lynn et al 2013 cns oxy-signals poster handout · oxytocin! is! associated! with! differences! in!...

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Gender Differences in Oxytocin1associated Disrup5on of Decision Bias During Emo5on Percep5on Spencer Lynn 1* , Elizabeth Hoge 2* , Laura Fischer 2 , Lisa Feldman Barre? 1,2 , Naomi Simon 2 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 η 2 =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 η 2 =0.20, power=0.57). Oxytocin did not influence women's performance (F(1,12)=0.6, p>0.4, parLal η 2 =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 STAIHT b 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). [email protected] 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 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

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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).!

[email protected]!

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