Reading language of the eyes

Reading language of the eyes. Marina A. Pavlova, Arseny A. Sokolov. Neuroscience & Biobehavioral Reviews, June 25 2022, 104755. https://doi.org/10.1016/j.neubiorev.2022.104755

Highlights

• In neurotypical individuals, RMET scores are tightly correlated with other social cognition skills;

• The RMET assesses recognition of facial affect, but also relies on receptive language comprehension and memory;

• RMET performance is underwritten by the large-scale ensembles of neural networks well-outside the social brain;

• The RMET is limited in its capacity to differentiate between neuropsychiatric conditions as well as between stages and severity of a single disorder;

• Merely gender rather than neurobiological sex impacts performance on the RMET.

Abstract: The need for assessment of social skills in clinical and neurotypical populations has led to the widespread, and still increasing use of the ‘Reading the Mind in the Eyes Test’ (RMET) developed more than two decades ago by Simon Baron-Cohen and colleagues for evaluation of social cognition in autism. By analyzing most recent clinical and brain imaging data, we illuminate a set of factors decisive for using the RMET. Converging evidence indicates: (i) In neurotypical individuals, RMET scores are tightly correlated with other social skills (empathy, emotional intelligence, and body language reading); (ii) The RMET assesses recognition of facial affect, but also heavily relies on receptive language skills, semantic knowledge, and memory; (iii) RMET performance is underwritten by the large-scale ensembles of neural networks well-outside the social brain; (iv) The RMET is limited in its capacity to differentiate between neuropsychiatric conditions as well as between stages and severity of a single disorder, though it reliably distinguishes individuals with altered social cognition or elevated pathological traits from neurotypical persons; (v) Merely gender (as a social construct) rather than neurobiological sex influences performance on the RMET; (vi) RMET scores do not substantially decline in healthy aging, and they are higher with higher education level, cognitive abilities, literacy, and mental well-being; (vii) Accuracy on the RMET, and engagement of the social brain, are greater when emotions are expressed and recognized by individuals with similar cultural/ethnic background. Further research is required to better inform usage of the RMET as a tool for swift and reliable examination of social cognition. In light of comparable visual input from the RMET images and faces covered by masks due to COVID-19 regulations, the analysis is of value for keeping efficient social interaction during the current pandemic, in particular, in professional settings related to social communication.

Keywords: Reading the Mind in the Eyes Test (RMET)visual social cognitionfacial affectsocial brainbrain imagingneuropsychiatrygender and sexclinical studieshealthy aging

Sexual humor was used to distinguish between primary and secondary sexual rewards; the amygdala serves as a reward hub, especially in processing sexual humor appreciation

Differential Neural Substrates for Responding to Monetary, Sexual Humor, and Erotic Rewards. lYu-Chen Chan, Wei-Chin Hsu, Tai-LiChou. Biological Psychology, June 28 2022, 108385. https://doi.org/10.1016/j.biopsycho.2022.108385

Highlights

• Sexual humor was used to distinguish between primary and secondary sexual rewards.

• The amygdala serves as a reward hub, especially in processing sexual humor appreciation.

• Sexual versus monetary rewards have been identified in the OFC along a postero-anterior axis.

• The pOFC-amygdala coupling was found for sexual humor appreciation and erotic pleasure.

• The NAc-midbrain coupling was active for anticipation of monetary rewards.

Abstract: Sexual humor involves neural mechanisms related to both humor and sexual arousal. However, evidence on the role of the amygdala in processing sexual humor is lacking. Unlike erotic stimuli that directly involve a biological drive, sexual humor gains its value through learned associations. Processes related to responding to erotic versus monetary rewards have been identified in the lateral orbitofrontal cortex (lOFC) along a postero-anterior axis, but it is less clear whether these processes are also active during the appreciation of sexual humor. Results showed the processing of sexual humor appreciation in the amygdala. Psychophysiological interaction (PPI) analysis further identified functional connectivity in the amygdala-midbrain coupling during sexual humor versus monetary gains appreciation. The present study provides evidence demonstrating roles for the posterior OFC (pOFC) and anterior OFC (aOFC) in distinguishing between sexual (sexual humor and erotic) and non-sexual (monetary) rewards. The experience of sexual pleasure induced by erotic rewards involves phylogenetically and ontogenetically older regions in the pOFC, while the experience of receiving monetary gains involves the aOFC. This study also provides additional insights into sexual humor appreciation in the pOFC, with findings of a postero-anterior dissociation in the processing of sexual humor appreciation. PPI analysis revealed functional connectivity in the pOFC-amygdala coupling in response to both types of sexual rewards versus monetary rewards. Together, our results suggest that the amygdala serves as a reward hub, especially in processing sexual humor versus monetary gains appreciation. Functional connectivity analysis showed amygdala-midbrain and pOFC-amygdala coupling during the appreciation of sexual humor.

Keywords: fMRIsexual rewardsamygdalaorbitofrontal cortexnucleus accumbens

4. Discussion

Sexual humor involves neural mechanisms related to both humor processing and sexual arousal. The amygdala has been found to play a key role in humor. However, evidence on the role of the amygdala in processing sexual humor is unclear. Many studies have focused on humor appreciation using cartoon stimuli (Bartolo et al., 2006, Goel and Dolan, 2001, Goel and Dolan, 2007, Mobbs et al., 2003, Samson et al., 2008, Samson et al., 2009, Wild et al., 2006). Humor does more than just make people laugh; it can serve numerous social functions as a ‘social glue’ (Bartolo et al., 2021, Chan et al., 2016, Goel and Dolan, 2007). However, few studies have made use of humor as a social reward (Chan et al., 2018a).

In this study, sexual humor was used as a reward to make it possible to distinguish between sexual humor and non-humor rewards (erotic and monetary). A large body of research has shown that the amygdala plays a core role in humor appreciation (Chan et al., 2012, Chan et al., 2013, Mobbs et al., 2003, Vrticka et al., 2013). However, empirical evidence on the role of the amygdala in processing sexual humor is lacking. As predicted, our results show that sexual humor rewards involve the bilateral amygdala during the experience of amusement (Fig. 3). The amygdala showed differentially greater activation to sexual humor rewards. This is consistent with a view in which the amygdala plays a crucial role in the ‘hedonic brain’ during the appreciation of humor rewards (Chan et al., 2018a). Based on the salience theory of humor (Ruch & Hehl, 1988), the amygdala, part of the ventral salience network (SN), may be involved in focusing attention on salient sexual and humor stimuli and then integrating cognitive and affective information related to the stimuli (Beaty et al., 2015, Beaty et al., 2019, Beaty et al., 2021, Menon and Uddin, 2010).

The first aim of this study was to investigate reward-related brain activity during the consumption of sexual humor and non-humor (erotic and monetary) rewards. The segregated response to sexual humor versus erotic outcomes (HO > EO) in the left amygdala suggests a functional division in the experience of humor-related amusement, perhaps related to hedonic value representation during humor appreciation. Sexual humor involves sexual arousal and humor appreciation (Chapman and Gadfield, 1976, Ruch and Hehl, 1988), while erotic stimuli involve primarily sexual arousal (Sescousse et al., 2010). Therefore, compared to the consumption of erotic rewards, the amygdala plays a core role in “humor appreciation” during the consumption of sexual humor rewards. This is consistent with previous findings that the amygdala contributes to humor appreciation (Chan, in press, Chan et al., 2012, Chan et al., 2013, Farkas et al., 2021, Mobbs et al., 2003, Vrticka et al., 2013). Additionally, the segregated responses to sexual humor appreciation versus monetary gains (HO > MO) in the bilateral amygdala suggest a role for reward-specific regions in the experience of amusement related to sexual humor. Together, our results support a key role for the amygdala in the hedonic enjoyment of sexual humor.

Psychophysiological interaction (PPI) analysis further revealed amygdala-midbrain coupling and amygdala-ACC coupling in response to sexual humor appreciation when compared with the response to the non-reward baseline (HO > NO). The amygdala seed of the salience network showed positive correlations with another salience network (the ACC and midbrain). The results are consistent with the Freudian theory of humor and sexual arousal. Sexual humor appears to be funnier (Chan et al., 2016). The contrast between erotic rewards and sexual humor rewards (EO > HO) suggests increased biological drive supported by the functional coupling of the NAc-ACC (Fig. 5). Additionally, the contrast between sexual humor rewards and monetary rewards (HO > MO) revealed increased sexual arousal and amusement in the amygdala-midbrain coupling. The results of the present study are consistent with previous findings on amygdala-midbrain coupling for the consumption of humor versus monetary rewards (HO > MO) (Chan et al., 2018a). In sum, the appreciation of sexual humor rewards elicited sexual arousal and amusement via amygdala-midbrain connectivity.

The second aim of this study was to investigate reward-related brain activity during the consumption of sexual (sexual humor and erotic) and non-sexual (monetary) rewards. In this study, sexual humor and erotic stimuli were used as sexual rewards to make it possible to distinguish between sexual and non-sexual rewards. The lOFC is known to play a key role in encoding reward-related value, memory, and semantic processing (Sescousse et al., 2010, Zald et al., 2014). Previous studies have shown that reward value processing during the consumption of erotic versus monetary rewards in the lateral OFC (lOFC) occurs along a postero-anterior axis (Li et al., 2015, Sescousse et al., 2013). In the outcome phase, the processing of erotic pleasure has been found in phylogenetically and ontogenetically older parts of the posterior lOFC (pOFC, MNI (x y z), -30, 33, -15), while the processing of monetary gains has been found in phylogenetically more recent parts of the anterior lOFC (aOFC, -30, 51, 0) (Sescousse et al., 2010). The present study further used sexual humor rewards and found that the processing of reward value coding in the outcome phase for sexual humor appreciation versus monetary gains can be identified in the posterior lOFC (pOFC).

Visual sexual stimuli as rewards may trigger autonomic sexual arousal for humans (Putkinen et al., 2022). As predicted, processing related to hedonic experiences by reward-specific brain networks along a postero-anterior axis appears to be what is reflected in value-related lOFC activity during the outcome phase (Fig. 4). The pleasure of sexual arousal (in response to both sexual humor and erotic stimuli) revealed increased activation in the posterior part of the lOFC (pOFC), while processing for monetary gains showed increased activation in the anterior part of the lOFC (aOFC). In term of sexual rewards, sexual humor appreciation versus monetary gains (HO > MO) specifically recruited activation in the bilateral pOFC (MNI = -42, 28, -8 and MNI = 34, 30, -16), while erotic pleasure versus monetary gains (EO > MO) elicited activation in the left pOFC (-28, 30, -12). In term of non-sexual rewards, monetary versus sexual humor rewards (MO > HO) elicited greater activation in the aOFC (34, 54, -4); monetary versus erotic rewards (MO > EO) similarly elicited more aOFC activation (34, 54, -2). The postero-anterior distinction of the lOFC was shown. The more complex or abstract rewards (e.g., monetary gain or loss) showed increased activation in the aOFC, while less complex rewards (e.g., erotic or taste stimuli) showed increased activation in the pOFC (Kringelbach, 2005, Kringelbach and Rolls, 2004).

Previous studies have used happy faces (Spreckelmeyer et al., 2009), social feedback (e.g., praise or compliments) (Fussner et al., 2018), social decision making (Izuma et al., 2008), and affective touch (Korb et al., 2020) as social rewards. Humor is another type of reward that plays an important role in social relations (Chan et al., 2018a). The present study used sexual humor as a social reward. The results of the present study identified a role in sexual humor appreciation for the pOFC during the outcome phase. In contrast, previous studies have shown processing of social rewards in a similar aOFC region (Izuma et al., 2008). A possible interpretation for the results of the present study is that sexual humor rewards involve both sexual arousal and humor appreciation. This may be consistent with previous findings that the pOFC contributes to the experience of sexual arousal related to erotic rewards (Sescousse et al., 2010). Sescousse et al.’s study showed increased activation for monetary gains versus erotic pleasure in the left aOFC (-30, 51, 0) during the outcome phase (Sescousse et al., 2010). However, the present study showed activation for both monetary gains versus erotic rewards (MO > EO) and monetary gains versus sexual humor rewards (MO > HO) in the bilateral aOFC, especially increased activation in the right aOFC (MNI = 34, 54, -4 and MNI = 34, 54, -2). Future studies might further examine the neural mechanisms related to processing monetary gains in the left or right aOFC with different types of rewards.

Another interesting question relates to how to interpret differences in functional connectivity between sexual reward conditions. Our PPI analysis demonstrated the functional connectivity of the pOFC (-42, 28, -8) as a seed, showing pOFC-amygdala, pOFC-NAc, and pOFC-ACC couplings in response to sexual humor appreciation versus monetary gains (HO > MO) during the outcome phase, while the functional connectivity of the pOFC (-28, 30, -12) as a seed showed pOFC-amygdala and pOFC-ACC couplings in response to erotic pleasure versus monetary gains (EO > MO) during the outcome phase (Fig. 6). Taken together, it appears that sexual rewards elicit sexual pleasure via pOFC-amygdala and pOFC-ACC connectivity.

Our findings implicate the pOFC in sexual pleasure related to both sexual humor and erotic stimuli. Also, the hypothalamus, which plays a core role in human sexual motivation and pleasure, is known to be particularly sensitive to the presentation of visual erotic stimuli (Sescousse et al., 2013). In our study, the erotic versus monetary rewards conditions (EO > MO) revealed greater activation in the hypothalamus (-8, -6, -4) during the outcome or consumption phase. This is consistent with previous studies on sexual arousal and sexual pleasure (Karama et al., 2002, Sescousse et al., 2013).

Finally, the third aim of this study was to investigate reward-related brain activity during monetary and non-monetary (sexual humor and erotic stimuli) motivation. The present study investigated neural mechanisms for cue-triggered motivation during the anticipation phase. We used a range of monetary rewards (10 to 12 New Taiwan Dollars) for successfully completed trials and showed cumulative earnings at the end of each monetary reward trial, in order to provide immediate feedback (as in the tasks with other reward types). During the anticipation phase, as predicted, we found the most prominent modulation in response to monetary cues, indicating the NAc’s role as a ‘monetary incentive center’ (Fig. 2; Chan et al., 2018a; Knutson et al., 2001a). The present study provided additional support related to the role of the NAc in motivating responses to monetary incentives in the anticipation of monetary rewards versus sexual humor rewards (MA > HA) and monetary rewards versus erotic rewards (MA > EA). 

In termites: Ancestral sex-role plasticity facilitates the evolution of same-sex sexual behaviour

Ancestral sex-role plasticity facilitates the evolution of same-sex sexual behaviour. Nobuaki Mizumoto, Thomas Bourguignon, Nathan W. Bailey. bioRxiv Jun 22 2022. https://doi.org/10.1101/2022.06.20.496918

Abstract: Recent attempts to explain the evolutionary prevalence of same-sex sexual behaviour (SSB) have focused on the role of indiscriminate mating. However, in many cases, SSB involves plastically adjusting sex roles to achieve successful courtship or pairing. To evaluate this overlooked factor, we tested whether ancestral sex-role plasticity facilitated the evolution of SSB in the termite Reticulitermes speratus. Male termites follow females in paired tandems before mating, and movement patterns are sexually dimorphic. Adaptive same-sex tandems occur in both sexes. We show that in such cases, one partner adopts the other sexs movement patterns, resulting in behavioural dimorphism. Data-based simulations confirmed that this socially-cued plasticity contributes to pair maintenance because dimorphic movements improve reunion success upon accidental separation. Phylogenetic analysis indicated that the ancestors of modern termites lack consistent sex roles during pairing, indicating that R. speratus inherited the plasticity from the ancestor. Socio-environmental induction of ancestral behavioural potential may be of widespread importance to the evolutionary maintenance of SSB.