Oxytocin Modulates FMRI Responses to Facial Expression in Macaques

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2015 May 28

PMID 26015576

Citations 32

Authors

Ning Liu

Fadila Hadj-Bouziane

Katherine B Jones

Janita N Turchi

Bruno B Averbeck

Leslie G Ungerleider

Affiliations

Soon will be listed here.

Abstract

Increasing evidence has shown that oxytocin (OT), a mammalian hormone, modifies the way social stimuli are perceived and the way they affect behavior. Thus, OT may serve as a treatment for psychiatric disorders, many of which are characterized by dysfunctional social behavior. To explore the neural mechanisms mediating the effects of OT in macaque monkeys, we investigated whether OT would modulate functional magnetic resonance imaging (fMRI) responses in face-responsive regions (faces vs. blank screen) evoked by the perception of various facial expressions (neutral, fearful, aggressive, and appeasing). In the placebo condition, we found significantly increased activation for emotional (mainly fearful and appeasing) faces compared with neutral faces across the face-responsive regions. OT selectively, and differentially, altered fMRI responses to emotional expressions, significantly reducing responses to both fearful and aggressive faces in face-responsive regions while leaving responses to appeasing as well as neutral faces unchanged. We also found that OT administration selectively reduced functional coupling between the amygdala and areas in the occipital and inferior temporal cortex during the viewing of fearful and aggressive faces, but not during the viewing of neutral or appeasing faces. Taken together, our results indicate homologies between monkeys and humans in the neural circuits mediating the effects of OT. Thus, the monkey may be an ideal animal model to explore the development of OT-based pharmacological strategies for treating patients with dysfunctional social behavior.

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References

Gordon I, Vander Wyk B, Bennett R, Cordeaux C, Lucas M, Eilbott J . Oxytocin enhances brain function in children with autism. Proc Natl Acad Sci U S A. 2013; 110(52):20953-8. PMC: 3876263. DOI: 10.1073/pnas.1312857110. View

Schall J, Morel A, King D, Bullier J . Topography of visual cortex connections with frontal eye field in macaque: convergence and segregation of processing streams. J Neurosci. 1995; 15(6):4464-87. PMC: 6577698. View

Phillips M, Drevets W, Rauch S, Lane R . Neurobiology of emotion perception I: The neural basis of normal emotion perception. Biol Psychiatry. 2003; 54(5):504-14. DOI: 10.1016/s0006-3223(03)00168-9. View

Modi M, Connor-Stroud F, Landgraf R, Young L, Parr L . Aerosolized oxytocin increases cerebrospinal fluid oxytocin in rhesus macaques. Psychoneuroendocrinology. 2014; 45:49-57. PMC: 4120060. DOI: 10.1016/j.psyneuen.2014.02.011. View

Vanduffel W, Fize D, Mandeville J, Nelissen K, Van Hecke P, Rosen B . Visual motion processing investigated using contrast agent-enhanced fMRI in awake behaving monkeys. Neuron. 2001; 32(4):565-77. DOI: 10.1016/s0896-6273(01)00502-5. View

Romanski L, Diehl M . Neurons responsive to face-view in the primate ventrolateral prefrontal cortex. Neuroscience. 2011; 189:223-35. PMC: 3150453. DOI: 10.1016/j.neuroscience.2011.05.014. View

Schorscher-Petcu A, Sotocinal S, Ciura S, Dupre A, Ritchie J, Sorge R . Oxytocin-induced analgesia and scratching are mediated by the vasopressin-1A receptor in the mouse. J Neurosci. 2010; 30(24):8274-84. PMC: 2902996. DOI: 10.1523/JNEUROSCI.1594-10.2010. View

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

Young L, Toloczko D, Insel T . Localization of vasopressin (V1a) receptor binding and mRNA in the rhesus monkey brain. J Neuroendocrinol. 1999; 11(4):291-7. DOI: 10.1046/j.1365-2826.1999.00332.x. View

10.

Gamer M, Zurowski B, Buchel C . Different amygdala subregions mediate valence-related and attentional effects of oxytocin in humans. Proc Natl Acad Sci U S A. 2010; 107(20):9400-5. PMC: 2889107. DOI: 10.1073/pnas.1000985107. View

11.

Mesulam M, Mufson E, Levey A, Wainer B . Cholinergic innervation of cortex by the basal forebrain: cytochemistry and cortical connections of the septal area, diagonal band nuclei, nucleus basalis (substantia innominata), and hypothalamus in the rhesus monkey. J Comp Neurol. 1983; 214(2):170-97. DOI: 10.1002/cne.902140206. View

12.

Wilson C, Gaffan D, Browning P, Baxter M . Functional localization within the prefrontal cortex: missing the forest for the trees?. Trends Neurosci. 2010; 33(12):533-40. PMC: 2997428. DOI: 10.1016/j.tins.2010.08.001. View

13.

Domes G, Heinrichs M, Michel A, Berger C, Herpertz S . Oxytocin improves "mind-reading" in humans. Biol Psychiatry. 2006; 61(6):731-3. DOI: 10.1016/j.biopsych.2006.07.015. View

14.

Dal Monte O, Noble P, Turchi J, Cummins A, Averbeck B . CSF and blood oxytocin concentration changes following intranasal delivery in macaque. PLoS One. 2014; 9(8):e103677. PMC: 4136720. DOI: 10.1371/journal.pone.0103677. View

15.

Landman R, Sharma J, Sur M, Desimone R . Effect of distracting faces on visual selective attention in the monkey. Proc Natl Acad Sci U S A. 2014; 111(50):18037-42. PMC: 4273369. DOI: 10.1073/pnas.1420167111. View

16.

Willis M, Palermo R, McGrillen K, Miller L . The nature of facial expression recognition deficits following orbitofrontal cortex damage. Neuropsychology. 2014; 28(4):613-623. DOI: 10.1037/neu0000059. View

17.

Guastella A, Mitchell P, Dadds M . Oxytocin increases gaze to the eye region of human faces. Biol Psychiatry. 2007; 63(1):3-5. DOI: 10.1016/j.biopsych.2007.06.026. View

18.

Blatt G, Andersen R, Stoner G . Visual receptive field organization and cortico-cortical connections of the lateral intraparietal area (area LIP) in the macaque. J Comp Neurol. 1990; 299(4):421-45. DOI: 10.1002/cne.902990404. View

19.

Watson K, Platt M . Of mice and monkeys: using non-human primate models to bridge mouse- and human-based investigations of autism spectrum disorders. J Neurodev Disord. 2012; 4(1):21. PMC: 3445833. DOI: 10.1186/1866-1955-4-21. View

20.

Dal Monte O, Noble P, Costa V, Averbeck B . Oxytocin enhances attention to the eye region in rhesus monkeys. Front Neurosci. 2014; 8:41. PMC: 3939446. DOI: 10.3389/fnins.2014.00041. View