442, 105–118. : +52 449 910 7400/Ext. Baribeau, D. A., and Anagnostou, E. (2014). Proc. doi: 10.1210/endo-110-3-1058, Postina, R., Kojro, E., and Fahrenholz, F. (1996). Tribollet and colleagues were some of the first investigators to apply this approach to the rat brain (Tribollet et al., 1988), suggesting that AVP and OT receptor distributions were sufficiently distinct. Neuropsychopharmacol. The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. Chem. Human neuroimaging of oxytocin and vasopressin in social cognition. (2005) were one of the first groups to employ functional neuroimaging technology in order to try to better understand the mechanism by which oxytocin exerts behavioral effects in humans following acute administration. Arginine Vasopressin (AVP) and oxytocin (OXT) are peptide hormones found in most mammals that have vital physiological and behavioral actions. For example, certain oxytocin autoradiographic receptor ligands have been shown to have significant cross reactivity with AVP receptors (Toloczko et al., 1997). Oxytocin modulates neural reactivity to children's faces as a function of social salience. Natl. Little was done until recent times. Oxytocin increases amygdala reactivity to threatening scenes in females. Mitigation of sociocommunicational deficits of autism through oxytocin-induced recovery of medial prefrontal activity: a randomized trial. doi: 10.1016/j.biopsych.2012.12.023, Hamilton, P. J., Campbell, N. G., Sharma, S., Erreger, K., Herborg Hansen, F., Saunders, C., et al. One study in human brains used immunohistochemistry with a monoclonal antibody targeted to the oxytocin receptor (Boccia et al., 2013). Mol. Acad. Proc. (2007). AVP has two primary functions. Quantification of the level of inter individual variation in receptor expression will be important as well. Oxytocin promotes facial emotion recognition and amygdala reactivity in adults with asperger syndrome. Gordon et al., also found that oxytocin enhanced fMRI activity in regions including the amygdala, nucleus accumbens, and orbitofrontal cortex during social tasks in a group of children with ASD (Gordon et al., 2013). doi: 10.1016/j.neulet.2005.10.019, Smith, A. L., Freeman, S. M., Voll, R. J., Young, L. J., and Goodman, M. M. (2013a). Localization of oxytocin binding sites in the human brainstem and upper spinal cord: an autoradiographic study. Chepkova, A. N., French, P., De Wied, D., Ontskul, A. H., Ramakers, G. M., Skrebitski, V. G., et al. Neuroscience 32, 435–439. 24, 45–51. Nonapeptide receptors, like oxytocin receptor (OTR) and vasopressin 1a receptor (V1aR), modulate a variety of functions across taxa, and mediate phenotypic variation within and between species. doi: 10.1111/j.1749-6632.1996.tb32513.x, Freeman, S. M., Inoue, K., Smith, A. L., Goodman, M. M., and Young, L. J. doi: 10.1016/0306-4522(88)90078-4. Endocrinol. doi: 10.1016/j.neuroscience.2013.08.048, Bos, P. A., Panksepp, J., Bluthé, R. M., and van Honk, J. doi: 10.1523/JNEUROSCI.4572-07.2008, Pinol, R. A., Jameson, H., Popratiloff, A., Lee, N. H., and Mendelowitz, D. (2014). Oxytocin improves behavioural and neural deficits in inferring others' social emotions in autism. doi: 10.1038/305325a0. doi: 10.1016/j.neuroscience.2014.04.055. doi: 10.1016/0014-5793(94)01268-7, Declerck, C. H., Boone, C., and Kiyonari, T. (2014). Common polymorphism in the oxytocin receptor gene (OXTR) is associated with human social recognition skills. [email protected], For editorial issues, like the status of your submitted paper or proposals, write to [email protected], IOS Press Interestingly, oxytocin and vasopressin neurons have receptors for their own secreted neuropeptides on their cell surfaces, and are able modulate their own release, respectively, without necessarily triggering action potentials (Gouzenes et al., 1998; Ludwig et al., 2002). OXTR and AVPR1a were also shown to mediate reciprocal inhibitory effects in different regions within the rat amygdala via GABA activity (Huber et al., 2005). Its actions are mediated by specific oxytocin receptors. Metab. Plasma oxytocin concentrations and OXTR polymorphisms predict social impairments in children with and without autism spectrum disorder. [Epub ahead of print]. Impact Factor 3.707 | CiteScore 5.1More on impact ›, Essential pathways and circuits of autism pathogenesis In vertebrates, these systems innervate conserved neural networks that regulate social learning and behavior, including conspecific recognition, social attachment, and parental behavior. Enhanced partner preference in a promiscuous species by manipulating the expression of a single gene. doi: 10.1097/PSY.0b013e31821df0c2, Takahata, R., and Moghaddam, B. Brain Dev. The relevance of these findings to research looking at behavioral effects in humans remains unclear; a single intranasal dose of oxytocin in humans led to slight augmentation in peripheral testosterone levels, but no change in progesterone or estradiol levels (Gossen et al., 2012). Recent data have used fMRI technology to attempt to understand the potential effects of oxytocin administration in individuals with ASD. Both corticotrophin releasing hormone and vasopressin exert numerous regulatory functions throughout the entire organism. Gregory, S. G., Connelly, J. J., Towers, A. J., Johnson, J., Biscocho, D., Markunas, C. A., et al. Cortical and brainstem networks may also be impacted in this way; a recent optogenetic study showed that oxytocin secretion via hypothalamic projections to the piriform cortex was necessary for social learning around both salient and aversive stimuli (Choe et al., 2015), while oxytocin projections to brainstem autonomic nuclei mediated heart rate variability (Pinol et al., 2014). doi: 10.1016/j.brainres.2013.10.051, Walker, L. C., Price, D. L., and Young, W. S. III. Endocrinol. doi: 10.1073/pnas.1402236111, Perlow, M. J., Reppert, S. M., Artman, H. A., Fisher, D. A., Self, S. M., and Robinson, A. G. (1982). It is now clear that oxytocin is an immunoregulatory hormone and it shows therapeutic value in the inhibition of septic conditions. 14, 167–176. Brain Res. doi: 10.1016/j.regpep.2004.12.009, Gamer, M., Zurowski, B., and Buchel, C. (2010). The thymus and the pituitary gland produce oxytocin. As well, both oxytocin and vasopressin can exert effects on the cardiovascular system by affecting blood pressure, vasodilation, diuresis, and water intake (Pittman et al., 1982; Petersson et al., 1996). Some studies have also detected differential activation patterns in the basal forebrain and brainstem. The oxytocin receptor. 3,4, pp. Assembling the puzzle: pathways of oxytocin signaling in the brain. (2014). Occurring 4 times more in boys than girls (Baron-Cohen et al., 2005; Steyaert and De la Marche, 2008; Lintas and Persico, 2009), this severe developmental disorder is characte… doi: 10.1038/nature12107, Coccaro, E. F., Kavoussi, R. J., Hauger, R. L., Cooper, T. B., and Ferris, C. F. (1998). 395, 9–21. A subsequent paper confirmed differential sex effects in the same, but larger group of participants; findings were more specific, however, with increased activity in the frontal pole, medial prefrontal cortex, and caudate/putamen in men, but decreased or no activity in these regions in women, in response to reciprocal cooperation while being treated with oxytocin (Feng et al., 2014). Increased amygdala activation in females in response to negative or threatening social information was replicated in a small sample (Lischke et al., 2012), although subsequent studies did not find the same effect (see Table 2). Recent literature using optogenetic methods further support an association between the inhibitory GABA system, oxytocin, vasopressin, and behavior. Fax: +86 10 8446 7947 Vasopressin is capable of maintaining immune function, both innate and adaptive immunity. Information on the central distribution, structure, and function of these receptors will be discussed further in subsequent sections. In the following section, we review functional neuroimaging literature in response to acute peptide administration in humans. Past, present and future of vasopressin and oxytocin receptor oligomers, prototypical GPCR models to study dimerization processes. (2010). When endogenous oxytocin was released as triggered by blue light, there was a local increase in GABAergic interneuron signaling within the amygdala, which was associated with a reduction in freezing behavior in fear conditioned rats (Knobloch et al., 2012). The word oxytocin literally means "quick birth" in Greek, which is an accurate description of the hormone's action. Chem. However, OXT, AVP, and their receptors are also expressed in several areas of the CNS and exert widespread neuromodulatory effects on homeostasis and behavior. Oxytocin will be released in response to sepsis, and other form of infections, inflammatory disease and in stress situations. Rilling and colleagues have published several manuscripts attempting to tease apart the sex effects of this response, with increasingly large sample sizes, using the prisoner's dilemma game. Behav. (2007). They found AVPR1a receptors diffusely throughout the brain, with oxytocin receptors more localized to specific areas (e.g., the hippocampus and surrounding areas, nucleus basalis, thalamus, visual cortex, and brainstem structures). Oxytocin and vasopressin are pituitary neuropeptides that have been shown to affect social processes in mammals. 127, 225–231. Oxytocin enhances brain function in children with autism. Intranasal oxytocin administration attenuates the ACTH stress response in monkeys. 555, 220–232. doi: 10.1016/j.psyneuen.2005.04.002, Parker, K. J., Garner, J. P., Libove, R. A., Hyde, S. A., Hornbeak, K. B., Carson, D. S., et al. A separate body of research proposes that the neuropeptide effects occur specifically on fast spiking interneurons. doi: 10.1016/j.cell.2014.09.020, Nakamura, K., Sekine, Y., Ouchi, Y., Tsujii, M., Yoshikawa, E., Futatsubashi, M., et al. The specific distribution of oxytocin and vasopressin receptors in the human brain has been difficult to study precisely. doi: 10.1038/nature00822, McDonald, A. J., Muller, J. F., and Mascagni, F. (2011). In this case corticotrophin releasing hormone regulates the inflammatory process, and vasopressin supports this role. doi: 10.3109/10253890.2011.560309, Owen, S. F., Tuncdemir, S. N., Bader, P. L., Tirko, N. N., Fishell, G., and Tsien, R. W. (2013). Ferris, C. F. (1996). However, by looking across existing human studies, and extrapolating from primate data, several conclusions can be drawn: (1) Oxytocin and vasopressin receptors are consistently detected in the hypothalamus. Biol. Prog. Proc. Interaction between oestrogen and oxytocin on hypothalamic-pituitary-adrenal axis activity. Sex hormones appear to impact on the density of peptide receptor expression from early life, while both oxytocin and vasopressin can modulate stress responses in the hypothalamic-pituitary (HPA) axis. Learn vocabulary, terms, and more with flashcards, games, and other study tools. There is cross reactivity in binding of each peptide with its respective receptor; oxytocin binds to the oxytocin receptor with only 10x greater affinity than vasopressin, for example (Kimura et al., 1994). Science 343, 675–679. The genetic sequences coding for mouse, rat, and human oxytocin/vasopressin receptor genes are conserved across species, with over 80% identical amino acid residues. This finding may be of relevance in ASD given emerging evidence of aberrant autonomic functioning and heart rate reactivity in this condition (Ming et al., 2005; Kushki et al., 2013). Science 333, 104–107. (2014). 139, 147–162. The amygdala was no longer implicated with the larger sample size. doi: 10.1126/science.1201043, Voorthuis, A., Riem, M. M., Van, I. M. H., and Bakermans-Kranenburg, M. J. She has received grant funding from Sanofi-Aventis Canada and SynapDx. J. Neuroendocrinol. Acad. doi: 10.1016/j.psyneuen.2012.01.011, Liu, N., Hadj-Bouziane, F., Jones, K. B., Turchi, J. N., Averbeck, B. This effect persisted despite controlling for estradiol and progesterone levels. Nature 500, 458–462. Al-Ayadhi, L. Y. Oxytocin increased caudate activation in response to positive cooperation and also increased left amygdala activity on whole brain analysis. (1994). (2014a). Both oxytocin and vasopressin receptors show capacity to form hetero- homo- or oligo-dimers in vitro; it is unclear to what extent formation of receptor complexes is a biologically important process in vivo (Cottet et al., 2010). Cell 159, 295–305. Chem. 10, 383–390. doi: 10.1001/jamapsychiatry.2013.3181, Weiser, M. J., Foradori, C. D., and Handa, R. J. Correlation between oxytocin neuronal sensitivity and oxytocin receptor binding: an electrophysiological and autoradiographical study comparing rat and guinea pig hippocampus. Vasopressin modulates medial prefrontal cortex-amygdala circuitry during emotion processing in humans. doi: 10.1038/nrn2635, Shapiro, R. A., Xu, C., and Dorsa, D. M. (2000). Neuroscience 121, 537–544. The same investigators subsequently applied this technique to the entire brain, while adding an AVP receptor ligand ([3H]AVP) to distinguish AVP binding from binding to the oxytocin receptor, in both cortical and subcortical regions. (2003). Kirsch et al. BMC Med. Pept. This must be related of its immunoregulatory power. Proc. In this task, participants must choose whether to risk cooperating to achieve the best outcome for both participants, or defect against their partner and achieve a positive outcome for themselves only (Declerck et al., 2014). Oxytocin attenuates neural reactivity to masked threat cues from the eyes. 16, 255–260. Oxytocin selectively gates fear responses through distinct outputs from the central amygdala. During acute illness vasopressin will rise along with corticotrophin releasing hormone. The vasopressin 1b receptor and the neural regulation of social behavior. doi: 10.1016/j.yhbeh.2012.01.016, Zink, C. F., Stein, J. L., Kempf, L., Hakimi, S., and Meyer-Lindenberg, A. Oxytocin interacts with cytokines. J. Neurosci. In human subjects with personality disorders, CSF levels of AVP correlated with aggression, while one of two serotonin proxy-measures was inversely associated with aggressive behavior (Coccaro et al., 1998). Biol. Brain Imaging Behav. 60, 1311–1315. Nature 418, 85–89. Antidepressant and anxiolytic profiles of newly synthesized arginine vasopressin V1B receptor antagonists: TASP0233278 and TASP0390325. doi: 10.1038/npp.2013.254, Domes, G., Lischke, A., Berger, C., Grossmann, A., Hauenstein, K., Heinrichs, M., et al. Central administration of vasopressin triggered aggression in rats, but the effect was lessened if they had been castrated, thereby lowering testosterone levels (Korte et al., 1990). Functional neuroimaging studies further support a link between these neuropeptides and activity in specific brain regions implicated in social communication and behavior. For example, knockout of either the oxytocin gene, or estrogen receptors α or β led to deficient social abilities in mice (Choleris et al., 2003). 29, 2259–2271. In the cortical sections, oxytocin binding was strongest in the basal forebrain and nearby structures, including (1) specific cholinergic tracts (i.e., the basal nucleus of Meynert and the nucleus of the vertical limb of the diagonal band of Broca); (2) in the ventral part of the lateral septal nucleus (which relays between the hippocampus, thalamus, and midbrain); and (3) in parts of the hypothalamus and basal ganglia. The authors specifically commented on a lack of oxytocin receptor detection in the raphe nucleus of the brainstem. Behav. doi: 10.1111/j.1365-2826.2010.01976.x, Huang, H., Michetti, C., Busnelli, M., Manago, F., Sannino, S., Scheggia, D., et al. We contend that to fully understand their function, research should consider how they are flexibly fitted to maximize survival and reproduction given the variety of human experience. The role of the oxytocin and vasopressin systems in social functioning has developed out of a large body of animal research, focusing primarily on rodents. (2012). X-linked nephrogenic diabetes insipidus mutations in North America and the Hopewell hypothesis. Oxytocin injections to animals either stimulate (low dose) or inhibit (high dose) growth hormone secretion. 30, 109–115. Plasma estrogen levels did not modulate this effect. Neuron 73, 553–566. Oxytocin and vasopressin in the human brain: social neuropeptides for translational medicine. Specifically, Knobloch et al. doi: 10.1523/JNEUROSCI.3984-05.2005, Knobloch, H. S., Charlet, A., Hoffmann, L. C., Eliava, M., Khrulev, S., Cetin, A. H., et al. Neuroscience 273, 12–23. 12, 524–538. Data in rodent models suggest that the aggressive behavior stimulated as a result of AVP administration can be blocked via serotonergic activity (Delville et al., 1996a; Ferris, 1996). Tyzio, R., Cossart, R., Khalilov, I., Minlebaev, M., Hubner, C. A., Represa, A., et al. J. Neurosci. Muscarinic cholinergic contribution to memory consolidation: with attention to involvement of the basolateral amygdala. PLoS Biol. Modulation of stress-induced ACTH release by corticotropin-releasing factor, catecholamines and vasopressin. doi: 10.1016/j.neuron.2013.10.038, Stevenson, E. L., and Caldwell, H. K. (2012). Dopamine activity in the nucleus accumbens is central to behavioral reinforcement, reward, and motivation. The neuroanatomical distribution of oxytocin receptor binding and mRNA in the male rhesus macaque (Macaca mulatta). Pharmacol. J. Neuroendocrinol. Interest in using AVPR1b antagonism to treat anxiety disorders has been investigated showing potential benefits in rodent models (Iijima et al., 2014), while commercial human studies are underway for AVPR1a receptor antagonists as a potential treatment for ASD (e.g., RG7314, clinical trials.gov ID: NCT01793441). Anxious behavior when exploring an unfamiliar maze was also less (Windle et al., 1997). Behav. Natl. This effect resulted from reduced neuronal activity in the hypothalamus, hippocampus, and ventrolateral septum, as indicated by absence of elevations c-fos mRNA expression in these regions in the rats who were restrained and treated with oxytocin; no such effect was seen with vasopressin. The effects of oxytocin and vasopressin on partner preferences in male and female prairie voles (Microtus ochrogaster). doi: 10.1017/S1461145712000533, Stanley, D. A., and Adolphs, R. (2013). Evidence derived from mouse models indicates that a transmembrane glycoprotein called CD38 must be present to facilitate depolarization-induced oxytocin secretion in the pituitary, and that blockade of this molecule interrupts mouse maternal and social behavior (Jin et al., 2007; Lopatina et al., 2012). compared fMRI signals and functional connectivity measures in male participants during the prisoner's dilemma game, following administration of either oxytocin or vasopressin. We will then correlate this research with current functional neuroimaging literature examining responses to experimental manipulation of these systems. Psychiatry 51, 712–721.e1. Oxytocin and arginine vasopressin (AVP) are neuropeptides synthesized in the hypothalamus and secreted from the posterior pituitary gland. Adv. For example, numerous immune system differences have been detected in autism, while specific inflammatory cytokines have been shown to alter the expression of oxytocin receptors in vitro. Overall, a model in which the local neuromodulatory effects of pituitary neuropeptides on brainstem and basal forebrain regions strengthen signaling within social neurocircuits proves appealing. Evoked axonal oxytocin release in the central amygdala attenuates fear response. Genomic and epigenetic evidence for oxytocin receptor deficiency in autism. Imbalances in excitatory/inhibitory neurotransmission have increasingly been characterized in neurodevelopmental disorders such as ASD, while cellular physiology research suggests that both oxytocin and vasopressin can alter this balance by acting on interneurons. Solution for The hormones oxytocin and vasopressin are 9-mer peptides than differ in the identity of only two residues, yet have very different functions. Sci. Specifically, research in prairie voles has highlighted the importance of dopamine in facilitating the partner preference formation via oxytocin and vasopressin manipulation. Oxytocin attenuates stress-induced c-fos mRNA expression in specific forebrain regions associated with modulation of hypothalamo-pituitary-adrenal activity. doi: 10.1073/pnas.1508097112, Liu, Y., and Wang, Z. X. Clifton, VA 20124 In women, however, neither peptide led to activation in these brain regions; oxytocin instead decreased amygdala activity (Rilling et al., 2014). This is necessary to protect Reduced cardiac parasympathetic activity in children with autism. Of note, in ASD, abnormal levels of inflammatory cytokines have been described (Croonenberghs et al., 2002). Nat. While earlier studies suggested potentially lower oxytocin and vasopressin levels in the plasma of children with ASD as compared to typical children (Modahl et al., 1998; Al-Ayadhi, 2005), subsequent research has shown that plasma oxytocin levels tend to be similar within members of the same family, irrespective of a diagnosis of autism, although do correlate with social communication abilities overall (Parker et al., 2014). (2015). doi: 10.1016/0006-8993(89)90317-X, Ludwig, M., Callahan, M. F., Neumann, I., Landgraf, R., and Morris, M. (1994). (1990). doi: 10.1016/j.biopsych.2011.02.006, Riem, M. M., Bakermans-Kranenburg, M. J., Voorthuis, A., and van, I. M. H. (2014). Psychoneuroendocrinology 39, 237–248. doi: 10.1016/S0079-6123(02)39016-2, Toloczko, D. M., Young, L., and Insel, T. R. (1997). First, both peptides are produced in in hypothalamic neurosecrotor neurons (parvocellular neurons), whose axons project to the anterior pituitary and other brain regions in rodents (Castel and Morris, 1988; Ludwig and Leng, 2006). Our knowledge of these processes stems almost exclusively from research in animal models, primarily in rodents (see Ludwig and Leng, 2006, for an extensive review). In rats, application of AVP to hippocampal tissue sections increased the frequency of inhibitory signals; this process was shown to occur due to AVP binding to AVPR1a, which through a G-protein mediated cascade, increased the excitability of interneurons, leading to increased GABA release. Invest. 139, 179–196. (2012). The strength of binding of the neuropeptide into its specific binding pocket can be manipulated by mutational analyses; for example, single amino acid substitutions at key structural areas can significantly reduce or eliminate peptide binding (Hausmann et al., 1996; Postina et al., 1996). Lett. Ventral tegmental area involvement in pair bonding in male prairie voles. doi: 10.1016/S0306-4522(97)00683-0, Yizhar, O., Fenno, L. E., Prigge, M., Schneider, F., Davidson, T. J., O'shea, D. J., et al. Effects of oxytocin and prosocial behavior on brain responses to direct and vicariously experienced pain. Psychoneuroendocrinology 30, 924–929. Neuroendocrinol. A., Rossetti, M. A., McCullough, M. E., et al. Brain Res. There have been numerous and varied attempts to classify interneurons based on their structure and function. Select this link to jump to navigation, In footer section. Physiol. Sex differences in the neural and behavioral response to intranasal oxytocin and vasopressin during human social interaction. (2004). 61, 277–282. Estrogen receptor-beta mediates dihydrotestosterone-induced stimulation of the arginine vasopressin promoter in neuronal cells. Interestingly, these axonal projections are only detected in adult animals, and are absent in prenatal and early postnatal studies. Behav. Regul. Brain 137, 3073–3086. Available online at: http://www.neurosciencesjournal.org/pdffiles/Jan05/05Altered.pdf, Alves, S. E., Lopez, V., McEwen, B. S., and Weiland, N. G. (1998). (1998). doi: 10.1038/nrn1845, Ludwig, M., Sabatier, N., Bull, P. M., Landgraf, R., Dayanithi, G., and Leng, G. (2002). Busnelli, M., Bulgheroni, E., Manning, M., Kleinau, G., and Chini, B. 113, 1071–1079. Tissue taken from hysterectomy or cesarean section at different gestational time points in pregnant women has shown a significant and rapid up regulation (e.g., 200-fold) of oxytocin receptor expression around the onset of labor, facilitating uterine contractions (Fuchs et al., 1984). Rev. 262, 143–149. 276, 19452–19460. Potential implications for, and associations with ASD are included throughout. Endocrinology 110, 1058–1060. doi: 10.1016/S0031-9384(04)00346-4, Higashida, H., Lopatina, O., Yoshihara, T., Pichugina, Y. Following secretion, these peptides are thought diffuse throughout the extracellular space, serving a neuromodulatory effect on surrounding brain tissue (Landgraf and Neumann, 2004). Neuropsychopharmacology 39, 1102–1114. doi: 10.1016/j.psyneuen.2011.07.013, Rivier, C., and Vale, W. (1983). Figure 2. Neurosci. (2014). 52, 344–351. This mechanism appeared to be mediated via dopaminergic activity in the nucleus accumbens, as evidenced by increased dopamine turnover in this area, and specificity of the effects of D2 blockade injected into this region in particular (Gingrich et al., 2000; Aragona et al., 2003). It is beyond the scope of this review to present non-immune effects of these mediators.
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