Long-term opiate users experience pervasive social difficulties, but there has been surprisingly limited research focused on social-cognitive functioning in this population.
Aim:
The aim of this study was to investigate whether three important aspects of social cognition (facial emotion recognition, theory of mind (ToM) and rapid facial mimicry) differ between long-term opiate users and healthy controls.
Methods:
The participants were 25 long-term opiate users who were enrolled in opiate substitution programmes, and 25 healthy controls. Facial emotion recognition accuracy was indexed by responses to 60 photographs of faces depicting the six basic emotions (happiness, sadness, anger, fear, surprise and disgust). ToM was assessed using the Reading the Mind in the Eyes task, which requires participants to infer mental states of others from partial facial cues. Rapid facial mimicry was assessed by recording activity in the zygomaticus major and corrugator supercilii muscle regions while participants passively viewed images of happy and angry facial expressions.
Results:
Relative to the control group, the opiate user group exhibited deficits in both facial emotion recognition and ToM. Moreover, only control participants exhibited typical rapid facial mimicry responses to happy facial expressions.
Conclusions:
These data indicate that long-term opiate users exhibit abnormalities in three distinct areas of social-cognitive processing, pointing to the need for additional work to establish how social-cognitive functioning relates to functional outcomes in this group. Such work may ultimately inform the development of interventions aimed at improving treatment outcomes for long-term opiate users.
ArbuthnottKFrankJ (2000) Trail making test, part B as a measure of executive control: Validation using a set-switching paradigm. J Clin Exp Neuropsychol22: 518–528.
2.
Australian National Health and Medical Research Council (2009) Australian Guidelines to Reduce Health Risks from Drinking Alcohol. Canberra: NHMRC.
3.
BaileyPEHenryJD (2009) Subconscious facial expression mimicry is preserved in older adulthood. Psychol Aging24: 995–1000.
4.
BaileyPEHenryJDNangleMR (2009) Electromyographic evidence for age-related differences in the mimicry of anger. Psychol Aging24: 224–229.
5.
Baron-CohenSWheelwrightSHillJ, et al. (2001) The “Reading the Mind in the Eyes” test revised version: A study with normal adults, and adults with Asperger syndrome or high-functioning autism. J Child Psychol Psychiatry42: 241–251.
6.
BeallPMMoodyEJMcIntoshDN, et al. (2008) Rapid facial reactions to emotional facial expressions in typically developing children and children with autism spectrum disorder. J Exp Child Psychol101: 206–223.
7.
BiernackiKMcLennanSNTerrettG, et al. (2016) Decision-making ability in current and past users of opiates: A meta-analysis. Neurosci Biobehav Rev71: 342–351.
8.
BiernackiKTerrettGMcLennanSN, et al. (2018) Decision-making, somatic markers and emotion processing in opiate users. Psychopharmacology (Berl)235: 223–232.
9.
BlairR (2003) Facial expressions, their communicatory functions and neuro–cognitive substrates. Philos Trans R Soc Lond B Biol Sci358: 561–572.
10.
BrightPJaldowEKopelmanMD (2002) The national adult reading test as a measure of premorbid intelligence: A comparison with estimates derived from demographic variables. J Int Neuropsychol Soc8: 847–854.
11.
BucknerRLCarrollDC (2007) Self-projection and the brain. Trends Cogn Sci11: 49–57.
12.
BurgessPWShalliceT (1997) The Hayling and Brixton Tests. Bury St, Edmunds: Thames Valley Test Company.
13.
CarrLIacoboniMDubeauMC, et al. (2003) Neural mechanisms of empathy in humans: A relay from neural systems for imitation to limbic areas. Proc Natl Acad Sci U S A100: 5497–5502.
14.
CoxGComiskeyC (2007) Characteristics of opiate users presenting for a new treatment episode: Baseline data from the national drug treatment outcome study in Ireland (ROSIE). Drug-Educ Prev Polic14: 217–230.
15.
CraigAD (2002) How do you feel? Interoception: The sense of the physiological condition of the body. Nat Rev Neurosci3: 655–666.
16.
CraparoGGoriADell’AeraS, et al. (2016) Impaired emotion recognition is linked to alexithymia in heroin addicts. PeerJ4: e1864.
17.
Dan-GlauserESGrossJJ (2011) The temporal dynamics of two response-focused forms of emotion regulation: Experiential, expressive, and autonomic consequences. Psychophysiology48: 1309–1322.
18.
DarkeS (1998) Self-report among injecting drug users: A review. Drug and Alcohol Dependence51: 253–263.
19.
DarkeSHallW (1995) Levels and correlates of polydrug use among heroin users and regular amphetamine users. Drug Alcohol Depend39: 231–235.
20.
DarkeSRossJ (2002) Suicide among heroin users: Rates, risk factors and methods. Addiction97: 1383–1394.
21.
DarkeSWodakAHallW, et al. (1992) Prevalence and predictors of psychopathology among opioid users. Addiction87: 771–776.
22.
De LucaC (2006) Electromyography. In: WebsterJG (ed.) Encyclopedia of Medical Devices and Instrumentation. 2nd ed.Hoboken, NJ: Wiley Publisher, pp. 98–109.
23.
De MaeyerJVanderplasschenWBroekaertE (2010) Quality of life among opiate-dependent individuals: A review of the literature. Int J Drug Policy21: 364–380.
24.
DecetyJMeyerM (2008) From emotion resonance to empathic understanding: A social developmental neuroscience account. Dev Psychopathol20: 1053–1080.
25.
DegenhardtLWhitefordHAFerrariAJ, et al. (2013) Global burden of disease attributable to illicit drug use and dependence: Findings from the Global Burden of Disease Study 2010. Lancet382: 1564–1574.
26.
Di MartinoAShehzadZKellyC, et al. (2009) Relationship between cingulo-insular functional connectivity and autistic traits in neurotypical adults. Am J Psychiatry166: 891–899.
27.
DimbergUPettersonM (2000) Facial reactions to happy and angry facial expressions: Evidence for right hemisphere dominance. Psychophysiology37: 693–696.
ErscheKDClarkLLondonM, et al. (2006) Profile of executive and memory function associated with amphetamine and opiate dependence. Neuropsychopharmacology31: 1036–1047.
32.
FettAKViechtbauerWPennDL, et al. (2011) The relationship between neurocognition and social cognition with functional outcomes in schizophrenia: A meta-analysis. Neurosci Biobehav Rev35: 573–588.
33.
GandolpheMCLecluyseBTriquetC, et al. (2018) Mind reading abilities in opiate-dependent patients: An exploratory study. Compr Psychiatry83: 46–52.
34.
GaravanH (2010) Insula and drug cravings. Brain Struct Funct214: 593–601.
35.
Gunther MoorBOp de MacksZAGüroğluB, et al. (2011) Neurodevelopmental changes of reading the mind in the eyes. Soc Cogn Affect Neurosci7: 44–52.
36.
HavassyBEHallSMWassermanDA (1991) Social support and relapse: Commonalities among alcoholics, opiate users, and cigarette smokers. Addict Behav16: 235–246.
37.
HeiligMEpsteinDHNaderMA, et al. (2016) Time to connect: Bringing social context into addiction neuroscience. Nat Rev Neurosci17: 592–599.
38.
HenryJDVon HippelWMolenberghsP, et al. (2016) Clinical assessment of social cognitive function in neurological disorders. Nat Rev Neurol12: 28–39.
39.
HessUBlaisonCDandeneauS (2017) The impact of rewards on empathic accuracy and emotional mimicry. Motiv Emot41: 107–112.
40.
HessUFischerA (2014) Emotional mimicry: Why and when we mimic emotions. Trends Cogn Sci8: 45–57.
41.
JanssensMLatasterTSimonsC, et al. (2012) Emotion recognition in psychosis: No evidence for an association with real world social functioning. Schizophr Res142: 116–121.
42.
JonesJDMogaliSComerSD (2012) Polydrug abuse: A review of opioid and benzodiazepine combination use. Drug Alcohol Depend125: 8–18.
43.
KarowAVertheinUKrauszM, et al. (2008) Association of personality disorders, family conflicts and treatment with quality of life in opiate addiction. Eur Addict Res14: 38–46.
44.
KornreichCFoisyMLPhilippotP, et al. (2003) Impaired emotional facial expression recognition in alcoholics, opiate dependence subjects, methadone maintained subjects and mixed alcohol-opiate antecedents subjects compared with normal controls. Psychiatry Res119: 251–260.
45.
KornreichCPhilippotPFoisyML, et al. (2002) Impaired emotional facial expression recognition is associated with interpersonal problems in alcoholism. Alcohol Alcohol37: 394–400.
46.
LeriFBruneauJStewartJ (2002) Understanding polydrug use: Review of heroin and cocaine co-use. Addiction98: 7–22.
47.
LikowskiKUMühlbergerAGerdesA, et al. (2012) Facial mimicry and the mirror neuron system: Simultaneous acquisition of facial electromyography and functional magnetic resonance imaging. Front Hum Neurosci6: 214.
48.
LundqvistLO (1995) Facial EMG reactions to facial expressions: A case of facial emotional contagion?Scand J Psychol36: 130–141.
49.
MadduxJFDesmondDP (1984) Heroin addicts and nonaddicted brothers. Am J Drug Alcohol Abuse10: 237–248.
50.
MartinLClairJDavisP, et al. (2006) Enhanced recognition of facial expressions of disgust in opiate users receiving maintenance treatment. Addiction101: 1598–1605.
51.
McDonaldSDarkeSKayeS, et al. (2013) Deficits in social perception in opioid maintenance patients, abstinent opioid users and non-opioid users. Addiction108: 566–574.
52.
MillerGAChapmanJP (2001) Misunderstanding analysis of covariance. J Abnorm Psychol110: 40–48.
53.
MillerMABershadAKde WitH (2015) Drug effects on responses to emotional facial expressions: Recent findings. Behav Pharmacol26: 571–579.
54.
NaqviNHGaznickNTranelD, et al. (2014) The insula: A critical neural substrate for craving and drug seeking under conflict and risk. Ann N Y Acad Sci1316: 53–70.
55.
NelsonHE (1982) National Adult Reading Test (NART): Test Manual. Windsor: NFER-Nelson.
56.
NielsenL (2002) The simulation of emotion experience: On the emotional foundations of theory of mind. Phenomenol Cogn Sci1: 255–286.
57.
NummenmaaLHirvonenJParkkolaR, et al. (2008) Is emotional contagion special? An fMRI study on neural systems for affective and cognitive empathy. Neuroimage43: 571–580.
58.
PedderDJTerrettGBaileyPE, et al. (2016) Reduced facial reactivity as a contributor to preserved emotion regulation in older adults. Psychol Aging31: 114–125.
59.
PremackDWoodruffG (2010) Does the chimpanzee have a theory of mind?Behav Brain Sci1: 515–526.
60.
SchurzMRaduaJAichhornM, et al. (2014) Fractionating theory of mind: A meta-analysis of functional brain imaging studies. Neurosci Biobehav Rev42: 9–34.
61.
Shamay-TsoorySGAharon-PeretzJPerryD (2009) Two systems for empathy: A double dissociation between emotional and cognitive empathy in inferior frontal gyrus versus ventromedial prefrontal lesions. Brain132: 617–627.
62.
SingerTCritchleyHDPreuschoffK (2009) A common role of insula in feelings, empathy and uncertainty. Trends Cogn Sci13: 334–340.
63.
SingerTSeymourBDohertyJ, et al. (2004) Empathy for pain involves the affective but not sensory components of pain. Science303: 1157–1162.
64.
Sonnby–BorgströmM (2002) Automatic mimicry reactions as related to differences in emotional empathy. Scand J Psychol43: 433–443.
65.
StraussEShermanEMSpreenO (2006) A Compendium of Neuropsychological Tests: Administration, Norms, and Commentary. New York, NY: Oxford University Press.
66.
TabachnickBGFidellLS (2013) Using Multivariate Statistics. Boston: Pearson.
67.
TassinaryLGCacioppoJTVanmanEJ (2007) The skeletomotor system: Surface electromyography. In: CacioppoJTTassinaryLGBerntsonGG (eds) Handbook of Psychophysiology. New York, NY: Cambridge University Press, pp. 267–299.
68.
TeessonMMarelCDarkeS, et al. (2017) Trajectories of heroin use: 10–11-year findings from the Australian Treatment Outcome Study. Addiction112: 1056–1068.
69.
VarcinKJBaileyPEHenryJD (2010) Empathic deficits in schizophrenia: The potential role of rapid facial mimicry. J Int Neuropsychol Soc16: 621–629.
70.
von HippelCHenryJDTerrettG, et al. (2017) Stereotype threat and social function in opioid substitution therapy patients. Br J Clin Psychol56: 160–171.
71.
WangPWLinHCLiuGC, et al. (2016) Abnormal interhemispheric resting state functional connectivity of the insula in heroin users under methadone maintenance treatment. Psychiatry Res Neuroimaging255: 9–14.
72.
WollmanSCAlhassoonOMHallMG, et al. (2017) Gray matter abnormalities in opioid-dependent patients: A neuroimaging meta-analysis. Am J Drug Alcohol Abuse43: 505–517.
73.
WollmanSCAlhassoonOMSternMJ, et al. (2015) White matter abnormalities in long-term heroin users: a preliminary neuroimaging meta-analysis. Am J Drug Alcohol Abuse41: 133–138.
74.
YoungAWRowlandDCalderAJ, et al. (1997) Facial expression megamix: Tests of dimensional and category accounts of emotion recognition. Cognition63: 271–313.
75.
ZakiJDavisJIOchsnerKN (2012) Overlapping activity in anterior insula during interoception and emotional experience. Neuroimage62: 493–499.
76.
ZakiJOchsnerKN (2012) The neuroscience of empathy: Progress, pitfalls and promise. Nat Neurosci15: 675–680.
77.
ZigmondASSnaithRP (1983) The hospital anxiety and depression scale. Acta Psychiatr Scand67: 361–370.
78.
ZwickJCWolkensteinL (2017) Facial emotion recognition, theory of mind and the role of facial mimicry in depression. J Affect Disord210: 90–99.
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