Deficits in recognizing female facial expressions related to social network in cocaine-addicted men

1. Introduction

The emotional toll of drug addiction, which includes relationship break-ups and breaks with family ties that even lead to social exclusion, remains immeasurable. Whilst much research has been focussed on understanding the effects of drugs to curtail further use, relatively less is known how chronic drug use affect social functioning and how this knowledge could be used improve psychosocial interventions. For example, accumulating evidence indicates impairments in recognising emotional facial expressions (Ersche et al., 2015; Kuypers et al., 2015; Morgan and Marshall, 2013; Verdejo-García and Bechara, 2009; Kemmis et al., 2007) and deficits in social cognition, including perspective-taking and social decision-making (Quednow, 2017; Romero-Martínez and Moya-Albiol, 2015; Preller et al., 2014). As facial expressions reflect the emotional state of others, enabling us to adapt our behaviour appropriately to other people’s need, failure to recognise facial affect has been shown to be predictive of a pattern of social cognitive deficits (Trubanova et al., 2016; Corden et al., 2006). Specifically, failure to recognise negative emotions, such as fear, have been linked with an inability to inhibit socially inappropriate behaviours (Blair, 1995) and may create difficulties maintaining interpersonal relationships. It is thus conceivable that such deficits contribute to the difficulties frequently reported by chronic cocaine users such as maintaining healthy and rewarding relationships (Pachado et al., 2018).

Recognition of emotional expressions is largely affected by social influences such as biases towards one’s own gender (Wright and Sladden, 2003), ethnicity and culture (Lee et al., 2008; Rehnman and Herlitz, 2006). Gender-specific effects in emotion recognition have to the best of our knowledge not been investigated in cocaine addiction, although it may have far reaching consequences on drug users’ social lives. We therefore sought to first replicate previous findings showing facial affect recognition deficits in cocaine-addicted men and subsequently investigate the influence of facial gender. We hypothesised that men with chronic cocaine use show deficits in facial affect recognition, specifically in female faces. We further hypothesised that participants’ ability in recognising emotional expressions of others is associated with social aspects of their lives.

2. Methods

A total of eighty-nine male volunteers, with a mean age of 40.3 years (s.d. ± 10.7), were recruited via adverts in the local region and by word-of-mouth. Forty-five males were not seeking treatment for their cocaine use and have been using cocaine for an average of 13.2 years. Participants were assessed using the SCID for the DSM-IV-TR (Spitzer et al., 2002) and diagnoses were then followed up with DSM-5 (American Psychiatric Association, 2013) criteria for cocaine use disorder, subsequently referred to as CUD. The remaining forty-four men were healthy and without a personal and family history of drug abuse. All CUD men were active users of cocaine, as verified by a cocaine-positive urine sample prior to testing which has a detection window for cocaine of 2–3 days; urine samples provided by control participants were negative. Prior to testing, the absence of withdrawal and acute intoxication were checked. All participants were also breathalysed prior to testing to ensure no alcohol intoxication and completed the National Adult Reading Test (NART; Nelson and Willison, 1991) to estimate verbal intelligence and the Depression, Anxiety and Stress Scale (DASS-21; Lovibond and Lovibond, 1995) to assess affective states. The Multidimensional Scale of Perceived Social Support (MSPSS; Zimet et al., 1988), the Community Integration Questionnaire (CIQ-II; Sander et al., 1999) and the Social Provisions Scale (SPS; Cutrona and Russell, 1987) were used to evaluate the quality of participants’ social networks. Ninety-one percent of both groups reported being heterosexual; subsequent exclusion of non-heterosexual participants did not change the results. Whist the majority of CUD participants reported being single (82 %) and 18 % reported being divorced or separated, only 43 % of control participants reported being single, 9 % divorced or separated; the rest of the control group was married (47 %). Further details can be found in the supplemental material. The protocol was approved by the Psychological Research Ethics Committee.

We first verified participants’ ability to perceptually discriminate faces using the Benton Facial Recognition Test (Benton et al., 1983) and identified three CUD participants with severe difficulties, who were subsequently excluded from further analysis.

3. Results

As shown in Table 1, the two groups were well-matched for age but differed significantly with regard to verbal IQ, current emotional state, social support, social provisions and community integration. As differences in IQ were not correlated with task performance in CUD participants, they were not included in the analysis.

Results, depicted in Fig. 1, showed that CUD participants required significantly greater intensities to recognise facial emotion expressions [F(1,84) = 9.095,p = 0.003,η_p² = 0.10)]. Moreover, the group-by-gender interaction [F(1,84) = 5.76,p = 0.019,η_p² = 0.06)] revealed that CUD participants required significantly greater intensities to recognise emotional female faces [F(1,84) = 13.42,p = 0.001,η_p² = 0.14)] but did not differ from controls in their ability to recognise emotional male faces [F(1,84) = 1.61,p = 0.208,η_p² = 0.02)].

Multivariate analyses further revealed that CUD participants exhibited specific impairments in recognising happiness [F(1,84) = 7.90,p = 0.018,η_p² = 0.09)], fearfulness [F(1,84) = 6.15,p = 0.015,ηp² = 0.07)] and disgust in female faces [F(1,84) = 9.13,p = 0.003,η_p² = 0.10)], whereas sadness (p = 0.477) and anger (p = 0.590) were recognised similarly to control participants. However, recognition of fearful female faces was inversely correlated with level of community integration (CIQ-II-total: r=-0.24,p = 0.026), perceived social support (MSPSS-total: r=-0.20,p = 0.007) and social provisions (SPS-total: r=-0.24,p = 0.022). When further co-varying for DASS-21 scores, recognition of fearful female faces remained correlated with level of community integration (CIQ-II-total: r=-0.21,p = 0.05) and perceived social support (MSPSS-total: r=-0.25,p = 0.022) with a trend towards social provisions (SPS-total: r=-0.20, p = 0.077). However, we found that task performance was not associated with duration of cocaine use (r=-0.09,p = 0.53), age of onset of cocaine use (r=-0.06,p = 0.69), or the compulsive pattern of cocaine use, as reflected by the obsessive-compulsive drug use (OCDUS) score (r = 0.22,p = 0.31).

4. Discussion

Here we provide novel insights into facial affect recognition impairments in cocaine-addicted men by examining the effects of gender and their association with social aspects of participants’ lives. In line with previous studies (Ersche et al., 2015; Kuypers et al., 2015; Morgan and Marshall, 2013; Verdejo-García and Bechara, 2009; Kemmis et al., 2007), we showed that CUD participants exhibit deficits in facial affect recognition. In fact, these impairments were specific to female facial expressions, which were in turn, associated with participants’ level of social integration – an observation, which to best of our knowledge has not yet been reported.

Although CUD participants were significantly impaired in recognising the facial affect of others, this effect was, however, dependent upon the gender of the emotional face. Importantly, for the recognition of male facial affect, CUD participants were not measurably different from control participants across all five emotions tested, but they showed robust deficits in recognising female facial emotions. In fact, CUD participants required significantly greater intensity to detect emotions such as happy, fear and disgust in female faces compared with their non-drug using peers. Several accounts for this effect are conceivable. First, gender differences in expression of emotion is widely recognised, possibly due to an increased proneness of women to communicate nonverbally (Eagly, 1997; Eagly and Steffen, 1984). The cognitive deficits associated with CUD may present a particular disadvantage for CUD men, as they may not benefit as much from experiences with non-verbal strategies as much as women would (Thompson and Voyer, 2014). Consequently, they require greater intensity of emotional expressions to recognise emotion in female faces. Second, although both male and female faces were presented to participants, we only recruited men into the study, which means they could use their own-gender bias for 50 % of the trials. Own-gender bias describes the advantage of recognising facial expressions in faces of one’s own gender (Herlitz and Lovén, 2013). Consequently, CUD men may have benefitted more from this bias than their non-drug using peers. Future studies should use female CUD participants to further examine this possibility. Third, facial emotion recognition has been associated with the ability to empathise with others (Besel and Yuille, 2010) – an ability that has been suggested to be impaired in CUD (Preller et al., 2014). Possibly, CUD participants, who are unsure how to interpret a female facial emotional expression might not be able to compensate using empathetic intuition, and as a result, they are more likely to make wrong inferences about other people’s emotional states. It is unclear why CUD participants did not show deficits in recognising sadness or anger in female faces.

Whilst previous research has speculated about the potential neuro-biological nature of facial affect recognition impairment in CUD, the selective deficits for female facial expressions runs counter to such views and point more strongly towards social influences. Our results support the notion that the degree to which men recognise negative facial affect in women is associated with their social support, community integration, and social provisions such as guidance, attachment and perceived social support from friends and family. Social ties are strongly related to cocaine use trajectories (Hamil-Luker et al., 2004) and social support has been shown to be protective factors against current drug use (Williams and Latkin, 2007). Therefore suggesting an important role for social networks in emotion recognition ability in CUD.

Although drug addiction is known to destabilise friendships and family ties, such deficits in non-verbal communication are likely to further exacerbate existing tensions. This is in line with previous studies suggesting that problems with negative information processing have repercussion on social functioning in cocaine addiction and can predict treatment success (Forster et al., 2017; Turner et al., 2009). Indeed, drug-induced alterations in social perception may influence social behaviour (Wardle et al., 2012). Therefore, this impairment profile is more likely to reflect an interaction between vulnerability and the effect of the drug, which may also explain why we did not find any associations between cocaine-related variables such as the duration or compulsive pattern of use and task performance. The extent to which the impairment profile observed in the present study might be caused by cocaine specifically, should be tested by pharmacological studies using cocaine or methylphenidate (which is pharmacologically very similar to cocaine; Volkow et al., 1995) in healthy volunteers. Clearly, our work requires replication and research is warranted into whether specific training may help alleviate or improve social functioning in CUD patients.

The results of the present study are also consistent with a growing body of literature suggesting that negative emotions such as fear and disgust recognition are a particularly relevant for cocaine addiction (Albein-Urios et al., 2019; Ersche et al., 2015; Morgan and Marshall, 2013; Fernández-Serrano et al., 2010; Verdejo-García and Bechara, 2009; Kemmis et al., 2007). Facial expressions of these two emotions have been suggested to convey social signs of inhibition and avoidance – functions that are known to be impaired in CUD individuals (Ersche et al., 2016; Morein-Zamir and Robbins, 2015). Recognition of both fear and disgust is an adaptive function involving the ability to anticipate dangers, signal aversion and consequently trigger protective behaviours. CUD men did not exhibit complete impairment of these emotions with impairments only evident in recognising female faces. Specific deficits in fear and disgust recognition in female faces may therefore interfere with social functioning and lead to difficulties with relationships. Indeed, this was also reflected by fewer CUD participants being in a close relationship compared to controls.

We acknowledge a number of limitations of the present study such as the use of only male participants. It still remains unclear whether women with CUD would exhibit any gender biases in facial emotion recognition. Second, CUD and control participants significantly differed in IQ and emotional states, which is not unusual for this group (Buckley et al., 2001; Crum et al., 1993). Third, complementary measures such as theory of mind and empathy measures were not obtained and would be useful in elucidating the underlying processes in this observed gender bias as would neuroimaging data. Importantly, whilst facial emotion recognition has a neurological basis (Sprengelmeyer et al., 1998), neurological change is unlikely to explain a gender bias. Nor can it be explained by culture or age biases as there were no observed cultural differences between CUD and control participants, who came from the same local community and age was not significantly correlated with the outcome variables. Finally, given that our CUD sample were either single or separated, future research is needed to explore the relationship between gender biases in emotion recognition and links specifically with interpersonal relationships. This is particularly important considering that relationships are known to be stabilising factors during recovery and potential treatments should address these links.

In conclusion, the present study provides novel evidence of gender specific deficits in facial emotion recognition in CUD men. Specific impairments in recognising fear in female faces may provide a potential marker of social integration and functioning, which would be important for informing recovery interventions.

Supplementary Material