cited by 71 · see citing works
Sturman, D. A., & Moghaddam, B. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.4210-10.2011 · Cited by 69 · see citing works
Castration reduces vasopressin receptor binding in the hamster hypothalamus
Johnson, A. E., Barberis, C., & Elliott Albers, H. (1995) · Brain Research · doi:10.1016/0006-8993(95)00010-n · Cited by 65 · see citing works
Preoptic Inputs and Mechanisms that Regulate Maternal Responsiveness
Dobolyi, Á., Grattan, D. R., & Stolzenberg, D. S. (2014) · Journal of Neuroendocrinology · doi:10.1111/jne.12185 · Cited by 64 · see citing works
Lukas, M., & Neumann, I. D. (2014) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2014.03.013 · Cited by 63 · see citing works
Schulze, H. G., & Gorzalka, B. B. (1991) · Neuropeptides · doi:10.1016/0143-4179(91)90008-7 · Cited by 60 · see citing works
Snijdewint, F. G. M., van Leeuwen, F. W. B., & Gj, B. (1989) · PubMed · Cited by 56 · see citing works
Zheng, D., Larsson, B., Phelps, S. M., & Ophir, A. G. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.02.024 · Cited by 48 · see citing works
Elevated Correlations in Neuronal Ensembles of Mouse Auditory Cortex Following Parturition
Rothschild, G., Cohen, L., Mizrahi, A., & Nelken, I. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.4656-12.2013 · Cited by 46 · see citing works
Appearance and Transient Expression of Vasopressin and Oxytocin Receptors in the Rat Brain
Tribollet, E., Goumaz, M., Raggenbass, M., & Dreifuss, J.-J. (1991) · Journal of Receptor Research · doi:10.3109/10799899109066412 · Cited by 46 · see citing works
Septal oxytocin administration impairs peer affiliation via V1a receptors in female meadow voles
Anacker, A. M. J., Christensen, J. D., LaFlamme, E. M., Grunberg, D. M., & Beery, A. K. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2016.02.025 · Cited by 44 · see citing works
Ismail, N., Gelez, H., Lachapelle, I., & Pfaus, J. G. (2009) · Physiology & Behavior · doi:10.1016/j.physbeh.2008.09.013 · Cited by 38 · see citing works
Chapter 1.4 Vasopressin binding sites in the central nervous system: Distribution and regulation
Tribollet, E., Arsenijévic, Y., & Barberis, C. (1999) · Progress in brain research · doi:10.1016/s0079-6123(08)61561-7 · Cited by 37 · see citing works
Masugi-Tokita, M., Flor, P. J., & Kawata, M. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2015.198 · Cited by 35 · see citing works
Sexually dimorphic c-Fos expression following spatial working memory in young and adult rats
Méndez-López, M., Méndez, M., López, L., & Arias, J. L. (2009) · Physiology & Behavior · doi:10.1016/j.physbeh.2009.06.006 · Cited by 33 · see citing works
Noack, J., Murau, R., & Engelmann, M. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00152 · Cited by 32 · see citing works
Delville, Y., & Ferris, C. F. (1995) · Brain Research · doi:10.1016/0006-8993(95)00291-w · Cited by 31 · see citing works
Ophir, A. G., Sorochman, G., Evans, B. L., & Prounis, G. S. (2013) · Journal of Neuroendocrinology · doi:10.1111/jne.12049 · Cited by 31 · see citing works
Kelly, A. M., & Ophir, A. G. (2015) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2015.10.010 · Cited by 28 · see citing works
Behavioral effects of arginine8-vasopressin in the Hebb–Williams maze
Paban, V., Soumireu-Mourat, B., & Alescio‐Lautier, B. (2003) · Behavioural Brain Research · doi:10.1016/s0166-4328(02)00316-9 · Cited by 14 · see citing works
Dumais, K. M., & Veenema, A. H. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-802114-9.00011-1 · Cited by 11 · see citing works
Self-citationRelative Role of Neural Substrates in the Aggressive Behavior of Rats
Patil, S. N., & Brid, S. V. (2010) · Journal of Basic and Clinical Physiology and Pharmacology · doi:10.1515/jbcpp.2010.21.4.357 · Cited by 9 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- Paxinos G Watson C The rat brain atlas in stereotaxic coordinates 2007 Oxford Academic Press, Elsevier Inc
Cited by
Sorted by citations
The oxytocin receptor: from intracellular signaling to behavior
Jurek, B., & Neumann, I. D. (2018) · Physiological Reviews · doi:10.1152/physrev.00031.2017 · Cited by 999 · see citing works
Song, Z., & Albers, H. E. (2018) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2017.10.004 · Cited by 244 · see citing works
Duque-Wilckens, N., Steinman, M. Q., Busnelli, M., Chini, B., Yokoyama, S., Pham, M., Laredo, S. A., Hao, R., Perkeybile, A. M., Minie, V. A., et al. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.08.024 · Cited by 181 · see citing works
Microbial lysate upregulates host oxytocin
Varian, B. J., Poutahidis, T., DiBenedictis, B. T., Levkovich, T., Ibrahim, Y., Didyk, E., Shikhman, L., Cheung, H. K., Hardas, A., Ricciardi, C. E., et al. (2017) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2016.11.002 · Cited by 153 · see citing works
Self-citationBredewold, R., & Veenema, A. H. (2018) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.02.011 · Cited by 144 · see citing works
Self-citationDiBenedictis, B. T., Nussbaum, E. R., Cheung, H. K., & Veenema, A. H. (2017) · Journal of Comparative Neurology · doi:10.1002/cne.24216 · Cited by 74 · see citing works
“…tract 2564 | The Journal of Comparative Neurology DIBENEDICTIS ET AL. contains oxytocin receptors in both sexes and at both juvenile and adult ages (Smith et al., 2017), suggesting the possibility that AVP released in the MPOA acts through oxytocin receptors rather than V1AR, which has been…”
BackgroundInfluentialSelf-citationSmith, C. J. W., DiBenedictis, B. T., & Veenema, A. H. (2019) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2019.02.001 · Cited by 59 · see citing works
Inoue, K., Ford, C. L., Horie, K., & Young, L. J. (2022) · Journal of Comparative Neurology · doi:10.1002/cne.25382 · Cited by 45 · see citing works
Rigney, N., Whylings, J., de Vries, G. J., & Petrulis, A. (2021) · Neuroendocrinology · doi:10.1159/000509421 · Cited by 42 · see citing works
Bredewold, R., Nascimento, N. F., Ro, G. S., Cieslewski, S. E., Reppucci, C. J., & Veenema, A. H. (2018) · Neuropsychopharmacology · doi:10.1038/s41386-018-0100-2 · Cited by 31 · see citing works
Self-citationOxytocin receptor behavioral effects and cell types in the bed nucleus of the stria terminalis
Luo, P. X., Zakharenkov, H. C., Torres, L. Y., Rios, R. A., Gegenhuber, B., Black, A. M., Xu, C. K., Minie, V. A., Tran, A. M., Tollkuhn, J., et al. (2022) · Hormones and Behavior · doi:10.1016/j.yhbeh.2022.105203 · Cited by 27 · see citing works
Bredewold, R., Washington, C., & Veenema, A. H. (2025) · Neuropsychopharmacology · doi:10.1038/s41386-024-01987-z · Cited by 13 · see citing works
Self-citation
- Authors
- Smith, C. J. W., Poehlmann, M. L., Li, S., Ratnaseelan, A. M., Bredewold, R., & Veenema, A. H.
- Affiliations
- Boston College (US)
- Corresponding author
- Smith, Caroline J. W.
- Venue
- Brain Structure and Function
- Published
- 2016-07-07
- Volume
- 222
- Issue
- 2
- Pages
- 981-1006
- ISSN
- 1863-2653 (ISSN-L)
- 1863-2661
- PMC
- PMC5334374
- OpenAlex
- W2462807191
- Cited by
- 143
- References
- 137
- Citations by year
- 2026: 16 · 2025: 12 · 2024: 12 · 2023: 9 · 2022: 10 · 2021: 17 · 2020: 14 · 2019: 21 · 2018: 18 · 2017: 13 · 2016: 1
- FWCI
- 27.74
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- Brain Structure and Function (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- National Science Foundation (2012138127, IOS1253386)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Keywords
- oxytocin receptor, vasopressin V1a receptor, receptor binding density, age differences, sex differences, social behavior, juvenile development, reward, cortical regions, rat brain
- MeSH terms
- Animals, Autoradiography, Brain, Decision Making, Female, Male, Neural Pathways, Sex Characteristics, Social Behavior, Rats, Wistar, Receptors, Vasopressin, Receptors, Oxytocin, Rats, Spatial Memory
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
