Oxytocin and social adaptation:
Insights from neuroimaging studies of healthy and clinical populations
Yina Ma1, Simone Shamay-Tsoory2, Shihui Han3, Caroline F. Zink4
1State Key Laboratory of Cognitive Neuroscience and Learning, IDG/McGovern Institute for Brain Research
Beijing Normal University, Beijing, China
2Department of Psychology, University of Haifa, Israel
3Department of Psychology and PKU-IDG/McGovern Institute for Brain Research, Peking University, Beijing, China
4Lieber Institute for Brain Development, USA
Address correspondence to:
Yina Ma Ph. D.
State Key Laboratory of Cognitive Neuroscience and Learning
IDG/McGovern Institute for Brain Research
Beijing Normal University
Beijing, 100875, China
Email:
Table S1 Summary of oxytocin-fMRI studies.
Studies examining OT effects on human brain function published before August 2015 were selected through a standard search in PubMed and Embase with keywords [‘oxytocin’] AND [‘fMRI’ OR ‘magnetic resonance imaging’]. The current review focused on fMRI studies, and excluded papers that used EEG, MEG, SPECT, PET or MRS, and those did not employ a double-blind, placebo-controlled procedure. Additional studies were collected by reviewing the reference list of relevant papers in the first step, or through the ‘related article’ function of the PubMed database. Table S1 provided details of all eligible studies, including the experimental paradigm/task/stimuli, participants' information and summary of the main OT neural effects of each study.
First Author, year / Paradigm/task / Stimuli / Male / Female / Dose(IU) / Design / Main OT neural effect summary
Oxytocin-fMRI Studies Involved Patients
Pincus, 20101 / RMET (affect, motor, gender task) / Faces / - / D (8)
H (8) / 40 / 1 / OTSTG, Ins, IFG, SFG, MFG, ACC in D in affect attribution;
CA, AMY, ACC, STG, IFG in H in affect attribution
Labuschagne, 20102 / Emotion/Shape match / Happy/fearful/angry/neutral faces / SAD (18) H (18) / - / 24 / 1 / AMY to fearful faces in SAD;
No OT effect on AMY in H.
Labuschagne, 20123 / Emotional valence identification / Happy/sad/neutral faces / SAD (18) H (18) / - / 24 / 1 / mPFC, ACC, SMA, SPL, VC, FFG to sad face; mPFC, ACC, CA, CB to happy face in SAD;
ACC, MFG, SMA, SPL, Tha to sad face; mPFC, ACC, MFG, precu, FFG, CB, STG to happy face in H.
Domes, 20134 / Face/house matching / Faces, houses / ASD (14) H (14) / - / 24 / 1 / AMY to faces in ASD
AMY to faces in H.
Bertsch, 20135 / Emotion classification / Happy/fearful/angry faces / - / BP (41)
H (38) / 26 / 2 / AMYto happy faces, to angry faces in BPD. AMYto angry faces, to happy faces in H
Gordon, 20136 / RMET / Eye/vehicles / ASD (18) / ASD (3) / 24 / 1 / OT x Social (eye>vehicles) interaction: striatum, NAcc, CB, PreCu, PCC, IPL, STS for eye, for vehicle
Watanabe, 20147 / Foe/friend judgment / Positive/negative face/word / ASD (33) / - / 24 / 1 / dmPFC, ACC, SFG, STS; dmPFC-AI/ACC FC, AMY-ACC FC to face vs. word
Dodhia, 20148 / Resting-state / - / SAD (18) H (18) / - / 24 / 1 / AMY-rostral ACC/mPFC FC, amygdala-frontal FC in SAD
Domes, 20149 / Word/emotion judgment / Eye/mouth/word / ASD (14)
H (14) / - / 24 / 1 / AMY, TP, STG, IFG, SMA, CB, dlPFC, Tha, SPL to Eye; AMY, TP, AI, STG, IFG, PCC, brainstem, precentral, ACC, SMA, CB, dlPFC, Tha, SPL to mouth
Aoki, 201410 / First-order false belief task / Picture and sentence / ASD (20) / - / 24 / 1 / AI, cuneus, MT, IFG to social emotion inference
Gorka, 201511 / Emotion/Shape match / Happy/fearful/angry/neutral faces / SAD (16) H (17) / - / 24 / 1 / AMY activity to fearful faces in SAD. OT x Group interaction in FC between AMY and Ins, MCC, SMA, STG, PT to fearful faces in SAD, in H
Oxytocin-fMRI Studies Conducted on Healthy Volunteers
Kirsch, 200512 / Emotion/Shape match / Fearful/threatening scenes and faces / 15 / - / 27 / 1 / AMY to threatening faces/scenes, AMY-brainstem FC
Domes, 200713 / Morphed face / Happy/fearful/angry/neutral faces / 13 / - / 24 / 1 / AMY, ITG, MTG, MFG, CB to fear face; AMY, Tha, postcentral to angry face; AMY, ITG, MTG, paracentral to happy faces
Singer, 200814 / Empathy for pain / Experimental cues / 20 / - / 32 / 1 / AMY, striatum, midbrain, OFC to painful stimulation;
OFC to empathy for other’s pain.
Petrovic, 200815 / Fear conditioning / Direct/averted gazed faces / 27 / - / 32 / 2 / AMY, subgenual ACC, right vlPFC, FG, left vlPFC to conditioned direct eye-gaze; vmPFC, OFC, left vlPFC to conditioned averted eye-gaze
Baumgartner, 200816 / Trust and risk game / Numbers / 49 / 24 / 2 / AMY, Postcentral, PT, Ins, CA, midbrain to negative feedback in trust game;
no OT effect for negative feedback in risk game
Gamer, 201017 / Emotional valence identification / Happy/fearful/neutral faces / 46 / 24 / 2 / AMY to fearful faces; AMY to happy faces; AMY, SC, AMY-SC FC when shifting gazing to eye
Domes, 201018 / Emotion arousal / Happy/fearful/angry/neutral faces / - / 16 / 24 / 1 / MTL, AMY, Ins, FFG, STG, CB, brainstem; prefrontal to fearful face;
IFG, vlPFC, dlPFC to angry face; MTL, FFG, Ins, STG, hippo, CB; dlPFC to happy faces
Rilling, 201119 / Prisoner's Dilemma game / Numbers / 63 / - / 24 / 2 / ACC, VC, vlPFC, SPL to defect; PT, Ins, AMY, CA, vlPFC, PCC, ITG, OFC, MFG, MTG, IFG; AMY-AI FC to cooperation
Riem, 201120 / Passive listening infant cry / Cry sounds / - / 42 / 24 / 2 / AMY, Ins, IFG to infant cry
Sauer, 201221 / Emotion/Shape match / fearful/threatening scenes and faces / 55 / - / 25 / 1 / FFG, MT, CB, MCC, angular, Ins (this OT effect: A- A+ of rs3796863);
Exp. 221 / Eye gaze / Faces / 55 / - / 25 / MFG, MO to eye-gaze (this OT effect: A- > A+ of rs3796863);
CB, paracentral, PH to direct vs. averted eye-gaze (this OT effect: A- < A+);
Riem, 201222 / Passive listening infant cry/laughter / Cry/larghter sounds / - / 42 / 24 / 2 / AMY; FC between AMY and OFC, hippo, angular, MTG to infant laughter
Striepens, 201223 / Encoding/Retrieval / Aversive/neutral pictures / 70 / - / 24 / 2 / AMY; Ins;
FC between AMY and AI, IFG
Lischke, 201224 / Emotion arousal / Positive, negative, neutral scenes / - / 14 / 24 / 1 / AMY, ITG, TP, postcentral to negative scenes; SMA to positive scenes
Wittfoth-Schardt, 201225 / Passive view / Own/familar/unknown children / 19 / - / 24 / 1 / GP, CA viewing own child; GP, MTG viewing unknown child;
FC between left GP and right GP, Hippcampus, MFG, SPG viewing own vs. familiar child
Montag, 201326 / Eye gaze / Faces / 55 / - / 25 / 1 / AMY to directed eye-gaze in both genotypes of rs401015;
To averted eye-gaze: AMY in TC carriers; in TT of rs401015
Sauer, 201327 / Emotion/Shape match / Fearful/threatening scenes and faces / 55 / - / 25 / 1 / AMY to negative stimuli; no OT effect to positive stimuli;
CD38 gene x COMT gene x OT interaction in AMY activity
Rupp, 201328 / 1 back / Sexual/infant pic / - / 53 / 24 / 2 / AMY to sexual arousal; AMY to infant arousal
Scheele, 201329 / Passive view / Partner/familiar/unknown women / 40 / - / 24 / 1 / VTA, NAcc, PT, GP to partner’s face; to unfamiliar faces for heterosexual pair-bonded males
Sripada, 201330 / Resting-State / - / 15 / - / 24 / 1 / AMY-mPFC FC
Groppe, 201331 / Social incentive delay / Happy/angry faces / - / 28 / 26 / 2 / MT, MO, VTA, MCC, NAcc, Ins to social reward anticipation;
precentral, postcentral, cuneus
Riem, 201332 / Resting-State / - / - / 42 / 16 / 2 / FC between PCC and brainstem, CB
Rupp, 201433 / 1 back / Negative/neutral pictures / - / 53 / 24 / 2 / AMY to negative pictures
Grimm, 201434 / Montreal Imaging stress task / Arithmetic numbers / 32 / - / 24 / 1 / PH, PCC, ACC, Ins; Tha, hippo (all subjects);
Early-life stress x OT interaction in ACC, AMY, PH, Ins, PT, CA
Riem, 201435 / RMET / Faces / - / 50 / 16 / 2 / Ins, STG (all subjects); Maternal love withdrawal x OT interaction in STG (for high love-withdraw; no OT effect for low love withdraw)
Voorthuis, 201436 / emotion/gender judgment (Infant) / Infant picture/words / - / 50 / 16 / 2 / STG, IFG, MT
Rilling, 201437 / Prisoner's Dilemma game / Numbers / 60 / 45 / 24 / 2 / Gender x OT interaction in NAcc, basal forebrain, CA, hippo, PT, Ins, PCC, Tha, OFC, CB, PH (stronger OT effect in male vs. female)
Eckstein, 201438 / Montreal Imaging stress task / Arithmetic numbers / 60 / - / 24 / 2 / Precu, PCC, ACC
Scheele, 201439 / Pleasantness rating of touch / A male or female faces / 40 / - / 24 / 1 / Ins, OFC, Precu, cuneus, ACC to female touch; OFC to male touch; Precu, ACC to female vs. male touch
Scheele, 201440 / Arousal rating / Faces / 23 / - / 24 / 1 / ACC, MCC, Precu, Ins to disgust arousal
Riem, 201441 / Passive listening of infant crying / Infant cry labeled as sick or bored / - / 50 / 16 / 2 / Ins, IFG to sick infant crying; Ins IFG to bored crying;
AMY to 500 Hz crying, but to 700 Hz crying.
Fan, 201442 / Resting-State;
Montreal Imaging stress task / Arithmetic numbers / 18 / - / 24 / 1 / ACC-amygdala rest-task interaction, especially in subjects with low early life stress scores
Kanat, 201543 / Emotion detection / Angry/happy/neutral faces / 46 / - / 24 / 2 / AMY, FFG, CB, midbrain, Tha, hippo, MFG, striate, IP, CA, IFG to angry eye; AMY, Ins, dmPFC, pallidum, ITG, PT, hippo, dlPFC to happy mouth; AMY-FFG FC
Zunhammer, 201544 / Intensity/unpleasantness rating / Experimental cues / 36 / - / 32 / 1 / angular, frontal pole, postcentral with stimulation regressor;
hippo, OFC, Precu, calcarine, lingual with temperature regressor;
Preckel, 2015
Exp. 145 / Imagery of partner infidelity / Sentences / 22 / - / 24 / 1 / ventral ACC to sexual infidelity imagery
Exp. 245 / Moral/non-moral dilemma / Stories / 48 / - / 24 / 2 / ACC, PCC, PreCu, MCC, OFC to moral vs. non-moral judgment
Eckstein, 201546 / Fear Conditioning extinction / Faces/houses / 62 / - / 24 / 2 / mid-PFC, mPFC to early fear extinction; AMY to early and later extinction; AMY-PreCu, PFC-PCC FC to later vs. early extinction
Hu, 201547 / Reinforcement learning task / Smiling/angry faces or cartoon faces / 15 / - / 24 / 1 / AMY, hippo, PH, PT during social feedback; FC between AMY and Ins, CA
Bos, 201548 / Empathy for pain / Painful/non-painful black or white hand / 54 / - / 24 / 2 / SII, MCC, Ins to empathy for other’s pain (Black + White hands)
Gregory, 201549 / One-back matching task / Cry/smile infant, sexual photos / - / 59 / 24 / 2 / VTA to crying infant and sexual images; no OT effect to smiling infant
Feng, 201550
Fan, 201551
Kanat, in press52 / Gender judgment on eyes / Happy/fearful eyes / 43 / - / 24 / 2 / AMY, olfactory cortex, SMA, ACC, paracentral, MT to fear vs. happy eyes
Kumar, in press53 / Resting-State / - / 15 / - / 24 / 1 / the degree centrality of Precu; Precu-AMY FC
Feng, in press54 / Prisoner's Dilemma game / Numbers / 104 / 100 / 24 / 2 / Gender x OT interaction in CA, PT, dmPFC (stronger OT effect in male vs. female)
Chen, in press55
Note:
Column 2 - RMET= Read mind in the eyes test;
Column 4, 5 – Male/Female: SAD = Social anxiety disorder; ASD = Autism spectrum disorder; D = Depression; H = Healthy volunteers; BP = Border line personality disorder;
Column 7 - Design: 1 = Oxytocin vs. Placebo sessions, within-subject design; 2 = Oxytocin vs. Placebo groups, between-subject design;
Column 8 –STG=superior temporal gyrus; IFG=inferior frontal gyrus; SFG=superior frontal gyrus; MFG=middle frontal gyrus; ACC=anterior cingulate cortex; AMY=amygdala; mPFC=medial prefrontal cortex; SMA=supplementary motor area; SPL=superior parietal lobe; VC=visual cortex;FFG=fusiform gyrus; ITG=inferior temporal; TP=temporal pole; MCC=mid-cingulate cortex; PT=putamen; PreCu=precuneus; NAcc=Nucleus accumbens; PCC=posterior cingulate cortex; IPL=inferior parietal lobe; dlPFC=dorsal lateral prefrontal cortex; AI= anterior insula; MTG=medial temporal gyrus; Tha=thalamus; vlPFC=ventral lateral prefrontal cortex; SC=superior colliculi; CA=caudate; CB=cerebellum; FC=functional connectivity; Ins=insula; AI=anterior insula; PH=parahippocampal; GP=globus pallidus; VTA=ventral tegmental area; MO=middle occipital; hippo=hippocampus; SII= secondary somatosensory cortex; FC=functional connectivity.
Reference
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