Intranasal Oxytocin in Rhesus Monkeys Alters Brain Networks That Detect Social Salience and Reward

Overview

Journal Am J Primatol

Date 2018 Oct 9

PMID 30295946

Citations 3

Authors

Lisa A Parr

Thomas Mitchell

Erin Hecht

Affiliations

Soon will be listed here.

Abstract

In primates, resting state functional neuroimaging (rsfcMRI) has identified several large-scale, intrinsic brain networks, including the salience network (SN), which is involved in detecting stimulus salience. Intranasal oxytocin (IN-OT) has been shown to modulate the salience and rewarding quality of social stimuli in mammals and numerous studies have shown that it can affect the functional connectivity between brain regions. Less is known, however, about how these effects unfold over time following IN-OT administration. This study used rsfcMRI in anesthetized rhesus macaques to track temporal changes in the functional connectivity between brain regions involved in the SN, including the anterior cingulate cortex (ACC), anterior insula (AI), amygdala (amy), and ventral striatum (vstr), lasting 3 hr after IN-OT or Placebo (saline) administration. We found significant temporal changes in the functional connectivity between all regions associated with treatment condition. IN-OT increased the functional connectivity between AI_vstr, ACC_amy (right hemisphere), ACC_vstr (left hemisphere), and amy_vstr (right hemisphere), but reduced the functional connectivity between ACC_AI, and the AI_amygdala. These results suggest that IN-OT may dampen salience detection in rhesus monkeys, consistent with previous findings of reduced social vigilance, while enhancing the connectivity between the SN and regions involved in processing reward.

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References

Bartz J, Zaki J, Bolger N, Ochsner K . Social effects of oxytocin in humans: context and person matter. Trends Cogn Sci. 2011; 15(7):301-9. DOI: 10.1016/j.tics.2011.05.002. View

Quintana D, Westlye L, Alnaes D, Rustan O, Kaufmann T, Smerud K . 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. Psychoneuroendocrinology. 2016; 69:180-8. DOI: 10.1016/j.psyneuen.2016.04.010. View

Dosenbach N, Visscher K, Palmer E, Miezin F, Wenger K, Kang H . A core system for the implementation of task sets. Neuron. 2006; 50(5):799-812. PMC: 3621133. DOI: 10.1016/j.neuron.2006.04.031. View

Heinrichs M, Domes G . Neuropeptides and social behaviour: effects of oxytocin and vasopressin in humans. Prog Brain Res. 2008; 170:337-50. DOI: 10.1016/S0079-6123(08)00428-7. View

Seeley W, Menon V, Schatzberg A, Keller J, Glover G, Kenna H . Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci. 2007; 27(9):2349-56. PMC: 2680293. DOI: 10.1523/JNEUROSCI.5587-06.2007. View

Skuse D, Gallagher L . Dopaminergic-neuropeptide interactions in the social brain. Trends Cogn Sci. 2008; 13(1):27-35. DOI: 10.1016/j.tics.2008.09.007. View

Katz L, Shatz C . Synaptic activity and the construction of cortical circuits. Science. 1996; 274(5290):1133-8. DOI: 10.1126/science.274.5290.1133. View

Johnson N, Hanson L, Frey W . Trigeminal pathways deliver a low molecular weight drug from the nose to the brain and orofacial structures. Mol Pharm. 2010; 7(3):884-93. PMC: 2892271. DOI: 10.1021/mp100029t. View

Modi M, Young L . The oxytocin system in drug discovery for autism: animal models and novel therapeutic strategies. Horm Behav. 2011; 61(3):340-50. PMC: 3483080. DOI: 10.1016/j.yhbeh.2011.12.010. View

10.

Freeman S, Inoue K, Smith A, Goodman M, Young L . The neuroanatomical distribution of oxytocin receptor binding and mRNA in the male rhesus macaque (Macaca mulatta). Psychoneuroendocrinology. 2014; 45:128-41. PMC: 4043226. DOI: 10.1016/j.psyneuen.2014.03.023. View

11.

Stein M, Simmons A, Feinstein J, Paulus M . Increased amygdala and insula activation during emotion processing in anxiety-prone subjects. Am J Psychiatry. 2007; 164(2):318-27. DOI: 10.1176/ajp.2007.164.2.318. View

12.

Miranda-Dominguez O, Mills B, Grayson D, Woodall A, Grant K, Kroenke C . Bridging the gap between the human and macaque connectome: a quantitative comparison of global interspecies structure-function relationships and network topology. J Neurosci. 2014; 34(16):5552-63. PMC: 3988411. DOI: 10.1523/JNEUROSCI.4229-13.2014. View

13.

Rushworth M . Intention, choice, and the medial frontal cortex. Ann N Y Acad Sci. 2008; 1124:181-207. DOI: 10.1196/annals.1440.014. View

14.

Insel T . The challenge of translation in social neuroscience: a review of oxytocin, vasopressin, and affiliative behavior. Neuron. 2010; 65(6):768-79. PMC: 2847497. DOI: 10.1016/j.neuron.2010.03.005. View

15.

Chang S, Barter J, Ebitz R, Watson K, Platt M . Inhaled oxytocin amplifies both vicarious reinforcement and self reinforcement in rhesus macaques (Macaca mulatta). Proc Natl Acad Sci U S A. 2012; 109(3):959-64. PMC: 3271866. DOI: 10.1073/pnas.1114621109. View

16.

van den Heuvel M, Hulshoff Pol H . Exploring the brain network: a review on resting-state fMRI functional connectivity. Eur Neuropsychopharmacol. 2010; 20(8):519-34. DOI: 10.1016/j.euroneuro.2010.03.008. View

17.

Blackford J, Clauss J, Avery S, Cowan R, Benningfield M, VanDerKlok R . Amygdala-cingulate intrinsic connectivity is associated with degree of social inhibition. Biol Psychol. 2014; 99:15-25. PMC: 4274047. DOI: 10.1016/j.biopsycho.2014.02.003. View

18.

Piva M, Chang S . An integrated framework for the role of oxytocin in multistage social decision-making. Am J Primatol. 2018; 80(10):e22735. PMC: 6053333. DOI: 10.1002/ajp.22735. View

19.

Corbetta M, Shulman G . Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci. 2002; 3(3):201-15. DOI: 10.1038/nrn755. View

20.

Hanson L, Frey 2nd W . Intranasal delivery bypasses the blood-brain barrier to target therapeutic agents to the central nervous system and treat neurodegenerative disease. BMC Neurosci. 2008; 9 Suppl 3:S5. PMC: 2604883. DOI: 10.1186/1471-2202-9-S3-S5. View