Nonconscious associative learning: Pavlovian conditioning of skin conductance responses to masked fear-relevant facial stimuli

We examined the possibility of nonconscious associative learning in a context of skin conductance conditioning, using emotional facial expressions as stimuli. In the first experiment, subjects were conditioned to a backwardly masked angry face that was followed by electric shock, with a masked happy face as the nonreinforced stimulus. In spite of the effectively masked conditioned stimuli, differential conditioned skin conductance responses were observed in a subsequent nonmasked extinction phase. This effect could not be attributed to differential sensitization or pseudo-conditioning. In the second experiment, the differential responding during extinction was replicated with angry but not with happy faces as conditioned stimuli. It was concluded that with fear-relevant facial expressions as the conditioned stimulus, associative learning was possible even in conditions where the subjects remained unaware of the conditioned stimulus and its relationship to the unconditioned stimulus.     

Are two threats worse than one? The effects of face race and emotional expression on fear conditioning

Facial cues of racial outgroup or anger mediate fear learning that is resistant to extinction. Whether this resistance is potentiated if fear is conditioned to angry, other race faces has not been established. Two groups of Caucasian participants were conditioned with two happy and two angry face conditional stimuli (CSs). During acquisition, one happy and one angry face were paired with an aversive unconditional stimulus whereas the second happy and angry faces were presented alone. CS face race (Caucasian, African American) was varied between groups. During habituation, electrodermal responses were larger to angry faces regardless of race and declined less to other race faces. Extinction was immediate for Caucasian happy faces, delayed for angry faces regardless of race, and slowest for happy racial outgroup faces. Combining the facial cues of other race and anger does not enhance resistance to extinction of fear.     

Conditioning with facial expressions of emotion: Effects of CS sex and age

Two experiments examined the effects of facial expressions of emotion as conditioned stimuli (CSs) on human electrodermal conditioning and on a continuous measure of expectancy of the shock unconditioned stimulus. In Experiment 1, the CS+ was a picture of a person displaying an angry face and CS? was a neutral face. For half of the subjects, the expressions were depicted by males, for the other half by females. Male subjects showed larger skin conductance responses to pictures of males than did females. The responding of female subjects was the same regardless of the sex of the person in the picture. In Experiment 2, the CS+ and CS? were pictures of an angry or a happy face. For half of the subjects, the expressions were depicted by adult males, for the other half by preadolescent males, Subjects displayed greater differentiation when an adult male depicting anger was employed as the CS+ than when a preadolescent male depicting anger was the CS+. There were no differences when an adult or a child displayed happiness.     

Hemispheric Asymmetry in Conditioning to Facial Emotional Expressions

In the present experiment, we report a right hemisphere advantage for autonomic conditioning to facial emotional expressions. Specifically, angry, but not happy, facial expressions showed significantly more resistance to extinction when presented initially to the right as compared to the left hemisphere. Slides of happy and angry faces were used as conditioned stimuli (CS+ and CS-) with shock as the unconditioned stimulus (UCS). Half of the subjects (n = 15) had the angry face as CS+ (and the happy face as CS-), the other half had the happy face as CS+ (and the angry face as CS-). During acquisition, the CSs were presented foveally. During extinction, using the Visual Half-Field (VHF) technique, half of the CS+ and CS- trials were randomly presented in the right visual half-field (initially to the left hemisphere), and half of the trials were presented in the left half-field (initially to the right hemisphere). Stimuli were presented for 210 ms during acquisition, and for 30 ms during extinction. Bilateral skin conductance responses (SCRs) were recorded. The results showed effects of acquisition only for the angry CS+ group. During extinction, there was a significant Conditioning X Half-field interaction which was due to greater SCRs to the CS+ angry face when it was presented in the left half-field. It is concluded that the present results reveal hemisphere asymmetry effects in facial emotional conditioning.     

The Effects of Directional Facial Cues on Electrodermal Conditioning to Facial Stimuli

The present two Experiments demonstrate that the orientation of angry facial expressions is a critical cue when faces serve as conditioned stimuli during aversive electrodermal conditioning. Experiment 1 demonstrated that responses conditioned to angry faces directed toward the subjects showed significant resistance to extinction whereas responses conditioned to angry faces directed away extinguished immediately during extinction. Experiment 2 was designed to investigate whether the orientation factor was effective only during extinction, i.e. whether the orientation was a performance variable, or if the observed effect originated from factors active during acquisition, i.e. if the orientation primarily influenced learning. When the orientation was shifted between the acquisition and the extinction phase, it was found that it did not matter what direction the faces had during acquisition; it was only during extinction that the faces needed to be directed toward the subjects to evoke persistent responding. These results suggest that the subjects acquired a conditioned response to the angry face regardless of its direction, but that this learning effect remained only when the angry face was directed toward the subject during extinction.     

On the resistance to extinction of fear conditioned to angry faces

The present study investigated whether, like fear conditioned to pictures of snakes and spiders, fear conditioned to angry faces resists extinction even after verbal instruction and removal of the shock electrode. Participants were trained in a differential Pavlovian fear conditioning procedure with angry face or happy face conditional stimuli (CSs). Prior to extinction, half the participants in each group were informed that no more unconditional stimuli would be presented and the shock electrode was removed. In the absence of this manipulation, participants showed resistance to extinction after training with angry face CSs, but not after training with happy face CSs. Instructed extinction and electrode removal abolished fear conditioning regardless of the emotion expressed by the CS faces. This finding suggests that fear conditioned to angry faces, like fear conditioned to racial out-group faces, is more malleable than fear conditioned to snakes and spiders.     

Facial reactions, autonomic activity and experienced emotion: a three component model of emotional conditioning

The present study was designed to evaluate whether aversively conditioned responses to facial stimuli are detectable in all three components of the emotional response system, i.e. the expressive/behavioral, the physiological/autonomic and the cognitive/experienced component of emotion. Two groups of subjects were conditioned to angry or happy facial expression stimuli using a 100 dB noise as UCS in a differential aversive conditioning paradigm. The three components of the emotional response system were measured as: Facial-EMG reactions (corrugator and zygomatic muscle regions); autonomic activity (skin conductance, SCR; SCR half recovery time, T/2; heart rate, HR); and ratings of experienced emotion. It was found that responses in all components of the emotional response system were detectable in the angry group as greater EMG and autonomic resistance to extinction and greater self-reported fear. More specifically the angry group showed a resistant conditioning effect for the facial-EMG corrugator muscle that was accompanied by resistant conditioning for SCR frequency, slower SCR recovery, resistant conditioning in HR and a higher self-reported fear than the happy group. Thus, aversive conditioning to angry facial stimuli induce a uniform negative emotional response pattern as indicated by all three components of the emotional response system. These data suggest that a negative 'affect program' triggers responses in the different emotional components. The results suggest that human subjects are biologically prepared to react with a negative emotion to angry facial stimuli.     

Identity and expression processing during classical conditioning with faces

In classical conditioning, conditioned responses (CRs) to aversively paired (CS+) relative to unpaired (CS‐) face images are often interpreted in terms of the specific individual displayed in the CS + face image having adopted an aversive emotional connotation. This interpretation requires conditioning to rely on an association between CS + face identity and the occurrence of the aversive event (UCS). Here, we tested this requirement assuming that if an association between CS + face identity and UCS occurrence is established, CRs to originally conditioned face images should transfer to novel images of same‐identity faces. Forty‐eight participants underwent MultiCS conditioning with eight neutral faces as CSs and electric shock as UCS. Central, peripheral, evaluative, and behavioral CRs signaled successful emotional learning (as reported in Pastor et al., 2015). Behavioral and EEG responses of consecutive passive viewing showed enhanced reactions to novel angry and happy expressions of previously shocked CS + versus nonshocked CS‐ identities, indicating successful CR transfer within the dimension of face identity. Investigating the nature of CR transfer, EEG revealed an interaction of identity and expression information during face processing that followed emotional congruency (i.e., stronger reactions to congruent angry CS + and happy CS‐ vs. incongruent angry CS‐ and happy CS + compounds). While correlates of transfer appeared in late and midlatency time intervals, the congruency interaction became significant within the first 100 ms of face processing. Our results suggest conditioning to rely on an association of UCS occurrence with CS + identity and point to fast dynamic interrelations between identity and expression processing.     

Current status of the anger superiority hypothesis: A meta‐analytic review of N2pc studies

Numerous investigators have tested contentions that angry faces capture early attention more completely than happy faces do in the context of other faces. However, syntheses of studies on early event‐related potentials related to the anger superiority hypothesis have yet to be conducted, particularly in relation to the N200 posterior‐contralateral (N2pc) component which provides a reliable electrophysiological index related to orienting of attention suitable for testing this hypothesis. Fifteen samples (N = 534) from 13 studies featuring the assessment of N2pc amplitudes during exposure to angry‐neutral and/or happy‐neutral facial expression arrays were included for meta‐analysis. Moderating effects of study design features and sample characteristics on effect size variability were also assessed. N2pc amplitudes elicited by affectively valenced expressions (angry and happy) were significantly more pronounced than those elicited by neutral expressions. However, the mean effect size difference between angry and happy expressions was ns. N2pc effect sizes were moderated by sample age, number of trials, and nature of facial images used (schematic vs. real) with larger effect sizes observed when samples were comparatively younger, more task trials were presented and schematic face arrays were used. N2pc results did not support anger superiority hypothesis. Instead, attentional resources allocated to angry versus happy facial expressions were similar in early stages of processing. As such, possible adaptive advantages of biases in orienting toward both anger and happy expressions warrant consideration in revisions of related theory.     

Unit responses of the secondary somatosensory cortex during defensive conditioning in cats

Unit responses in the secondary somatosensory cortex during the formation and extinction of a defensive conditioned reflex to acoustic stimulation were investigated in chronic experiments on cats. In 21 of 28 neurons tested during defensive conditioning the firing pattern changed in accordance with the character of responses to electric shock reinforcement. Two types of conditioned-reflex unit responses were distinguished: excitatory and inhibitory. Most neurons responding to the conditioned stimulus by activation did so during the first 50 msec, which was 80–100 msec before the conditioned motor response. Considerable variability of the unit responses was observed during conditioning. By the time of stabilization of the conditioned-reflex connections the unit response to the conditioned stimulus was stable in form. The pattern of extinction of the conditioned unit activity was expressed as a decrease in the discharge frequency in responses of excitatory type and disinhibition of activity in the case of inhibitory responses.Translated from Neirofiziologiya, Vol. 9, No. 3, pp. 232–238, May–June, 1977.     

Differential conditioning to facial emotional expressions: effects of hemispheric asymmetries and CS identification

Previous studies on aversive learning have suggested a right hemispheric advantage for eliciting autonomic reactions to a masked conditioned facial stimulus (CS) depicting anger. The present study investigated the effects of visual field (VF), stimulus awareness, and emotional valence of the CSs on indicators of conditioning (bilateral SCRs, HR) using a differential conditioning paradigm (N = 41). In Group 1, four different negatively valenced facial expressions (CS+) but not four positively valenced CS- were associated with an unconditioned stimulus (US, aversive vocalization, 97 dB, 3 s) during acquisition. Group 2 received a treatment reversal with positive CS+ associated with the US. In a repeated measures design, CSs were presented with or without awareness during extinction (two weeks interval, order counterbalanced). SOAs were adapted for each subject and condition prior to the experiment so that identification performance was approaching chance level. The results revealed that both negative and positive facial expressions could be aversively conditioned providing evidence for a generalization of learning in the valence dimension. During extinction, preattentive negative CS+ presented to the left VF showed a trend towards greater electrodermal and cardiac reactions. However, no such effect emerged under full awareness of the CSs. These results confirm and further specify the nature of hemispheric asymmetries in emotional associative learning.     

Postauricular and eyeblink startle responses to facial expressions

Emotional facial expressions have affective significance. Smiles, for example, are perceived as positive and responded to with increased happiness, whereas angry expressions are perceived as negative and threatening. Yet, these perceptions are modulated in part by facial morphological cues related to the sex of the expresser. The present research assessed both eyeblink startle and the postauricular reflex during happy and angry expressions by men and women. For this 14 male and 16 female undergraduates saw happy, neutral, and angry facial expressions as well as positive and negative pictures. The postauricular reflex was potentiated during happy expressions and inhibited during anger expressions; however, as expected, this pattern was more clearly found for female expressers. Conversely, the expected pattern of eyeblink startle potentiation during angry faces and inhibition during happy faces was found only for male expressers.     

Right hemisphere representation of autonomic conditioning to facial emotional expressions

In this experiment, a lateralized right hemisphere effect was found for electrodermal associative learning to facial emotional expressions. Sixty-two subjects were presented simultaneously with a slide of a happy face in the right or left visual half field (VHF) and a slide of an angry face in the opposite VHF. Four groups were formed by the combination of the two VHF positions of angry/happy faces and the administration/omission of shock unconditioned stimuli. The results showed that simultaneous presentation of the angry face to the right hemisphere and the happy face to the left hemisphere, together with shock, resulted in a strong conditioned association with the angry face and a relatively weak association with the happy face. Furthermore, simultaneous presentation of the angry face to the left hemisphere and the happy face to the right hemisphere, together with shock, resulted in a relatively weak association with both stimuli. No significant differences were found for the no-shock control groups. The present results confirm previous findings of a right hemisphere advantage for representation of associative learning.     

Effects of social anxiety and facial expression on habituation of the electrodermal orienting response.

The present research examined electrodermal orienting to happy and angry faces as a function of social anxiety and threat of shock. A preliminary study using 569 undergraduate participants developed an adequate set of normative data of social anxiety for the Willoughby questionnaire (WQ) for use in subject selection. Electrodermal activity was measured in both high and low socially anxious subjects (N = 85) during exposure to 10 presentations of an angry face intermixed with 10 presentations of a happy face. Threat of shock (no-shock, shock work-up only, and shock work-up plus threat) was also manipulated. Skin conductance responses (SCRs) which occurred within 1-4 s of stimulus onset and trials-to-habituation constituted the data of primary interest. Although trials-to-habituation did not differ between angry and happy facial expressions, SCRs were larger to the angry face than to the happy face in both high and low socially anxious subjects. No differences in SCR magnitude were found as a function of threat of shock. The implications of these results for Ohman's functional-evolutionary model of social phobia are discussed, and alternative explanations in terms of prepotency and prior learning are examined.     

Modification of N170 by different emotional expression of schematic faces

The N170 is widely regarded as a face sensitive potential, having its maximum at occipito-temporal sites, with right-hemisphere dominance. However, it is debatable whether the N170 is modulated by different emotional expressions of a face. The aim of this study was to analyze the N170 elicited by schematic happy and angry faces when the emotional expression is semantically processed. To investigate the influence of different emotional expressions of schematic faces, we used a Prime-Probe procedure with the N400 effect as an indicator for a semantic processing. Eighteen subjects were presented the German word "happiness" or "anger" followed by happy and angry faces. The word-face pair could be congruent or incongruent in emotional meaning. Subjects were instructed to compare the emotional meaning of the words and faces and to count the congruent trials. Event-related potentials were recorded from 124 sites. Congruent faces elicited a smaller negativity in the N400 time range than incongruent faces, indicating that the facial emotional expression was cognitively processed. The face sensitive N170 was most pronounced at posterior and occipital sites, and N170 amplitudes were larger following the angry as compared to the happy faces. It is concluded that different emotional expressions of schematic faces can modulate the N170.     

The perceived duration of emotional face is influenced by the gaze direction

The present research investigates the effects of gaze direction on the perceived duration of the presentation of angry and happy expressions. When the facial expression was angry, a straight gaze elongated the perceived duration of the expression compared with an averted gaze. However, there was no effect of gaze direction when the facial expression was happy. These findings indicate that the subjective estimation of time is elongated when the observer encounters a socially important survival signal, considering that an angry face with a straight gaze may be perceived as a threat requiring a fight-or-flight response.     

Emotion in motion: Facial dynamics affect infants' neural processing of emotions

Research investigating the early development of emotional processing has focused mainly on infants' perception of static facial emotional expressions, likely restricting the amount and type of information available to infants. In particular, the question of whether dynamic information in emotional facial expressions modulates infants' neural responses has been rarely investigated. The present study aimed to fill this gap by recording 7-month-olds' event-related potentials to static (Study 1) and dynamic (Study 2) happy, angry, and neutral faces. In Study 1, happy faces evoked a faster right-lateralized negative central (Nc) component compared to angry faces. In Study 2, both happy and angry faces elicited a larger right-lateralized Nc compared to neutral faces. Irrespective of stimulus dynamicity, a larger P400 to angry faces was associated with higher scores on the Negative Affect temperamental dimension. Overall, results suggest that 7-month-olds are sensitive to facial dynamics, which might play a role in shaping the neural processing of facial emotional expressions. Results also suggest that the amount of attentional resources infants allocate to angry expressions is associated to their temperamental traits. These findings represent a promising avenue for future studies exploring the neurobiological processes involved in perceiving emotional expressions using dynamic stimuli.     

Gender differences in facial reactions to facial expressions

This study explored whether males and females differ in facial muscle reactivity when exposed to facial expressions. The study also examined whether the sex of the stimulus faces differentially influences the response patterns to facial stimuli. Thus, the sex was manipulated in a 2 x 2 factorial design by exposing males and females to slides of angry and happy faces displayed by both sexes. Facial electromyographic (EMG) activity was measured from the corrugator and zygomatic muscle regions. The subjects were also required to rate the stimuli on different dimensions. The results showed that angry faces evoked increased corrugator activity whereas happy faces evoked increased zygomatic activity. As predicted, these effects were more pronounced for females, particularly for the response to happy faces. Interestingly, there were no facial EMG effects for gender of stimulus. It was further found that males and females perceived the stimuli similarly. The results are consistent with previous findings indicating that females are more facially reactive than are males.     

Slow potentials, event-related potentials, “gamma-band” activity, and motor responses during aversive conditioning in humans

We examined slow potentials, transient event-related potentials, and oscillatory-like responses in the electroencephalogram during aversive conditioning in humans, in order to determine what is happening in the neocortex when behavioral adaptations are learned. Pictures of an angry and a happy human face served as rein-forced (CS+) and unreinforced (CS-) conditioned stimu li, respectively, in one group, and either the reversed condition or two discriminably different neutral faces in two other groups (total n=48 subjects). The unconditioned stimulus (US) was intracutaneous shock delivered to the left hand 5 s after CS+ onset. The electroencephalographic (EEG) activity was recorded from Fz, Cz, Pz, C3, and C4, electromyographic (EMG) activity from bilateral forearm and corrugator muscles, and skin conductance from the right hand. During acquisition a negative slow potential developed after CS+ (not CS-), which was more pronounced when a neutral face served as CS+. Early (iCNV, initial contingent negative variation) and late (tCNV, terminal contingent negative variation) components of the slow-potential response were positively related to the magnitude of conditioned EMG responses. Differentiation of tCNV was larger when neutral faces signaled the US; iCNV persisted during extinction when a happy face served as CS+. Late-occurring event-related potentials (ERPs) elicited by the US diminished over conditioning, whereas short-latency US components and ERPs elicited by CS events did not. Fourier analysis revealed oscillatory (gamma-band) activity between 30 and 40 Hz, which persisted up to 3 s after US delivery and diminished as conditioning progressed. Our findings indicate that learning is expressed in neocortical structures at the earliest stages of conditioning. The functional roles of the three types of EEG response in learning are discussed.     

Gender differences influence brain's beta oscillatory responses in recognition of facial expressions

There are only few studies describing gender differences in recognition of facial expressions. Our study has the aim to analyze the effect of gender differences in oscillatory brain responses. Three sets of Ekman and Friesens's facial expressions (neutral, angry, and happy) were presented to 26 healthy subjects (13 men) while recording from 13 different scalp locations. Occipital beta response (15-24Hz) was significantly larger for women than for men during the presentation of face expressions. Our results demonstrate that processing of emotional face expressions clearly differs between men and women. Accordingly, the results indicate the necessity of introducing standardization between male and female subjects by means of oscillatory dynamics. In turn, this standardization may be useful for cognitive and clinical studies.