The neuroanatomical distribution of oxytocin receptor binding and mRNA in the male rhesus macaque (Macaca mulatta)
Open accessAbstract
The rhesus macaque (Macaca mulatta) is an important primate model for social cognition, and recent studies have begun to explore the impact of oxytocin on social cognition and behavior. Macaques have great potential for elucidating the neural mechanisms by which oxytocin modulates social cognition, which has implications for oxytocin-based pharmacotherapies for psychiatric disorders such as autism and schizophrenia. Previous attempts to localize oxytocin receptors (OXTR) in the rhesus macaque brain have failed due to reduced selectivity of radioligands, which in primates bind to both OXTR and the structurally similar vasopressin 1a receptor (AVPR1A). We have developed a pharmacologically-informed competitive binding autoradiography protocol that selectively reveals OXTR and AVPR1A binding sites in primate brain sections. Using this protocol, we describe the neuroanatomical distribution of OXTR in the macaque. Finally, we use in situ hybridization to localize OXTR mRNA. Our results demonstrate that OXTR expression in the macaque brain is much more restricted than AVPR1A. OXTR is largely limited to the nucleus basalis of Meynert, pedunculopontine tegmental nucleus, the superficial gray layer of the superior colliculus, the trapezoid body, and the ventromedial hypothalamus. These regions are involved in a variety of functions relevant to social cognition, including modulating visual attention, processing auditory and multimodal sensory stimuli, and controlling orienting responses to visual stimuli. These results provide insights into the neural mechanisms by which oxytocin modulates social cognition and behavior in this species, which, like humans, uses vision and audition as the primary modalities for social communication.
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OT receptors are concentrated in cholinergic brain regions regulating visual and auditory attention in nonhuman primates.
“OT receptors are concentrated in cholinergic brain regions regulating visual and auditory attention in nonhuman primates (6, 42, 43)”
From Statistical and Methodological Considerations for the Interpretation of Intranasal Oxytocin Studies (2016) · cites this paper as [42]
The Discussion section on the nucleus basalis of Meynert and pedunculopontine tegmental nucleus reports OXTR expression in cholinergic regions linked to visual attention in rhesus macaques. The trapezoid-body section detects OXTR in an auditory relay, but calls its proposed auditory role speculative; it does not establish that receptors are concentrated in cholinergic regions regulating auditory attention. (LLM, conf=0.87)
Experimental — accuracy not yet measuredIn humans, visual processing of social cues is facilitated by intranasal oxytocin through increased attention to and recognition of emotional cues in faces.
“Similarly, in humans, visual processing of social cues is facilitated by IN-OT through increased attention to and recognition of emotional cues in faces [98,99].”
From The Neurobiology of Love and Pair Bonding from Human and Animal Perspectives (2023) · cites this paper as [99]
The optimized and reliable method for measuring OXTR and AVPR1a has been previously validated in nonhuman primate and human brain tissue to selectively reveal OXTR or AVPR1a.
“we measured both OXTR and AVPR1a with an optimized and reliable method previously validated in nonhuman primate and human brain tissue34,37,38.”
From Effect of age and autism spectrum disorder on oxytocin receptor density in the human basal forebrain and midbrain (2018) · cites this paper as [37]
The OXTR radioligand 125I-OVTA and the AVPR1a radioligand 125I-LVA bind to both receptor types when used in primate brain.
“These radioligands are now known to bind to both receptor types when they are used in primate brain37.”
From Effect of age and autism spectrum disorder on oxytocin receptor density in the human basal forebrain and midbrain (2018) · cites this paper as [37]
125I-OVTA and 125I-LVA bind selectively in rodents but have relatively high affinities for both oxytocin receptors and vasopressin receptor 1a in primates.
“Although these compounds bind selectively to their respective receptors in rodents, they have now been shown to exhibit relatively high affinities for both OXTR and AVPR1a in primates (27,28).”
From Comparative Perspectives on Oxytocin and Vasopressin Receptor Research in Rodents and Primates: Translational Implications (2016) · cites this paper as [27]
Using this method, the authors mapped oxytocin receptors in the rhesus macaque brain.
“With this method, which combines the use of the radioligands mentioned above with selective competitor ligands, we have now successfully mapped OXTR in the brain of the most common NHP model organism used in biomedical research: the rhesus macaque (Macaca mulatta) (27).”
From Comparative Perspectives on Oxytocin and Vasopressin Receptor Research in Rodents and Primates: Translational Implications (2016) · cites this paper as [27]
The authors designed a pharmacologically optimised competitive binding receptor autoradiography method that can selectively and reliably reveal oxytocin receptor and vasopressin receptor 1a distributions in primate tissue.
“We have recently reported the design of a pharmacologically optimised method for competitive binding receptor autoradiography that can selectively and reliably reveal the distributions of OXTR and AVPR1a in primate tissue (27).”
From Comparative Perspectives on Oxytocin and Vasopressin Receptor Research in Rodents and Primates: Translational Implications (2016) · cites this paper as [27]
The rhesus macaque brain exhibits extremely sparse oxytocin receptor expression relative to vasopressin receptor 1a, with the densest oxytocin receptor binding in the nucleus basalis of Meynert and superficial grey layer of the superior colliculus.
“The rhesus macaque brain in general exhibits extremely sparse OXTR expression relative to AVPR1a (27,31), with the most dense OXTR binding seen in the NBM and superficial grey layer of the SC (Fig. 2c,f).”
From Comparative Perspectives on Oxytocin and Vasopressin Receptor Research in Rodents and Primates: Translational Implications (2016) · cites this paper as [27]
ALS-II-69 blocks binding of OXTR radioligands to primate brain tissue.
“ALS-II-69 was evaluated in previous studies and shown to effectively block OXTR radioligand binding to primate brain tissue (27).”
From Comparative Perspectives on Oxytocin and Vasopressin Receptor Research in Rodents and Primates: Translational Implications (2016) · cites this paper as [27]
The macaque amygdala does not contain detectable levels of oxytocin receptor binding.
“However, we now know that this region of the macaque brain does not contain detectable levels of OXTR binding (27), although OXTR may be present on NBM terminals in the amygdala.”
From Comparative Perspectives on Oxytocin and Vasopressin Receptor Research in Rodents and Primates: Translational Implications (2016) · cites this paper as [27]
OXTR is distributed throughout the brain of many vertebrates, and its distribution pattern differs between species.
“OXTR is distributed throughout the brain of many vertebrates and, importantly, the pattern of OXTR distribution is diverse between species (32, 33).”
From Variation in the Oxytocin Receptor Gene Predicts Brain Region–Specific Expression and Social Attachment (2016) · cites this paper as [33]
In primates, oxytocin receptors have been detected in the superior colliculus, the pulvinar, and the primary visual cortex.
“In primates, OTR has been detected in the superior colliculus, the pulvinar, and the primary visual cortex (Freeman et al. 2014).”
From A precision medicine approach to oxytocin trials (2017) · cites this paper as Freeman et al. 2014
There is a high density of OT receptors in the amygdala.
“There is a high density of OT receptors in the amygdala (Insel and Shapiro, 1992; but see Freeman et al., 2014).”
From Low dose intranasal oxytocin delivered with Breath Powered device dampens amygdala response to emotional stimuli: A peripheral effect-controlled within-subjects randomized dose-response fMRI trial (2016) · cites this paper as Freeman et al., 2014
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“More recently, IN-OT administration in rhesus macaques has been shown to increase central OT concentrations (Chang et al., 2012) (Modi et al., 2014) and to affect a variety of social behaviors including increasing gaze to the eye region of monkey faces (Ebitz et al., 2013), increasing both selfish…”
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“A similar diversity in OXTR expression in found in rodents, as voles, mice, and rats each have unique distributions of OXTR binding (Burbach et al., 2006; Olazábal and Young, 2006).”
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“Behavioral studies in NHPs suggest that OT modulates social behaviors related to affiliation, sexual behavior, and pair bonding (Smith et al., 2010; Snowdon et al., 2010).”
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“Genetic studies also suggest that the OT receptor (OXTR) plays some role in face and emotion recognition and pair bonding behaviors in humans (Skuse et al., 2013; Walum et al., 2012).”
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“In humans, IN-OT affects the reaction to infant cries (Bakermans-Kranenburg et al., 2012) and infant laughter (Riem et al., 2012) and may even play a role in navigating the ‘‘cocktail party effect’’ (Tops et al., 2011), which is the phenomenon whereby an individual can focus one’s auditory…”
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“We also detected modest OXTR mRNA in the PPT, which is another highly interconnected region of the brain that has been implicated in a variety of functions, including sleep, locomotion, reaction time, reinforcement learning, sensation, attention, and consciousness (Winn, 2006).”
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“, 2012), and some of the behavioral effects of OT are mediated by AVPR1A (Schorscher-Petcu et al., 2010; Song et al., 2013).”
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“Insights into the neural mechanisms of OT action in humans have been gained using brain imaging (Zink and Meyer-Lindenberg, 2012), but inferences on precise mechanisms of action based on these techniques are limited compared to studies using animal models.”
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“…vector gene manipulations, and transgenic mouse technology have led to the elucidation of the neural mechanisms underlying the effects of these neuropeptides and their receptors on these complex social behaviors (Dölen et al., 2013; Ferguson et al., 2001; Lim et al., 2004b; Owen et al., 2013).”
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“OXTR binding has been found in VMH in mice, rats, guinea pigs, prairie and montane voles, two species of Central America singing mice, and two species of the South American rodent the tuco-tuco (Beery et al., 2008).”
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“In rats, OXTR in the VMH regulate female sexual receptivity in an estrogen (E2) dependent manner (Bale et al., 2001; McCarthy et al., 1994).”
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“Our results with (125)I-LVA fully match the previously reported distribution of AVPR1A binding in the rhesus macaque (Young et al., 1999).”
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“Behavioral studies in NHPs suggest that OT modulates social behaviors related to affiliation, sexual behavior, and pair bonding (Smith et al., 2010; Snowdon et al., 2010).”
BackgroundOxytocin blunts social vigilance in the rhesus macaque
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“, 2012), and changing social visual attentional bias (Ebitz et al., 2013; Parr et al., 2013).”
BackgroundInfluentialAerosolized oxytocin increases cerebrospinal fluid oxytocin in rhesus macaques
Modi, M. E., Connor-Stroud, F., Landgraf, R., Young, L. J., & Parr, L. A. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.02.011 · Cited by 129 · cited 1× · see citing works
“More recently, IN-OT administration in rhesus macaques has been shown to increase central OT concentrations (Chang et al., 2012) (Modi et al., 2014) and to affect a variety of social behaviors including increasing gaze to the eye region of monkey faces (Ebitz et al., 2013), increasing both selfish…”
BackgroundBakermans‐Kranenburg, M. J., van IJzendoorn, M. H., Riem, M. M. E., Mattie Tops, A., & Alink, L. R. A. (2011) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsr067 · Cited by 126 · see citing works
Intranasal oxytocin selectively attenuates rhesus monkeys’ attention to negative facial expressions
Parr, L. A., Modi, M., Siebert, E., & Young, L. J. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.02.011 · Cited by 124 · see citing works
LENG, G., ONAKA, T., CAQUINEAU, C., SABATIER, N., TOBIN, V, & TAKAYANAGI, Y. (2008) · Progress in brain research · doi:10.1016/s0079-6123(08)00413-5 · Cited by 112 · cited 1× · see citing works
“There is also evidence that OXTR in the VMH also play a role in the motivational switching between sexual behavior and feeding in rodents (Leng et al., 2008) and thus may have a role in regulating food intake and appetite in primates as well.”
BackgroundSchorscher-Petcu, A., Dupré, A., & Tribollet, E. (2009) · Neuroscience Letters · doi:10.1016/j.neulet.2009.06.016 · Cited by 111 · cited 6× · see citing works
“There were only two areas of consistent OXTR binding across all four primate species: NBM and SC (Loup et al., 1991; Schorscher-Petcu et al., 2009; S.M. Freeman et al., unpublished observations).”
BackgroundInfluentialGruber, C. W., Muttenthaler, M., & Freissmuth, M. (2010) · Current Pharmaceutical Design · doi:10.2174/138161210793292474 · Cited by 107 · cited 2× · see citing works
“It should be noted that the small molecule competitors did not eliminate the areas of high density specific binding at the concentrations used, which is likely due to the fact that the small, nonpeptide competitors can act as allosteric modulators to affect the affinity of the orthosteric ligand (in our case, the pept…”
BackgroundKobayashi, Y., Inoue, Y., Yamamoto, M., Isa, T., & Aizawa, H. (2002) · Journal of Neurophysiology · doi:10.1152/jn.2002.88.2.715 · Cited by 104 · cited 2× · see citing works
“The cholinergic subdivision, where we see OXTR expression, is the major source of cholinergic input to the midbrain and one of the major ascending arousal pathways in the brainstem (Kobayashi et al., 2002).”
BackgroundThe primate superior colliculus and the shift of visual attention.
Wurtz, R. H., & Goldberg, M. E. (1972) · PubMed · Cited by 96 · see citing works
Oxytocin-induced excitation of neurones in the rat central and medial amygdaloid nuclei
Terenzi, M. G., & Ingram, C. D. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.04.004 · Cited by 91 · cited 1× · see citing works
“Furthermore, previous studies have reported that the density of OXTR expression does not correlate with electrophysiological responses to OT, as brain regions with low OXTR binding often display greater responses to OT than those with dense binding (Terenzi and Ingram, 2005; Wilson et al., 2005).”
Background(1995) · PubMed · Cited by 90 · see citing works
Editorial comment: Oxytocin, vasopressin and social behavior
Young, L. J., & Flanagan-Cato, L. M. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.02.019 · Cited by 81 · cited 2× · see citing works
“There has been growing interest in the role of OT in human social cognition (Young and Flanagan-Cato, 2012).”
BackgroundEstradiol Increases Female Sexual Initiation Independent of Male Responsiveness in Rhesus Monkeys
Zehr, J. L., Dario Maestripieri, A., & Wallen, K. (1998) · Hormones and Behavior · doi:10.1006/hbeh.1998.1440 · Cited by 74 · cited 1× · see citing works
“In primates, female rhesus macaque sexual behavior is highest during the peak in E2 during estrous and increases after estrogen treatment in ovariectomized rhesus macaques (Zehr et al., 1998).”
BackgroundLocation of saccade-related neurons in the macaque superior colliculus
Ma, T. P., Graybiel, A. M., & Wurtz, R. H. (1991) · Experimental Brain Research · doi:10.1007/bf00229983 · Cited by 71 · cited 2× · see citing works
“6), and cholinergic input from the PPT strongly innervates the macaque superior colliculus (SC) (Ma et al., 1991).”
BackgroundOxytocin, vasopressin, and related peptides in the regulation of behavior
Choleris, E., Pfaff, D. W., & Kavaliers, M. (2013) · Cambridge University Press eBooks · doi:10.1017/cbo9781139017855.025 · Cited by 62 · see citing works
A Hormone-Activated Central Pattern Generator for Courtship
Wagenaar, D. A., Hamilton, M. S., Huang, T., Kristan, W. B., & French, K. A. (2010) · Current Biology · doi:10.1016/j.cub.2010.02.027 · Cited by 62 · see citing works
Oxytocin Receptor Gene Associated with the Efficiency of Social Auditory Processing
Mattie Tops, A., van IJzendoorn, M. H., Riem, M. M. E., Boksem, M. A. S., & Bakermans‐Kranenburg, M. J. (2011) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2011.00060 · Cited by 53 · cited 2× · see citing works
“…cries (Bakermans-Kranenburg et al., 2012) and infant laughter (Riem et al., 2012) and may even play a role in navigating the ‘‘cocktail party effect’’ (Tops et al., 2011), which is the phenomenon whereby an individual can focus one’s auditory attention on one particular stimulus and ‘‘tune out’’…”
BackgroundAre there oxytocin receptors in the primate brain?
TOLOCZKO, D. M., YOUNG, L., & INSEL, T. R. (1997) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1997.tb51953.x · Cited by 33 · cited 2× · see citing works
“2), which is consistent with what was previously reported for these radioligands in this species (Toloczko et al., 1997; Young et al., 1999).”
BackgroundResultInoue, K., Burkett, J. P., & Young, L. J. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.03.035 · Cited by 31 · cited 1× · see citing works
“Sections were allowed to thaw as described above, then hybridized with the probes and washed as described previously with minor modifications (Inoue et al., 2013).”
MethodInvestigation of an F-18 oxytocin receptor selective ligand via PET imaging
Smith, A. L., Freeman, S. M., Voll, R. J., Young, L. J., & Goodman, M. M. (2013) · Bioorganic & Medicinal Chemistry Letters · doi:10.1016/j.bmcl.2013.07.045 · Cited by 28 · cited 2× · see citing works
“…ligands that were developed specifically for use in human tissue for their ability to displace radioligand binding to hOXTR and hAVPR1A: a novel OXTR antagonist developed in our lab (ALS-II-69; Smith et al., 2013) and an AVPR1A antagonist developed by Sanofi Recherche (SR49059; Gal et al., 1993).”
BackgroundMethodOkada, K., & Kobayashi, Y. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.07009.x · Cited by 28 · see citing works
Facilitation of saccade initiation by brainstem cholinergic system
Kobayashi, Y., Saito, Y., & Isa, T. (2001) · Brain and Development · doi:10.1016/s0387-7604(01)00330-8 · Cited by 26 · cited 1× · see citing works
“Neurons in the PPT have also been shown to be active in monkeys during saccade tasks (Okada and Kobayashi, 2009) and to directly stimulate SC neurons and facilitate the initiation of saccadic eye movements (Kobayashi et al., 2001).”
BackgroundProperties of a new radioiodinated antagonist for human vasopressin V2 and V1a receptors
Ala, Y., Morin, D., Mahé, E., de la Cotte, N., Mouillac, B., Jard, S., Barberis, C., Tribollet, E., Dreifuss, J.-J., Sawyer, W. H., et al. (1997) · European Journal of Pharmacology · doi:10.1016/s0014-2999(97)01021-2 · Cited by 23 · cited 2× · see citing works
“For the AVPR1A competitor SR49059, whose use to selectively occupy AVPR1A in a competitive binding approach has been suggested previously (Ala et al., 1997), we determined that the best concentration for SR49059 to bind to displace 125I-OVTA from hAVPR1A without affecting binding to hOXTR is 10 nM…”
BackgroundOxytocin receptors in non-human primate brain visualized with monoclonal antibody
Boccia, M. L., Panicker, A. K., Pedersen, C., & Petrusz, P. (2001) · Neuroreport · doi:10.1097/00001756-200106130-00041 · Cited by 21 · cited 2× · see citing works
“Two publications have used immunohistochemistry (IHC) with an OXTR antibody to identify areas of OXTR expression in the macaque brain (Boccia et al., 2001) and in human brain tissue (Boccia et al., 2013).”
MethodOxytocin, vasopressin, and the evolution of mating systems in mammals
Freeman, S. M., & Young, L. J. (2013) · Cambridge University Press eBooks · doi:10.1017/cbo9781139017855.011 · Cited by 19 · cited 1× · see citing works
“Oxytocin (OT) and vasopressin (AVP) are structurally related peptides that modulate a range of complex social behaviors, including maternal behavior, aggression, territoriality, social recognition, and social bonding (Freeman and Young, 2013).”
BackgroundCloning and Expression of the Rhesus Monkey Oxytocin Receptor
Salvatore, C., Woyden, C. J., Guidotti, M. T., Pettibone, D. J., & Jacobson, M. A. (1998) · Journal of Receptors and Signal Transduction · doi:10.3109/10799899809039162 · Cited by 17 · cited 2× · see citing works
“(Salvatore et al., 1998; Young et al., 1999).”
BackgroundWilson, B. C., Terenzi, M. G., & Ingram, C. D. (2005) · Neuropeptides · doi:10.1016/j.npep.2005.04.001 · Cited by 13 · cited 1× · see citing works
“Furthermore, previous studies have reported that the density of OXTR expression does not correlate with electrophysiological responses to OT, as brain regions with low OXTR binding often display greater responses to OT than those with dense binding (Terenzi and Ingram, 2005; Wilson et al., 2005).”
Background
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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
The Social Salience Hypothesis of Oxytocin
Shamay-Tsoory, S. G., & Abu-Akel, A. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.07.020 · Cited by 904 · see citing works
Plasticity of Cortical Excitatory-Inhibitory Balance
Froemke, R. C. (2015) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-071714-034002 · Cited by 458 · see citing works
“Oxytocin may be an important modulator of nucleus basalis, as indicated by recent autoradiography and in situ hybridization data from macaques (Freeman et al. 2014).”
BackgroundOxytocin enhances social recognition by modulating cortical control of early olfactory processing
Oettl, L.-L., Ravi, N., Schneider, M., Scheller, M. F., Schneider, P., Mitre, M., da Silva Gouveia, M., Froemke, R. C., Chao, M. V., Young, W. S., et al. (2016) · Neuron · doi:10.1016/j.neuron.2016.03.033 · Cited by 359 · see citing works
“…and early cortical visual areas and cholinergic nuclei controlling sensory processing in these modalities, suggesting the involvement of OXT in a variety of functions relevant to social cognition, including modulating visual attention, processing, and sensory stimuli (Freeman et al., 2014a, 2014b).”
Environmental influence in the brain, human welfare and mental health
Tost, H., Champagne, F. A., & Meyer‐Lindenberg, A. (2015) · Nature Neuroscience · doi:10.1038/nn.4108 · Cited by 349 · see citing works
Statistical and Methodological Considerations for the Interpretation of Intranasal Oxytocin Studies
Walum, H., Waldman, I. D., & Young, L. J. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.06.016 · Cited by 345 · see citing works
“For example, OT receptors are concentrated in cholinergic brain regions regulating visual and auditory attention in nonhuman primates (6, 42, 43), consistent with the putative localization of OT receptors in human brain (44).”
BackgroundAssembling the puzzle: pathways of oxytocin signaling in the brain
Grinevich, V., Knobloch-Bollmann, H. S., Eliava, M., Busnelli, M., & Chini, B. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.04.013 · Cited by 309 · see citing works
“supports the hypothesis that, in primates, OTRs act at the most relevant sensory modalities to regulate social approach and behavior (29) (Figure 4).”
BackgroundJohnson, Z. V., & Young, L. J. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.01.034 · Cited by 242 · see citing works
“exhibit dense OTR expression in the NAc, while socially monogamous and alloparental coppery titi monkeys exhibit dense V1aR expression in this region (Freeman and Young, 2016); in contrast, non-monogamous rhesus macaques exhibit low levels of OTR and V1aR binding in the NAc (Figure 2) (Freeman et al., 2014; Young et a…”
Prefrontal–amygdala circuits in social decision-making
Gangopadhyay, P., Chawla, M., Monte, O. D., & Chang, S. W. C. (2020) · Nature Neuroscience · doi:10.1038/s41593-020-00738-9 · Cited by 247 · see citing works
Baribeau, D. A., & Anagnostou, E. A. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00335 · Cited by 229 · see citing works
“Oxytocin has a single receptor (OXTR) encoded on chromosome 3, whereas vasopressin has three types of receptors, AVPR1a and AVPR1b (also called V3) and V2, on chromosome 20 (De Keyzer et al., 1994; Thibonnier et al., 2002).”
BackgroundInfluentialGenetic origins of social networks in rhesus macaques
Brent, L. J. N., Heilbronner, S. R., Horvath, J. E., Gonzalez-Martinez, J., Ruiz-Lambides, A., Robinson, A. G., Skene, J. H. P., & Platt, M. L. (2013) · Scientific Reports · doi:10.1038/srep01042 · Cited by 220 · see citing works
Freeman, S. M., & Young, L. J. (2016) · Journal of Neuroendocrinology · doi:10.1111/jne.12382 · Cited by 196 · see citing works
“ALS-II-69 was evaluated in previous studies and shown to effectively block OXTR radioligand binding to primate brain tissue (27).”
BackgroundMethodInfluentialKing, L. B., Walum, H., Inoue, K., Eyrich, N. W., & Young, L. J. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.12.008 · Cited by 191 · see citing works
“The OXTR is distributed throughout the brain of many vertebrates, and the pattern of OXTR distribution is diverse among species (32,33).”
Young, L. J., & Barrett, C. E. (2015) · Science · doi:10.1126/science.aaa8120 · Cited by 200 · see citing works
Self-citationYamasue, H., Okada, T., Munesue, T., Kuroda, M., Fujioka, T., Uno, Y., Matsumoto, K., Kuwabara, H., Mori, D., Okamoto, Y., et al. (2020) · Molecular Psychiatry · doi:10.1038/s41380-018-0097-2 · Cited by 185 · see citing works
Hormonal influences in migraine — interactions of oestrogen, oxytocin and CGRP
Krause, D. N., Warfvinge, K., Haanes, K. A., & Edvinsson, L. I. (2021) · Nature Reviews Neurology · doi:10.1038/s41582-021-00544-2 · Cited by 207 · see citing works
Blevins, J. E., Graham, J. L., Morton, G. J., Bales, K. L., Schwartz, M. W., Baskin, D. G., & Havel, P. J. (2014) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00441.2014 · Cited by 187 · see citing works
“While systemic OT increases the induction of Fos (a marker of neuronal activation) in the VMH in mice (72) and OTRs are expressed in the VMH of rhesus monkeys (9, 24), it remains to be determined whether systemic OT is capable of reaching OTRs in the DMH or VMH in sufficient concentrations to stimulate EE in rhesus mo…”
Parker, K. J., Oztan, O., Libove, R. A., Mohsin, N., Karhson, D. S., Sumiyoshi, R. D., Summers, J. E., Hinman, K. E., Motonaga, K. S., Phillips, J. M., et al. (2019) · Science Translational Medicine · doi:10.1126/scitranslmed.aau7356 · Cited by 185 · see citing works
Klin, A., Shultz, S., & JONES, W. R. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.10.006 · Cited by 183 · see citing works
Neurobiological mechanisms of social attachment and pair bonding
Johnson, Z. V., & Young, L. J. (2015) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2015.01.009 · Cited by 169 · see citing works
Self-citationNeural mechanisms of social decision-making in the primate amygdala
Chang, S. W. C., Fagan, N. A., Toda, K., Utevsky, A. V., Pearson, J. M., & Platt, M. L. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1514761112 · Cited by 157 · see citing works
“Recently, it has been demonstrated that OT administration modulates hemodynamic activity in the amygdala in rhesus macaques (30), and it has been hypothesized that the primate amygdala may express presynaptic OT receptors (46).”
BackgroundFreeman, S. M., Walum, H., Inoue, K., Smith, A. L., Goodman, M. M., Bales, K. L., & Young, L. J. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.04.055 · Cited by 153 · see citing works
“In the rhesus macaque, OXTR distribution is even further restricted, with low levels of expression detectable in only five areas of the brain: NBM, ventromedial hypothalamus (VMH), SuG, trapezoid body (TB), and the pedunculopontine tegmental nucleus (PPT)(Freeman et al., in press).”
BackgroundMethodResultInfluentialOxytocin and the Neurobiology of Prosocial Behavior
Marsh, N., Marsh, A. A., Lee, M. R., & Hurlemann, R. (2020) · The Neuroscientist · doi:10.1177/1073858420960111 · Cited by 149 · see citing works
Oxytocin and Pain Perception: From Animal Models to Human Research
Boll, S., de Minas, A. C. A., Raftogianni, A., Herpertz, S. C., & Grinevich, V. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.09.041 · Cited by 137 · see citing works
Blevins, J. E., & Baskin, D. G. (2015) · Physiology & Behavior · doi:10.1016/j.physbeh.2015.05.023 · Cited by 132 · see citing works
“nucleus accumbens, preoptic area, VMH, DMV, and spinal cord) [73–75] and humans (e.”
BackgroundLabeled oxytocin administered via the intranasal route reaches the brain in rhesus macaques
Lee, M. R., Shnitko, T. A., Blue, S. W., Kaucher, A. V., Winchell, A. J., Erikson, D. W., Grant, K. A., & Leggio, L. (2020) · Nature Communications · doi:10.1038/s41467-020-15942-1 · Cited by 132 · see citing works
Aerosolized oxytocin increases cerebrospinal fluid oxytocin in rhesus macaques
Modi, M. E., Connor-Stroud, F., Landgraf, R., Young, L. J., & Parr, L. A. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.02.011 · Cited by 129 · see citing works
“Moreover, the neuroanatomical distribution of OTreceptors in rhesus macaques have recently been described, providing insights into the sites of OT action in the brain in this nonhuman primate (NHP) model organisms (Freeman et al., 2014).”
Oxytocin in the socioemotional brain: implications for psychiatric disorders
Kirsch, P. (2015) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2015.17.4/pkirsch · Cited by 122 · see citing works
Oxytocin and social functioning
Jones, C., Barrera, I., Brothers, S., Ring, R., & Wahlestedt, C. (2017) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2017.19.2/cjones · Cited by 132 · see citing works
Oxytocin receptors modulate a social salience neural network in male prairie voles
Johnson, Z. V., Walum, H., Xiao, Y., Riefkohl, P. C., & Young, L. J. (2017) · Hormones and Behavior · doi:10.1016/j.yhbeh.2016.10.009 · Cited by 113 · see citing works
Oxytocin reduces alcohol cue-reactivity in alcohol-dependent rats and humans
Hansson, A. C., Koopmann, A., Uhrig, S., Bühler, S., Domi, E., Kiessling, E., Ciccocioppo, R., Froemke, R. C., Grinevich, V., Kiefer, F., et al. (2018) · Neuropsychopharmacology · doi:10.1038/npp.2017.257 · Cited by 109 · see citing works
“However, some studies on non-human primates suggest significant binding to other nonapeptide receptors, most notably vasopressin 1a receptors (Toloczko et al, 1997; Freeman et al, 2014a, b).”
BackgroundMethodA Review of Oxytocin’s Effects on the Positive, Negative, and Cognitive Domains of Schizophrenia
Feifel, D., Shilling, P. D., & MacDonald, K. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.07.025 · Cited by 110 · see citing works
Social Decision-Making and the Brain: A Comparative Perspective
Tremblay, S., Sharika, K. M., & Platt, M. L. (2017) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2017.01.007 · Cited by 105 · see citing works
Quintana, D. S., Westlye, L. T., Alnæs, D., Rustan, Ø. G., Kaufmann, T., Smerud, K. T., Mahmoud, R. A., Djupesland, P. G., & Andreassen, O. A. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2016.04.010 · Cited by 102 · see citing works
Cataldo, I., Azhari, A., & Esposito, G. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2018.00027 · Cited by 95 · see citing works
“…et al., 2015; Wang et al., 2016), processing and recognition of facial expressions (Israel et al., 2008; Knafo et al., 2008; Moons et al., 2014; Uzefovsky et al., 2015; Wang et al., 2016) and non-human mammals (Murakami et al., 2011; Freeman et al., 2014; Paré et al., 2016; Lesse et al., 2017).”
BackgroundLin, Y.-T., & Hsu, K. (2018) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2018.10.003 · Cited by 97 · see citing works
The role of oxytocin in regulation of appetitive behaviour, body weight and glucose homeostasis
Lawson, E. A., Olszewski, P. K., Weller, A., & Blevins, J. E. (2019) · Journal of Neuroendocrinology · doi:10.1111/jne.12805 · Cited by 97 · see citing works
Freeman, S. M., Palumbo, M. C., Lawrence, R. H., Smith, A. L., Goodman, M. M., & Bales, K. L. (2018) · Translational Psychiatry · doi:10.1038/s41398-018-0315-3 · Cited by 82 · see citing works
Leng, G., & Sabatier, N. (2017) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2017.02.007 · Cited by 89 · see citing works
Adaptations for social cognition in the primate brain
Platt, M. L., Seyfarth, R. M., & Cheney, D. L. (2016) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2015.0096 · Cited by 87 · see citing works
“Recent studies have demonstrated that OT receptors in both monogamous titi monkeys (Callicebus cupreus) and rhesus macaques [127,128] appear to be limited to areas of the hypothalamus and brainstem implicated in arousal and visual orienting behaviour.”
BackgroundOxytocin receptor dynamics in the brain across development and species
Vaidyanathan, R., & Hammock, E. A. D. (2016) · Developmental Neurobiology · doi:10.1002/dneu.22403 · Cited by 82 · see citing works
“…well demonstrated within the brain (Insel et al., 1991; Dubois-Dauphin et al., 1992; Insel and Shapiro, 1992; Insel et al., 1993; Young et al., 1996; Wang and Young, 1997; Rabhi et al., 1999; Olazabal and Young, 2006; Beery et al., 2008; Campbell et al., 2009; Freeman et al., 2014a, 2014b).”
BackgroundKrol, K. M., Puglia, M. H., Morris, J. P., Connelly, J. J., & Grossmann, T. (2019) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2019.100648 · Cited by 86 · see citing works
“Limited work in the non-human primate brain reports the majority of OXTR in subcortical regions (Freeman et al., 2014a, b; Freeman and Young, 2016).”
Bürkner, P., Williams, D. R., Simmons, T. C., & Woolley, J. D. (2017) · Schizophrenia Bulletin · doi:10.1093/schbul/sbx053 · Cited by 80 · see citing works
Uhrig, S., Hirth, N., Broccoli, L., von Wilmsdorff, M., Bauer, M., Sommer, C., Zink, M., Steiner, J. H., Frodl, T., Malchow, B., et al. (2016) · Schizophrenia Research · doi:10.1016/j.schres.2016.04.019 · Cited by 75 · see citing works
Advances in nonhuman primate models of autism: Integrating neuroscience and behavior
Bauman, M. D., & Schumann, C. M. (2017) · Experimental Neurology · doi:10.1016/j.expneurol.2017.07.021 · Cited by 71 · see citing works
Arginine Vasopressin Is a Blood-Based Biomarker of Social Functioning in Children with Autism
Carson, D. S., Garner, J. P., Hyde, S. A., Libove, R. A., Berquist, S. W., Hornbeak, K. B., Jackson, L. P., Sumiyoshi, R. D., Howerton, C. L., Hannah, S. L., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0132224 · Cited by 71 · see citing works
Oxytocin and Serotonin Brain Mechanisms in the Nonhuman Primate
Lefèvre, A., Richard, N., Jazayeri, M., Beuriat, P.-A., Fieux, S., Zimmer, L., Duhamel, J., & Angela Sirigu, B. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.0659-17.2017 · Cited by 71 · see citing works
“…in the primate brain is not well understood; and although they have not been found in limbic areas of humans and macaques (Loup et al., 1991; Freeman et al., 2014; but see Boccia et al., 2013), administration of OT has consistently produced effects in these areas (Chang et al., 2015;…”
BackgroundTabak, B. A., Meyer, M. L., Castle, E., Dutcher, J. M., Irwin, M. R., Han, J. H., Lieberman, M. D., & Eisenberger, N. I. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.10.006 · Cited by 67 · see citing works
Neuropeptide diversity and the regulation of social behavior in New World primates
French, J. A., Taylor, J. H., Mustoe, A. C., & Cavanaugh, J. (2016) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2016.03.004 · Cited by 66 · see citing works
“…968in the visual processing areas in primates is consistent with the 969importance and predominance of visual stimuli in primate social 970relationships, akin to the central role of olfaction, and the rich 971expression of OTR in odor-processing networks, in rodents 972(Freeman et al., 2014b).”
InfluentialOxytocin modulates fMRI responses to facial expression in macaques
Liu, N., Hadj-Bouziane, F., Jones, K. B., Turchi, J. N., Averbeck, B. B., & Ungerleider, L. G. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1508097112 · Cited by 65 · see citing works
“In the rhesus monkey brain, OT receptors are most robustly expressed in the nucleus basalis of Meynert, the superficial gray layer of the superior colliculus, the pedunculopontine tegmental nucleus, the trapezoid body, and the ventromedial hypothalamus (37).”
BackgroundPharmacological Treatment of Generalised Anxiety Disorder: Current Practice and Future Directions
Fagan, H. A., & Baldwin, D. S. (2023) · Expert Review of Neurotherapeutics · doi:10.1080/14737175.2023.2211767 · Cited by 68 · see citing works
“widely throughout the mammalian brain [120].”
Jiang, Y., & Platt, M. L. (2018) · Scientific Reports · doi:10.1038/s41598-018-25607-1 · Cited by 66 · see citing works
Oxytocin, social cognition and psychiatry
Young, L. J. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2014.186 · Cited by 64 · see citing works
Self-citationTargeting the Oxytocin System: New Pharmacotherapeutic Approaches
Gulliver, D. W., Werry, E. L., Reekie, T. A., Katte, T. A., Jorgensen, W. T., & Kassiou, M. (2018) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2018.11.001 · Cited by 63 · see citing works
“…direct approach to modulate oxytocinergic signaling is through activation of the OT receptor (OXTR), a class-A G-protein-coupled receptor (GPCR) expressed throughout the central nervous system (CNS) and in several peripheral tissues, including the uterus, mammary glands, heart, and kidney [16,17].”
Adaptive coding of the value of social cues with oxytocin, an fMRI study in autism spectrum disorder
Andari, E., Richard, N., Leboyer, M., & Sirigu, A. (2016) · Cortex · doi:10.1016/j.cortex.2015.12.010 · Cited by 62 · see citing works
Titi Monkeys as a Novel Non-Human Primate Model for the Neurobiology of Pair Bonding .
Bales, K. L., Razo, R. A., Conklin, Q. A., Hartman, S., Mayer, H. S., Rogers, F. D., Simmons, T. C., Smith, L. K., Williams, A. V., Williams, D. R., et al. (2017) · Europe PMC (PubMed Central) · Cited by 62 · see citing works
The Role of Hypothalamic Neuropeptides in Neurogenesis and Neuritogenesis
Bakoš, J., Zatkova, M., Bačová, Z., & Ostatníková, D. (2016) · Neural Plasticity · doi:10.1155/2016/3276383 · Cited by 61 · see citing works
“Neural circuitry for social cognition depends on oxytocin and vasopressin receptor density in specific brain regions [119, 120].”
BackgroundThe Neurobiology of Love and Pair Bonding from Human and Animal Perspectives
Blumenthal, S. A., & Young, L. J. (2023) · Biology · doi:10.3390/biology12060844 · Cited by 59 · see citing works
“Similarly, in humans, visual processing of social cues is facilitated by IN-OT through increased attention to and recognition of emotional cues in faces [98,99].”
BackgroundModulation of social behavior by distinct vasopressin sources
Rigney, N., Vries, G. J. D., & Petrulis, A. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1127792 · Cited by 61 · see citing works
Ebert, A., & Brüne, M. (2017) · Current topics in behavioral neurosciences · doi:10.1007/7854_2017_21 · Cited by 62 · see citing works
Marmosets as model species in neuroscience and evolutionary anthropology
Burkart, J. M., & Finkenwirth, C. (2014) · Neuroscience Research · doi:10.1016/j.neures.2014.09.003 · Cited by 60 · see citing works
Translating Oxytocin Neuroscience to the Clinic: A National Institute of Mental Health Perspective
Insel, T. R. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.02.002 · Cited by 56 · see citing works
Putnam, P. T., Roman, J. M., Zimmerman, P. E., & Gothard, K. M. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2016.05.016 · Cited by 53 · see citing works
“including the nucleus basalis of Meynert (NBM) (Freeman et al., 2014).”
Circuits for social learning: a unified model and application to autism spectrum disorder
DeMayo, M. M., Young, L. J., Hickie, I. B., Song, Y. J. C., & Guastella, A. J. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.09.034 · Cited by 52 · see citing works
Duque‐Wilckens, N., Steinman, M. Q., Laredo, S. A., Hao, R., Perkeybile, A. M., Bales, K. L., & Trainor, B. C. (2016) · Neuropharmacology · doi:10.1016/j.neuropharm.2016.07.018 · Cited by 52 · see citing works
“…in V1aR binding (Bester-Meredith et al., 1999; Hammock and Young, 2006), dense V1aR binding in the bed nucleus of the stria terminalis (BNST) is observed in a diverse group of rodents (Bales et al., 2007; Bosch et al., 2010) and primates (Freeman et al., 2014a, 2014b; Young et al., 1999).”
Selective localization of oxytocin receptors and vasopressin 1a receptors in the human brainstem
Freeman, S. M., Smith, A. L., Goodman, M. M., & Bales, K. L. (2017) · Social Neuroscience · doi:10.1080/17470919.2016.1156570 · Cited by 51 · see citing works
“The slides were processed for OXTR receptor autoradiography as described previously (Freeman et al., 2014a).”
BackgroundMethodResultInfluentialDevelopmental effects of oxytocin neurons on social affiliation and processing of social information
Nunes, A. R., Gliksberg, M., Varela, S. A. M., Teles, M., Wircer, E., Blechman, J., Petri, G., Levkowitz, G., & Oliveira, R. F. (2021) · The Journal of Neuroscience · doi:10.1523/jneurosci.2939-20.2021 · Cited by 47 · see citing works
Association between the oxytocin receptor ( OXTR ) gene and children's social cognition at 18 months
Wade, M., Hoffmann, T. J., Wigg, K., & Jenkins, J. M. (2014) · Genes Brain & Behavior · doi:10.1111/gbb.12148 · Cited by 47 · see citing works
“Interestingly, OXTR has been found in non-human species to be distributed in several brain regions known to support social cognition (Freeman et al. 2014; Vaccari et al. 1998).”
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
“In primates, OXTRs are more densely expressed in areas responsible for visual information processing and attention, including the nucleus basalis of Meynert and superior colliculus (S. M. Freeman et al., 2014; S. M. Freeman & Young, 2016; Grebe et al., 2021).”
BackgroundSelf-citationKranz, T. M., Kopp, M., Waltes, R., Sachse, M., Duketis, E., Jarczok, T. A., Degenhardt, F., Görgen, K., Meyer, J., Freitag, C. M., et al. (2016) · Autism Research · doi:10.1002/aur.1597 · Cited by 46 · see citing works
“…processing social cues like the olfactory bulb and the medial amygdala, rhesus macaques show the highest OXTR levels in cholinergic brain regions such as the nucleus basalis of Meynert (NBM), which sends massive projections to the limbic brain system and the neocortex [Freeman et al., 2014].”
BackgroundNeuropeptide Regulation of Social Attachment: The Prairie Vole Model
Tabbaa, M., Paedae, B., Liu, Y., & Wang, Z. (2016) · Comprehensive physiology · doi:10.1002/cphy.c150055 · Cited by 53 · see citing works
Intranasal gene delivery for treating Parkinson’s disease: overcoming the blood–brain barrier
Aly, A. E.-E., & Waszczak, B. L. (2015) · Expert Opinion on Drug Delivery · doi:10.1517/17425247.2015.1069815 · Cited by 45 · see citing works
“Oxytocin receptor expression is very restricted in the brain, with most expression in areas related to visual processing, sensory functions and social cognition [59].”
BackgroundLee, M. R., Sheskier, M. B., Farokhnia, M., Feng, N., Marenco, S., Lipska, B. K., & Leggio, L. (2018) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2018.05.039 · Cited by 44 · see citing works
Oxytocin and Anxiety Disorders: Translational and Therapeutic Aspects
Naja, W., & Aoun, M. P. (2017) · Current Psychiatry Reports · doi:10.1007/s11920-017-0819-1 · Cited by 40 · see citing works
Positive reinforcing effect of oxytocin microinjection in the rat central nucleus of amygdala
László, K., Kovács, A., Zagorácz, O., Ollmann, T., Péczely, L., Kertes, E., Lacy, D. G., & Lénárd, L. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.09.021 · Cited by 43 · see citing works
An integrated framework for the role of oxytocin in multistage social decision‐making
Piva, M., & Chang, S. W. C. (2018) · American Journal of Primatology · doi:10.1002/ajp.22735 · Cited by 38 · see citing works
“While previous studies were unable to differentiate between OXTRs and vasopressin 1a receptors (AVPR1As), the authors of this study utilized a competitive binding autoradiography protocol that allowed them to specifically localize OXTRs (Freeman et al., 2014).”
BackgroundMethodResultInfluentialA precision medicine approach to oxytocin trials
Andari, E., Hurlemann, R., & Young, L. J. (2017) · Current Topics in Behavioral Neurosciences · doi:10.1007/7854_2017_29 · Cited by 40 · see citing works
“They are also found in regions involved in attention such as the basal nucleus of Meynert and the diagonal band of Broca that have a high number of cholinergic neurons (Freeman et al. 2014).”
BackgroundSelf-citationThe impact of sex as a biological variable in the search for novel antidepressants
Williams, A. V., & Trainor, B. C. (2018) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2018.05.003 · Cited by 40 · see citing works
Tops, S., Habel, U., & Radke, S. (2018) · Hormones and Behavior · doi:10.1016/j.yhbeh.2018.03.002 · Cited by 39 · see citing works
Prounis, G. S., Thomas, K., & Ophir, A. G. (2018) · The Journal of Comparative Neurology · doi:10.1002/cne.24450 · Cited by 36 · see citing works
“…OTR and V1aR expression in adult rhesus macaques, common marmosets, and copper titi monkeys, and these studies indicate intriguing species differences (Freeman, Inoue, Smith, Goodman, & Young, 2014a; Freeman et al., 2014b; Schorscher-Petcu, Dupre, & Tribollet, 2009; Young, Toloczko, & Insel, 1999).”
BackgroundMarmosets treated with oxytocin are more socially attractive to their long-term mate
Cavanaugh, J., Huffman, M. C., Harnisch, A. M., & French, J. A. (2015) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2015.00251 · Cited by 36 · see citing works
“The OXTA (L368,899r provided by Dr. Peter Williams, Merck and Co., Inc.) is readily absorbed by the bloodstream after passage through the digestive system (Thompson et al., 1997), penetrates the CNS after peripheral administration, and accumulates in areas of the limbic system (Boccia et al., 2007).”
BackgroundSimpson, E. A., Paukner, A., Sclafani, V., Kaburu, S., Suomi, S. J., & Ferrari, P. F. (2016) · Psychopharmacology · doi:10.1007/s00213-016-4480-x · Cited by 36 · see citing works
“More recently, researchers have described the neuroanatomical distribution of OT receptors binding and mRNA in rhesus macaques (Freeman et al. 2014).”
BackgroundIntrinsic links among sex, emotion, and reproduction
Yang, L. Y., Comninos, A. N., & Dhillo, W. S. (2018) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-018-2802-3 · Cited by 36 · see citing works
“This method of detecting oxytocin and vasopressin binding in humans and non-human primates has since been disputed due to the relative non-specificity and high cross-reactivity of radiolabelled ligands for the oxytocin and vasopressin receptor [128, 129].”
MethodOxytocin increases eye-gaze towards novel social and non-social stimuli
Eckstein, M., Bamert, V., Stephens, S. B. Z., Wallen, K., Young, L. J., Ehlert, U., & Ditzen, B. (2018) · Social Neuroscience · doi:10.1080/17470919.2018.1542341 · Cited by 36 · see citing works
Autism Pathogenesis: The Superior Colliculus
Jure, R. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.01029 · Cited by 34 · see citing works
Kotani, M., Shimono, K., Yoneyama, T., Nakako, T., Matsumoto, K., Ogi, Y., Konoike, N., Nakamura, K., & Ikeda, K. (2017) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2017.05.009 · Cited by 34 · see citing works
Lee, M. R., Schwandt, M. L., Sankar, V., Suchankova, P., Sun, H., & Leggio, L. (2017) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2017.07.481 · Cited by 33 · see citing works
Oxytocin and Facial Emotion Recognition
Ellenbogen, M. A. (2017) · Current topics in behavioral neurosciences · doi:10.1007/7854_2017_20 · Cited by 33 · see citing works
Johnson, K. V. ‐., & Burnet, P. W. J. (2020) · BMC Neuroscience · doi:10.1186/s12868-020-00583-3 · Cited by 31 · see citing works
Rogers Flattery, C. N., Coppeto, D. J., Inoue, K., Rilling, J. K., Preuss, T. M., & Young, L. J. (2022) · Brain Structure and Function · doi:10.1007/s00429-021-02369-7 · Cited by 31 · see citing works
Oxytocin, vasopressin and social behavior in the age of genome editing: a comparative perspective
Boender, A. J., & Young, L. J. (2020) · Hormones and Behavior · doi:10.1016/j.yhbeh.2020.104780 · Cited by 30 · see citing works
Oxytocin Fails to Recruit Serotonergic Neurotransmission in the Autistic Brain
Lefèvre, A., Mottolese, R., Redouté, J., Costes, N., Bars, D. L., Geoffray, M., Leboyer, M., & Angela Sirigu, B. (2017) · Cerebral Cortex · doi:10.1093/cercor/bhx272 · Cited by 30 · see citing works
García-Boll, E., Martı́nez-Lorenzana, G., Condés‐Lara, M., & González‐Hernández, A. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.11.031 · Cited by 30 · see citing works
“Similar results were obtained in other Primates (Macaca mulatta, Freeman et al., 2014a; Callicebus cupreus, Freeman et al., 2014b).”
ResultBridging the gap between rodents and humans: The role of non‐human primates in oxytocin research
Putnam, P. T., Young, L. J., & Gothard, K. M. (2018) · American Journal of Primatology · doi:10.1002/ajp.22756 · Cited by 28 · see citing works
Smith, A. L., Freeman, S. M., Barnhart, T. E., Abbott, D. H., Ahlers, E. O., Kukis, D. L., Bales, K. L., Goodman, M. M., & Young, L. J. (2016) · Bioorganic & Medicinal Chemistry Letters · doi:10.1016/j.bmcl.2016.04.097 · Cited by 29 · see citing works
Oxytocin as an Anti-obesity Treatment
Niu, J., Tong, J., & Blevins, J. E. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.743546 · Cited by 30 · see citing works
Synaptic plasticity as a cortical coding scheme
Froemke, R. C., & Schreiner, C. E. (2015) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2015.10.003 · Cited by 29 · see citing works
“These systems are also extensively interrelated: in macaques, the cholinergic nucleus basalis expresses a high level of oxytocin receptors [85 ], and a major input to the oxytocin-producing paraventricular nucleus comes from noradrenergic neurons of the brainstem [86].”
BackgroundWade, M., Hoffmann, T. J., & Jenkins, J. M. (2015) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsv064 · Cited by 26 · see citing works
“Studies in non-human primates show that OXTR is selectively distributed in various brain regions known to support social cognition (Freeman et al., 2014).”
BackgroundBAXTER, A. B., Anderson, M., Seelke, A. M. H., Kinnally, E. L., Freeman, S. M., & Bales, K. L. (2020) · Scientific Reports · doi:10.1038/s41598-020-74243-1 · Cited by 26 · see citing works
Maninger, N., Hinde, K., Mendoza, S. P., Mason, W. A., Larke, R. H., Ragen, B., Jarcho, M. R., Cherry, S. R., Rowland, D. J., Ferrer, E. E., et al. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.02.028 · Cited by 27 · see citing works
“In contrast to the more common biomedical model, the rhesus monkey (Macaca mulatta) (Freeman et al., 2014a), titi monkeys display OT receptors in more forebrain areas, including the lateral septum (Freeman et al., 2014b).”
- Authors
- Freeman, S. M., Inoue, K., Smith, A. L., Goodman, M. M., & Young, L. J.
- Affiliations
- Emory University (US)
- Corresponding author
- Freeman, Sara M.
- Venue
- Psychoneuroendocrinology
- Publisher
- Elsevier BV
- Published
- 2014-07
- Volume
- 45
- Pages
- 128-141
- ISSN
- 0306-4530 (ISSN-L)
- PMC
- PMC4043226
- OpenAlex
- W1989923863
- Cited by
- 185
- References
- 73
- Citations by year
- 2026: 2 · 2025: 4 · 2024: 4 · 2023: 7 · 2022: 13 · 2021: 17 · 2020: 9 · 2019: 12 · 2018: 28 · 2017: 26 · 2016: 29 · 2015: 23 · 2014: 10 · 2013: 1
- FWCI
- 43.40
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Psychoneuroendocrinology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (5t32mh073525-05, P51OD011107, P51OD011132)
- National Institute of Mental Health (T32-MH073525, R21MH090776, T32MH073525-06, P50MH100023, MH090776)
- National Center for Research Resources (P51RR000165)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
- Keywords
- oxytocin receptor, vasopressin 1a receptor, AVPR1A, rhesus monkeys, neuroanatomical distribution, nucleus basalis of Meynert, pedunculopontine nucleus, superior colliculus, trapezoid body, ventromedial hypothalamus, social cognition, visual attention, auditory processing, orienting response, autism spectrum disorder, schizophrenia
- MeSH terms
- Animals, Brain, Cricetulus, Cricetinae, Humans, Macaca mulatta, Male, Neurons, Oxytocin, Protein Binding, RNA, Messenger, Tissue Distribution, CHO Cells, Receptors, Oxytocin
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