Sexual Orientation Affects Neural Responses to Subtle Social Aggression Signals.

The current series of studies are the first to examine brain responses to social aggression signals as a function of male and female sexual orientation. For the first set of studies (1a, 1b), axillary sweat had been collected from 17 heterosexual men and 17 heterosexual women aggressively responding to frustrating opponents (aggression condition) and while playing a construction game (control condition). Sweat samples were pooled according to sex and condition, and presented via a constant flow olfactometer to 17 gay and 23 heterosexual men (Study 1a), and 19 lesbian and 25 heterosexual women (Study 1b). Ongoing EEG was recorded from 61 scalp locations, chemosensory event-related potentials (CSERPs; P2, P3-1, P3-2) were analyzed, and neuronal sources calculated (low resolution electromagnetic tomography). Within the second set of studies (2a, 2b), pictures of males' and females' weak angry and neutral facial expressions were presented to 21 gay and 23 heterosexual men (Study 2a), and 19 lesbian and 26 heterosexual women (Study 2b), and ERPs (N170, P3) were analyzed. Gay men showed larger P3-1 amplitudes than heterosexual men upon presentation of male aggression sweat, accompanied by activation of the right inferior frontal gyrus (IFG, BA 10). Gay men also displayed longer N170 latencies in response to men's compared to women's angry facial expressions, while heterosexual men did not. In women, sexual orientation did not affect the processing of aggression sweat or anger expressions. Gay men showed preferential processing of chemosensory aggression signals (P3-1 amplitudes), indicating fine-tuned socioemotional sensitivity, related to activation of brain areas involved in emotion regulation (IFG). They further process the relative relevance of visual aggression signals (N170 latency). These results were in line with theories proposing a common evolutionary pathway for same-sex attraction and traits easing social integration.

Past, Present, and Future of Human Chemical Communication Research.

Although chemical signaling is an essential mode of communication in most vertebrates, it has long been viewed as having negligible effects in humans. However, a growing body of evidence shows that the sense of smell affects human behavior in social contexts ranging from affiliation and parenting to disease avoidance and social threat. This article aims to (a) introduce research on human chemical communication in the historical context of the behavioral sciences; (b) provide a balanced overview of recent advances that describe individual differences in the emission of semiochemicals and the neural mechanisms underpinning their perception, that together demonstrate communicative function; and (c) propose directions for future research toward unraveling the molecular principles involved and understanding the variability in the generation, transmission, and reception of chemical signals in increasingly ecologically valid conditions. Achieving these goals will enable us to address some important societal challenges but are within reach only with the aid of genuinely interdisciplinary approaches.

Comparing fear and anxiety chemosignals: Do they modulate facial muscle activity and facilitate identifying facial expressions?

Fear and anxiety are the most frequently studied emotional states in chemosignal research. Despite differences between these two emotional states, findings from research using fear and anxiety body odors (BOs) are often treated as part of a similar phenomenon. In this article, we examine possible similarities and differences between participants exposed to fear and anxiety BOs on 2 dependent variables commonly used in chemosignals' research: (1) the activation of facial muscles in displays of fear expressions (i.e. the medial frontalis and the corrugator supercilii); and (2) the time required to discriminate between negative emotional expressions (fear, anger, and disgust) and neutral ones. Our results show that fear (vs. rest) and anxiety (vs. exercise) BOs activate the medial frontalis, suggesting that both have a similar impact on receivers' facial muscles. However, we could not replicate previous findings regarding the influence of fear BOs in discriminating negative emotional faces from neutral ones. Two additional replication attempts failed to replicate the earlier results, indicating that the results reported in the literature with this specific paradigm should be interpreted cautiously. Suggestions for future research examining possible differences between fear and anxiety BOs are advanced.

Reading the Mind through the Nose: Mentalizing Skills Predict Olfactory Performance.

A growing body of literature suggests a close link between olfaction and social expertise. The current study examines whether mentalizing skills are related to olfactory discrimination performance. In order to assess their mentalizing ability, 21 women and 20 men completed the "Reading the Mind in the Eyes" test (RMET). Here, the participants have to infer other persons' mental state from photographs of eye regions. Odor discrimination was assessed using the "Düsseldorf Odour Discrimination Test" (DODT). The DODT consists of 15 items, each containing mixtures of four monomolecular substances. Within each item, two bottles contain the same mixing ratio, while the third contains the reversed mixing ratio. The participants had to identify the deviating odor. Women's expertise in mentalizing (RMET score) is strongly related to olfactory discrimination performance (DODT score): The better women are in mentalizing, the better their performance in olfactory discrimination (rho = 0.572, p = 0.042, Bonferroni-corrected). Men's mentalizing capability was unrelated to olfactory discrimination (rho = −0.117, p > 0.999, Bonferroni-corrected). The current results suggest that the social skill of mentalizing might underly the link between olfaction and social integration, at least in women, and are discussed with regard to the social nature of human olfaction.

You See What You Smell: Preferential Processing of Chemosensory Satiety Cues and Its Impact on Body Shape Perception.

The current study examines neural responses to satiety- and fasting-related volatiles and their effect on the processing of body shapes. Axillary sweat was sampled with cotton pads from 10 individuals after 12 h of fasting, and after having consumed a standard breakfast. Pure cotton pads served as the control. The chemosensory stimuli were presented to 20 participants (via a constant-flow olfactometer) exclusively, and additionally as context to images of overweight and underweight avatars. EEG was recorded (61 electrodes), and chemosensory (CSERPs; P1, N1, P2, P3) and visual event-related potentials (VERPs; N1, P2, P3a, P3b) were analyzed. The amplitudes of all positive CSERP components differed more strongly from cotton in response to chemosensory satiety cues as compared to fasting cues (P1: p = 0.023, P2: p = 0.083, P3: p = 0.031), paralleled by activity within the middle frontal and temporal gyrus. Overweight compared to underweight body shapes tended to elicit larger VERP P2 amplitudes (p = 0.068), and chemosensory satiety cues amplified the VERP amplitudes in response to any body shape (P2, P3a, P3b; all ps ≤ 0.017) as compared to the cotton control. The results indicate that chemosensory satiety cues transmit complex social information, overriding the processing of analogous visual input.

It's trust or risk? Chemosensory anxiety signals affect bargaining in women.

It is well documented how chemosensory anxiety signals affect the perceiver's physiology, however, much less is known about effects on overt social behavior. The aim of the present study was to investigate the effects of chemosensory anxiety signals on trust and risk behavior in men and women. Axillary sweat samples were collected from 22 men during the experience of social anxiety, and during a sport control condition. In a series of five studies, the chemosensory stimuli were presented via an olfactometer to 214 participants acting as investors in a bargaining task either in interaction with a fictitious human co-player (trust condition) or with a computer program (risk condition). It could be shown that chemosensory anxiety signals reduce trust and risk behavior in women. In men, no effects were observed. Chemosensory anxiety is discussed to be transmitted contagiously, preferentially in women.

The role of olfaction and sex-hormone status in empathy-related measures.

Reports of a female advantage in empathy-related measures suggest a role for sex hormones, although the data are inconsistent. Studies also report similar sex differences in human olfactory perception. In rodents, olfaction is involved in detecting and integrating socially relevant information and is modulated by the brain actions of estrogens. We hypothesized that olfaction may untangle the mixed evidence on the relationship between sex hormones and empathy-related measures (cognitive and affective) in humans. To test this, we examined 60 healthy participants in three sex-hormone-status groups: free-cycling women tested in cycle phases with higher 17-ß estradiol and progesterone, oral-contraceptive users (low estradiol and progesterone), and men. We assessed empathy-related measures, facial mimicry (from zygomaticus and corrugator muscle activity), and odor discrimination ability. In the empathy-related measures and facial mimicry, we did not find overall group effects or meaningful associations with salivary levels of estradiol, progesterone, or testosterone. Free-cycling women only outperformed men in the recognition of emotions from pictures of the eye region, but sex hormones were unrelated to emotion recognition performance. Oral contraceptive users showed higher scores in the affective empathy-related measure when viewing negative emotions, with no relation to hormone levels. Free-cycling women exhibited the strongest facial mimicry (viewing female, but not male protagonists), positively associated with progesterone. Finally, the groups differed in odor discrimination, with free-cycling women outperforming men. However, odor discrimination ability and empathy-related performance were not correlated. Our results support a role of sex hormones in odor perception and in empathy-related measures, to a certain extent. However, no common underlying mechanism was found.

Chemosensory communication of aggression: women's fine-tuned neural processing of male aggression signals.

The current study is the first to examine the central nervous processing of aggression chemosignals within men and women by means of chemosensory event-related potential (CSERP) analysis. Axillary sweat was collected from 17 men and 17 women participating in a competitive computer game (aggression condition) and playing a construction game (control condition). Sweat samples were pooled with reference to donor gender and condition, and presented to 23 men and 25 women via a constant flow olfactometer. Ongoing electroencephalogram was recorded from 61 scalp locations, CSERPs (P2, P3-1, P3-2) were analysed and neuronal sources calculated (low-resolution electromagnetic tomography, LORETA). Women, especially, showed larger P3-1 and P3-2 amplitudes in response to male as compared with female aggression signals (all p values < 0.01). The peak activation of this effect was related to activity within the dorsomedial prefrontal cortex (Brodmann area 8). As male aggression commonly targets physical harm, the competence of the human brain to sensitively detect male aggression signals is considered to be highly adaptive. The detection of male aggression signals seems to be of higher importance for women than for men. It is suggested that the processing of male aggression signals in women induces an immediate response selection. This article is part of the Theo Murphy meeting issue 'Olfactory communication in humans'.

[Olfactory Dysfunctions: References to Neuropsychiatric Disorders and Diagnostics]. / Störungen des Geruchssinns: Psychiatrisch-neurologische Bezüge und Diagnostik.

Past research has revealed a variety of olfactory deficits associated with psychiatric and neurodegenerative disorders. These deficits are evident in psychophysical olfactory testing as well as neurophysiological and neuroanatomical examinations. The specific type of olfactory dysfunction appears disorder specific. For example, with regard to affective disorders, the functional and anatomical overlap between olfactory and emotion-specific brain areas has been suggested as a major underlying factor for olfactory dysfunction. Based on converging evidence of changes in olfactory perception related to Major Depression, Schizophrenia, Alzheimer's and Parkinson's Disease, olfactory testing has been discussed as an important additional diagnostic marker. Hence, valid methods for objective and reliable olfactory testing as well as guidelines for the interpretation of the respective diagnostic findings are required. The aim of this review is to provide an overview of reported olfactory deficits in psychiatric and neurodegenerative disorders. In addition, a selection of olfactory tests, available in German-speaking countries, with regard to the respective disorder-related olfactory deficit in question are presented and classified. Original data regarding an empirical validation of the Düsseldorf Odour Discrimination Test in a clinical population are presented.

Parent-Reports of Sex-Typed Play Preference in Preschool Children: Relationships to 2D:4D Digit Ratio and Older Siblings' Sex.

Sex-typed play behavior shows large sex differences and seems to be affected by prenatal sex hormones. For example, a smaller, more male-typical ratio between the second and fourth digit length (2D:4D), a proposed marker for prenatal testosterone exposure, has been shown to be related to sex-typed play preference in childhood. Nevertheless, it is still being debated whether 2D:4D displays a stable sex difference throughout childhood, as there are few longitudinal studies. In the present study, children's 2D:4D was measured on both hands on four occasions from early infancy to early childhood (T1: 5 months, T2: 9 months, T3: 20 months, and T4: 40 months) providing the rare possibility to test the temporal stability of the sex difference. Parents completed the Preschool Activities Inventory at T4 and reported on the number of older brothers and sisters as a measure for socialization influences. Parents described boys as playing more masculine and less feminine than girls. Boys had smaller 2D:4D than girls at all measurements (T1-T4) and on both hands (right/left). Nevertheless, 2D:4D increased significantly from T3 to T4 in both sexes. Girls, but not boys, who were described as playing more masculine and less feminine had more masculine 2D:4D ratios at T1-T4 on both hands (except for right 2D:4D at T2 and T3) and had more older brothers and fewer older sisters. These data underline the stability of the sex difference in 2D:4D and show the importance of both biological and social influences on sex-typed play behavior.

Mu-Suppression as an Indicator of Empathic Processes in Lesbian, Gay, and Heterosexual Adults.

Self-reported empathy differs with gender and sexual orientation. The current study investigated whether mu-suppression, reflecting brain activity especially related to state empathy, also is modulated by gender and sexual orientation. Pictures of painful and non-painful actions were presented to 20 lesbians, 20 gay men, 20 heterosexual men and 20 heterosexual women, while EEG was recorded. Individual peak frequencies of mu-activity (electrodes C3, C4) were detected within the 6-11 Hz band for each participant, and mu-suppression indices were calculated. Further, verbal indicators of state empathy (pain ratings) and compassion were assessed. Only heterosexual individuals showed the typical pattern of enhanced mu-suppression in response to painful relative to non-painful pictures. Lesbian women and gay men did not show a differential mu-response. Moreover, they felt less compassion compared to heterosexual individuals. In line with this finding, the more compassion the participants reported, the stronger the mu-suppression in response to painful relative to non-painful pictures was. Pain ratings did not vary with sexual orientation. The lesser compassion reported by lesbian women and gay men is discussed as a mediator of their non-differential mu-suppression response. It is hypothesized that this pattern might relate to gay men and lesbian women tending to perceive the anonymous depicted actors as outgroup members, hence showing less compassion and reduced mu-suppression. As empathy is often related to negative feelings (empathic stress), a clear distinction between individuals to empathize with versus individuals not to emphasize with may well be an adaptive feature in same-sex oriented individuals.

Prenatal testosterone exposure is associated with delay of gratification and attention problems/overactive behavior in 3-year-old boys.

Sex differences in self-control become apparent during preschool years. Girls are better able to delay their gratification and show less attention problems and overactive behavior than boys. In this context, organizational effects of gonadal steroids affecting the neural circuitry underlying self-control could be responsible for these early sex differences. In the present study testosterone levels measured in amniotic fluid (via ultra performance liquid chromatography and tandem mass spectrometry) were used to examine the role of organizational sex hormones on self-control. One hundred and twenty-two 40-month-old children participated in a delay of gratification task (DoG task) and their parents reported on their attention problems and overactive behavior. Girls waited significantly longer for their preferred reward than boys, and significantly more girls than boys waited the maximum period of time, providing evidence for sex differences in delay of gratification. Boys that were rated as suffering from more attention problems and overactive behavior waited significantly shorter in the DoG task. Amniotic testosterone measures were reliable in boys only. Most importantly, boys who waited shorter in the DoG task and boys who were reported to suffer from more attention problems and overactive behavior had higher prenatal testosterone levels. These findings extend our knowledge concerning organizational effects of testosterone on the brain circuitry underlying self-control in boys, and are of relevance for understanding how sex differences in behavioral disorders are connected with a lack of self-control.

Empathic Cognitions Affected by Undetectable Social Chemosignals: An EEG Study on Visually Evoked Empathy for Pain in an Auditory and Chemosensory Context.

Reduction of mu activity within the EEG is an indicator of cognitive empathy and can be generated in response to visual depictions of others in pain. The current study tested whether this brain response can be modulated by an auditory and a chemosensory context. Participants observed pictures of painful and non-painful actions while pain associated and neutral exclamations were presented (Study 1, N = 30) or while chemosensory stimuli were presented via a constant flow olfactometer (Study 2, N = 22). Chemosensory stimuli were sampled on cotton pads while donors participated in a simulated job interview (stress condition) or cycled on a stationary bike (sport condition). Pure cotton was used as a control. The social chemosignals could not be detected as odors. Activity within the 8-13 Hz band at electrodes C3, C4 (mu activity) and electrodes O1, O2 (alpha-activity) was calculated using Fast-Fourier-Transformation (FFT). As expected, suppression of power in the 8-13 Hz band was stronger when painful as compared to non-painful actions were observed (Study 1, p = 0.020; Study 2, p = 0.005). In addition, as compared to the neutral auditory and chemosensory context, painful exclamations (Study 1, p = 0.039) and chemosensory stress signals (Study 2, p = 0.014) augmented mu-/alpha suppression also in response to non-painful pictures. The studies show that processing of social threat-related information is not dominated by visual information. Rather, cognitive appraisal related to empathy can be affected by painful exclamations and subthreshold chemosensory social information.

Pregnancy reduces the perception of anxiety.

In humans, stress can be contagiously transmitted via chemosignals on a subconscious level. This study investigates how pregnancy affects neural responses to anxiety chemosignals. Using cotton pads, 28 men donated axillary sweat immediately before an academic examination (anxiety sweat) and during ergometer training (control). Via a constant-flow olfactometer, samples were presented (oddball paradigm) to 12 non-pregnant (NP) women, 14 women in their first (T1), and 18 in their third (T3) trimester of pregnancy. Chemosensory event-related potentials and current source densities (CSD) were analysed (60 electrode setup). Compared to NP-women, pregnant women display diminished evaluative processing of the sweat samples (targets; P3-1/ P3-2 amplitudes) and delayed evaluative processing of the anxiety sweat (targets; P3-2 latency). T3-women show attenuated early processing (targets; N1 amplitude) compared to NP-women, and reduced evaluative processing compared to T1-women (standards; P3-2 amplitude). CSDs (P3-1/ P3-2 latency ranges) reveal that T1- and T3-women show an atypical activation distribution to anxiety sweat. Most participants were unable to detect the sweat samples (anxiety sweat: 79.5%, sport sweat 88.6%). The results demonstrate that the processing of anxiety chemosignals progressively vanishes during pregnancy. This effect is likely to occur without any cognitive control.

Sensitivity of the human mirror neuron system for abstract traces of actions: An EEG-study.

Theories of neuroaesthetics assume, that looking at traces of actions used in creating artwork (e.g. brush marks) is associated with a simulation of these actions in the observer's sensorimotor-cortex. The aim of the current study is to dissociate the activation of the sensorimotor-cortex by the observation of action traces from associated visual processes. Twenty-eight participants observed handmade graphics (acrylic paint on paper) of different complexity (line, triangle, shape of a house) and computer-generated counterparts. Central mu-activity, as an index of sensorimotor-cortex activity, and occipital alpha-activity, as an index of visual cortex activity were recorded in the 8-13Hz EEG-band. In line with the hypothesis, mu-activity at electrode C4 is sensitive for the complexity of handmade (p=0.001), but not computer-generated graphics (p>0.500). In contrast, occipital alpha-activity is sensitive for the complexity of both handmade and computer-generated graphics (p<0.001). Furthermore, the more empathic the participants rated themselves, the stronger mu-suppression was induced by handmade graphics compared to computer-generated graphics (electrode C4; r=-0.612, p=0.001). These results support the involvement of the sensorimotor-cortex in the recognition of action traces and strengthen evidence that individuals scoring high in emotional empathy feature a particularly responsive mirror neuron system.

The Impact of Stress on Odor Perception.

The olfactory system and emotional systems are highly intervened and share common neuronal structures. The current study investigates whether emotional (e.g., anger and fear) and physiological (saliva cortisol) stress responses are associated with odor identification ability and hedonic odor judgments (intensity, pleasantness, and unpleasantness). Nineteen men participated in the modified Trier Social Stress Test (TSST) and a control session (cycling on a stationary bike). The physiological arousal was similar in both sessions. In each session, participants' odor identification score was assessed using the University of Pennsylvania Smell Identification Test, and their transient mood was recorded on the dimensions of valence, arousal, anger, and anxiety. Multivariate regression analyses show that an increase of cortisol in the TSST session (as compared with the control session) is associated with better odor identification performance (ß = .491) and higher odor intensity ratings (ß = .562). However, increased anger in the TSST session (as compared with the control session) is associated with lower odor identification performance (ß = -.482). The study shows divergent effects of the emotional and the physiological stress responses, indicating that an increase of cortisol is associated with better odor identification performance, whereas increased anger is associated with poorer odor identification performance.

Chemosensory anxiety signals prime defensive behavior in prepubertal girls.

Chemosensory anxiety signals effectively prime motor responses related to withdrawal behavior, such as the startle reflex, in adult humans. As the reproductive status strongly affects the response to social chemosignals, the current study examined whether chemosensory anxiety signals would augment the startle response in prepubertal children as it does in adults. Using cotton pads, axillary sweat was collected from 28 men while waiting for an important oral examination (anxiety condition), and during ergometer training (sport control condition). Using a constant-flow olfactometer, sweat samples and pure cotton samples (cotton control) were presented to 10 prepubertal girls aged 9-13years (M=11.25, SD=1.25) for 3000ms during inhalation. White noise bursts of 102dB(A) served as startle probes, and startle responses were recorded via electromyography of the orbicularis oculi muscle. The girls showed larger startle amplitudes to probes presented in the context of chemosensory anxiety signals as compared to a context of sport control sweat (p<0.01) as well as cotton control (p<0.05). This effect was not attributable to differences in stimulus detection rates or stimulus hedonics. The results show that in prepubertal girls, similar to adults, chemosensory anxiety signals prime defensive motor behavior. This effect appears unrelated to the odorous quality of anxiety sweat, but seems to reflect a specific preparedness to respond to the underlying social alarm signal. Thus, chemosensory communication supporting individual harm protection is independent of the reproductive status in humans.

Enhanced startle responsivity 24 hours after acute stress exposure.

Cortisol release in a stressful situation can be beneficial for memory encoding and memory consolidation. Stimuli, such as odors, related to the stressful episode may successfully cue memory contents of the stress experience. The current investigation aimed at testing the potency of stress to influence startle responsivity 24 hr later and to implicitly reactivate emotional memory traces triggered by an odor involved. Participants were assigned to either a stress (Trier Social Stress Test [TSST]) or control (friendly TSST [f-TSST]) condition featuring an ambient odor. On the next day, participants underwent an auditory startle paradigm while their eyeblink reflex was recorded by an electrooculogram. Three different olfactory stimuli were delivered, one being the target odor presented the day before. Additionally, negative, positive, and pictures of the committee members were included for comparing general startle responsivity and fear-potentiated startle. Participants of the stress group demonstrated an enhanced startle response across all stimuli compared to participants of the control group. There were no specific effects with regard to the target odor. The typical fear-potentiated startle response occurred. Stressed participants tended to rate the target odor more aversive than control participants. Odor recognition memory did not differ between the groups, suggesting an implicit effect on odor valence. Our results show that acute stress exposure enhances startle responsivity 24 hr later. This effect might be caused by a shift of amygdala function causing heightened sensitivity, but lower levels of specificity. (PsycINFO Database Record

Fancy Citrus, Feel Good: Positive Judgment of Citrus Odor, but Not the Odor Itself, Is Associated with Elevated Mood during Experienced Helplessness.

Aromatherapy claims that citrus essential oils exert mood lifting effects. Controlled studies, however, have yielded inconsistent results. Notably, studies so far did not control for odor pleasantness, although pleasantness is a critical determinant of emotional responses to odors. This study investigates mood lifting effects of d-(+)-limonene, the most prominent substance in citrus essential oils, with respect to odor quality judgments. Negative mood was induced within 78 participants using a helplessness paradigm (unsolvable social discrimination task). During this task, participants were continuously (mean duration: 19.5 min) exposed to d-(+)-limonene (n = 25), vanillin (n = 26), or diethyl phthalate (n = 27). Participants described their mood (Self-Assessment-Manikin, basic emotion ratings) and judged the odors' quality (intensity, pleasantness, unpleasantness, familiarity) prior to and following the helplessness induction. The participants were in a less positive mood after the helplessness induction (p < 0.001), irrespective of the odor condition. Still, the more pleasant the participants judged the odors, the less effective the helplessness induction was in reducing happiness (p = 0.019). The results show no odor specific mood lifting effect of d-(+)-limonene, but indicate a positive effect of odor pleasantness on mood. The study highlights the necessity to evaluate odor judgments in aromatherapy research.