Gender&Differences&in&Oxytocin1associated&Disrup5on&of&Decision&Bias&During&Emo5on&Percep5on!Spencer!Lynn
1*
,!Elizabeth!Hoge2*
,!Laura!Fischer2
,!Lisa!Feldman!Barre?1,2
,!Naomi!Simon2
!
1
Psychology,!Northeastern!University;!2
Psychiatry,!Massachuse?s!General!Hospital;!*CoHfirst!authors!
• 40!parLcipants!(age:!M=44.0!±!10.32![SD]!years,!45%!women)!were!
given!30!IU!intranasal!oxytocin!(n=22,!9!women)!or!placebo!(n=18,!7!
women).!The!randomized,!doubleHblind!administraLon!occurred!70!
min!prior!to!the!task.!
• Faces! that! depicted! expressions! ranging! from! relaxed! to! strongly!
scowling! comprised! two! categories:! "angry"! (targets)! and! "not!
angry"!(foils).!SLmulus!duraLon!was!750!ms.!!
• Uncertainty! was! implemented! by! creaLng! distribuLons! of! targets!
and! foils!which! shared!exemplars.! The!distribuLons!overlapped!on!
the! perceptual! domain:! targets! were!M! =! 60! ±! 15%! (1! SD)! scowl!
intensity,!foils!were!M!=!40!±!15%!(1!SD)!scowl!intensity.!!
• Risk!was!created!by!earning!or!losing!points!for!correct!vs.!incorrect!categorizaLon!of!targets!and!foils!(i.e.,!categorizing!a!target!as!"not!
angry"!cost!more!points!than!categorizing!a!foil!as!"angry"),!with!a!
target:foil!base!rate!=!0.6!(i.e.,!60%!of!trials!were!targets).!!
• Over! 230! trials,! parLcipants! a?empted! to! earn! as!many! points! as!
they!could,!answering!the!onHscreen!prompt!"Is!this!person!angry?".!
ParLcipants!received!immediate!onHscreen!feedback!("Yes!H!that!was!
right"!or!"No!H!that!was!wrong",!points!earned!for!the!current!trial,!
and!cumulaLve!points!earned).!
The! probability! of! encountering! angry! faces! and! the! cost! of!
misidenLfying!them!as!not!angry!created!a!risky!environment!wherein!
a!bias!to!categorize!faces!as!angry!would!maximize!point!earnings.!!
We!measured! the! effect! of! oxytocin! on! perceivers'! ability! to! achieve!
opLmal!bias!in!this!environment.!!
RelaLve! to! placebo,!we& hypothesized& that& receiving& oxytocin&would&result& in& insufficient&bias&due& to&under1es5ma5ng& the&probability&of&encountering& angry& faces& and/or& under1valuing& the& cost& of& missed&detec5ons.! This! contrasts! with! the! expectaLon! that! oxytocin! should!improve!emoLon!percepLon.!
Methods&
We!found!a!significant!interacLon!of!drug!and!gender!on!response!bias!
(ANCOVA,!F(1,32)=4.1,!p<0.049,!parLal!η2
=0.11,!power=0.51),!without!
main!effects,!controlling!for!baseline!perceived!stress!(Perceived!Stress!
Scale)!and!trait!anxiety!(State!Trait!Anxiety!Index,!Trait!Total!Score)!in!
this!nonHpsychiatrically!ill!sample.!
Men& given& oxytocin& were& less& influenced& by& cost& and& base& rate,&exhibi5ng& a& less& liberal& (i.e.,& worse)& response& bias,& than&men& given&placebo!(F(1,20)=5.0,!p<0.037,!parLal!η2=0.20,!power=0.57).!!
Oxytocin!did!not! influence!women's!performance! (F(1,12)=0.6,!p>0.4,!
parLal!η2
=0.04,!power=0.11).!
Results&
Men! given! oxytocin! appeared! less! able! to! calibrate! their! emoLon!
percepLon!to!the!signal!detecLon!parameters!that!cause!bias!(payoffs,!
base!rate,!or!both).!We!suggest!that!this!impaired!risk!sensiLvity!is!the!
mechanism!underlying!oxytocin's!effect!on!"trust"!(Kosfeld!et!al!2005,!Baumgartner!et!al!2008,!Mikolajczak!et!al!2010).!
…But,! isn't! oxytocin! supposed! to! improve! social! percepLons?!Use! of!accuracy! as! a! measure! of! performance! in! most! studies! may! explain!
why! oxytocin! someLmes! appears! to! "improve"! social! percepLons:!
Accuracy!is!highest!at!neutral!bias!(c),!!no!ma?er!a!perceiver's!ability!to!
discriminate! (d').! If! oxytocin! impairs! bias! adjustment! (making! bias!
more!neutral),!then!it!will!increase!accuracy!at!the!expense!of!uLlity.!
Conclusions&
References&Baumgartner,! T.,! Heinrichs,!M.,! Vonlanthen,! A.,! Fischbacher,!U.,! Fehr,! E.! 2008.!Oxytocin!
shapes! the! neural! circuitry! of! trust! and! trust! adaptaLon! in! humans.! Neuron! 58,!
639H650.!
Di! Simplicio,! M.,! MasseyHChase,! R.,! Cowen,! P.J.,! Harmer,! C.J.! 2009.! Oxytocin! enhances!
processing! of! posiLve! versus! negaLve! emoLonal! informaLon! in! healthy! male!
volunteers.!J!Psychopharmacol!23,!241H248.!
Domes,!G,! Lischke,!A,!Berger,!C,!Grossmann,!A,!Hauenstein,!K,!Heinrichs,!M,!et!al.!2010.!
Effects! of! intranasal! oxytocin! on! emoLonal! face! processing! in! women.!
Psychoneuroendocrinology,!35,!83H93.!
FischerHShouy,! M.,! ShamayHTsoory,! S.G.,! Harari,! H.,! &! Levkovitz,! Y.! 2010.! The! effect! of!
intranasal! administraLon! of! oxytocin! on! fear! recogniLon.! Neuropsychologia,! 48,!
179H184.!
FischerHShouy,!M.,! Levkovitz,! Y.,! ShamayHTsoory,! S.G.! 2013.!Oxytocin! facilitates! accurate!
percepLon!of!compeLLon!in!men!and!kinship!in!women.!Soc!Cogn!Affect!Neurosci,!
8,!313H317.!
Guastella!A.J.,!Mitchell!P.B.,!Mathews!F.!2008.!Oxytocin!enhances!the!encoding!of!posiLve!
social!memories!in!humans.!Biol!Psychiatry,!64,!256H258.!
Kosfeld,!M.,!Heinrichs,!M.,!Zak,!P.J.,!Fischbacher,!U.,!Fehr,!E.!2005.!Oxytocin!increases!trust!
in!humans.!Nature!435,!673H676.!
Lynn,!S.!K.,!Zhang,!X.,!Barre?,!L.F.!2012.!AffecLve!state!influences!percepLon!by!affecLng!
decision!parameters!underlying!bias!and!sensiLvity.!EmoLon,!12,!726H736.!!
Marsh,! A.,! Yu,! H.,! Pine,! D.,! Blair,! R.,! 2010.! Oxytocin! improves! specific! recogniLon! of!
posiLve!facial!expressions.!Psychopharmacol!209,!225H232.!
Mikolajczak,! M.,! Gross,! J.J.,! Lane,! A.,! Corneille,! O.,! de! Timary,! P.,! Luminet,! O.,! 2010.!
Oxytocin!makes!people!trusLng,!not!gullible.!Psych!Sci!21,!1072H1074.!
Petrovic,! P.,! Kalisch,! R.,! Singer,! T.,! Dolan,! R.J.,! 2008.! Oxytocin! a?enuates! affecLve!
evaluaLons!of!condiLoned!faces!and!amygdala!acLvity.!J!Neurosci!28,!6607H6615.!
Ring!R,!Malberg!J,!PotesLo!L,!Ping!J,!Boikess!S,!Luo!B,!et!al.!2006.!AnxiolyLcHlike!acLvity!of!
oxytocin! in! male! mice:! behavioral! and! autonomic! evidence,! therapeuLc!
implicaLons.!Psychopharmacol!185:218H225.!
Singer,!T.,!Snozzi,!R.,!Bird,!G.,!Petrovic,!P.,!Silani,!G.,!Heinrichs,!M.,!Dolan,!R.J.,!2008.!Effects!
of! oxytocin! and! prosocial! behavior! on! brain! responses! to! direct! and! vicariously!
experienced!pain.!EmoLon!8,!781H791.!
Bias,&sensi5vity,&stress,&and&anxiety&scores&(M&±&1&SD)&Bias!(c)! SensiLvity!(d')! PSS
a
! STAIHTb
! n!
Oxytocin&!!!!!Male! H0.09!±!0.186! 1.02!±!0.219! !!9.2!±!3.91! 31.0!±!4.93! 13!
!!!!!Female! H0.20!±!0.179! 0.99!±!0.179! 10.9!±!5.86! 31.6!±!9.40! 9!
Placebo&!!!!!Male! H0.29!±!0.227! 1.06!±!0.362! !!8.0!±!5.55! 29.8!±!6.57! 11!
!!!!!Female! H0.15!±!0.260! 1.08!±!0.178! !!6.0!±!4.28! 26.6!±!4.08! 7!
a
PSS!(Perceived!Stress!Scale)!was!marginally!higher!in!the!oxytocin!group!than!in!the!
placebo!group!(F(1,38)=2.9,!p<0.098).!
b
STAIHT!(State!Trait!Anxiety!Index–Trait!Total)!was!significantly!correlated!with!bias!in!the!
oxytocin!group!(r=H0.44,!p<0.041)!but!not!in!the!placebo!group!(r=H0.31,!p>0.2).!
www.neu.edu/spencerlynn!
Introduc5on&Oxytocin! is! associated! with! differences! in! the! percepLon! of! and!
response!to!socially!mediated!informaLon,!including!facial!expressions.!
Although!oxytocin!is!widely!believed!to!increase!"accuracy"!of!emoLon!
percepLon,!across!studies!oxytocin's!effect!on!emoLon!percepLon!has!
been!inconsistent.!!
Happy! Angry! Neutral! Disgusted! Fearful! Sad! Surprised!
Gaustella!et!
al!2008!
YES! n.s.& n.s.&Marsh!et!al!
2010!
YES& n.s.& n.s.& n.s.& n.s.& n.s.&DiSimplicio!et!
al!2009!
n.s.& YES! YES!
FischerH
Shouy!
!et!al!2010!
n.s.& YES!
Foils!
Targets!
H2!
H1!
0!
1!
2!
3!
4!
5!
6!
7!
ULlity!
ULlity!
!0 !10 !20 !30 !40 !50 !60 !70 !80 !90 !100!
Scowl!intensity!(%)!
Foils:!What!notHangry!faces!look!like!
Targets:!What!angry!faces!look!like!
H0.40!
H0.35!
H0.30!
H0.25!
H0.20!
H0.15!
H0.10!
H0.05!
0.00!
Men! Women!
!EsLmated!!marginal!mean!bias!(c)!
(!<–!Be?er!!…!!Worse!–>!)!
Oxytocin!
Placebo!
*!
AffecLve!judgments!about!another!person!(e.g.,!Is!that!person!angry!at!
me?)! involve! interpretaLon!of!perceptual!uncertainty! (e.g.,!scowls!do!not!always!indicate!anger)!and!assessment!of!behavioral!risk!(e.g.,!the!costs!of!inferring!anger!when!it!does!not!exist!differ!from!the!costs!of!
missing!anger!when!it!does!exist).!An!account!of!these!decision!factors!
is! missing! from! studies! of! the! effects! of! oxytocin! on! emoLon!
percepLon.!
Of! relevance,! studies! of! oxytocin's! effect! on! learning! (Petrovic! et! al!
2008,! Singer! et! al! 2008)! and! decisionHmaking! (Kosfeld! et! al! 2005,!
Baumgartner!et!al!2008,!Mikolajczak!et!al!2010)!indicate!that!oxytocin!
a?enuates!risk!aversion.!!
We!used!a!uLlityHbased!signal!detecLon!approach!(Lynn!et!al!!2012)!to!
frame!emoLon!percepLon!as!a!risky,!uncertain!decision.!We!examined!
the! effects! of! oxytocin! in! an! emoLon! percepLon! task! requiring!
perceivers! to!effecLvely!account! for! risk!by!opLmizing! their! response!
bias.!
H1.5!
H1.0!
H0.5!
0.0!
0.5!
1.0!
1.5!
0.0! 1.0! 2.0! 3.0!
Bias!(c)!
SensiLvity!(d’)!
(Liberal!!!!!.!.!.!!!!ConservaLve)!
Accuracy!
0.9!
0.8!
0.7!
0.6!
0.5!
Oxytocin! may! impair! men's! ability! to! opLmally! adapt! emoLon!
percepLon! (e.g.,! judgments!of! angriness! from! faces)! to!differences! in!
risk!and!uncertainty!that!characterize!different!social!contexts.!
Our! null! finding! for! women! is! congruent! with! Domes! et! al's! (2010)!
report!of!oxytocin! influence!on!amygdala! acLvaLon! to!angry! faces! in!
men!but!not!women.!Nonetheless,!oxytocin!has!been!shown!to!affect!
women's!social!percepLon!in!other!domains!(Marsh!et!al!2010,!FischerH
Shouey!et!al!2010).!
In!anxiety!disorders,!oxytocin!might!reduce!(normalize)!overHesLmates!
of!the!base!rate!of!threat!or!reduce!(normalize)!overHesLmates!of!the!
magnitude! of! punishments! that! could! contribute! to! excessive! social!
withdrawal!or!reduced!social!approach!behaviors.!!
Because! oxytocin! also! influences! behavior! in! nonHsocial! realms! (e.g.,!
Ring! et! al! 2006),! oxytocin! pharmacotherapy! could! have! unintended!
consequences! (i.e.,! riskHprone! decisionHmaking)! while! nonetheless!
normalizing!pathological!social!interacLon.!
Presented(at(the(20th(Annual(Mee1ng(of(the(Cogni1ve(Neuroscience(Society,(13?16(April(2013,(San(Francisco,(CA(USA
