Brain asymmetry and human electrodermal conditioning

Two experiments are reviewed that demonstrate effects of brain laterality on human classical conditioning. Pictures of facial emotional expressions were used as conditioned stimuli (CSs) together with shock as unconditioned stimlus (UCS). Bilateral electrodermal responses were recorded as dependent measures. In the first experiment, one group was conditioned to an angry face, and one group to a happy face. During extinction, the face-CSs were presented to the right hemisphere on half of the trials and to the left hemisphere on the other half of the trials. Results showed that the right hemisphere was superior in showing persisting effects of learning, and especially to the angry CS+. In the second experiment, lateralized presentations of the angry and happy faces were made during acquisition, with foveal presentations during extinction. Once again, the angry face elicited greater skin conductance responses (SCRs) during extinction in the group that had this stimulus presented to the right hemisphere during acquisition. It is concluded that emotional conditioning is differentially regulated by the two hemispheres of the brain.     

Cerebral asymmetry in autonomic conditioning to facial expressions: Sex differences

In the present experiment, sex differences in hemispheric asymmetry during classical conditioning to emotional stimuli are reported. 125 subjects (62 females and 63 males) were shown a slide of a happy face in the right (or left) visual half field (VHF), and simultaneously a slide of an angry face in the left (or right) VHF. Eight groups were formed by the combination of male and female subjects; left and right VHF positions of the angry/happy faces; and the administration/omission of the shock unconditioned stimulus (UCS). Dependent measures were skin conductance responses recorded from both hands. The results during extinction showed a significant larger SCR magnitude to the shock compared to the no-shock groups only for the female subjects. CS position during conditioning was also important in revealing differential responding to either the happy or angry faces. A right hemisphere effect was found for the angry face CS for both the male and female subjects, however with a greater difference for the females.     

Brain asymmetry and autonomic conditioning: Sensitization control

In the present experiment we report effects of cerebral asymmetry, or laterality, during classical conditioning to facial emotional stimuli. Twenty-five female subjects were presented with slides of a happy face in one visual half-field (VHF), and simultaneously a slide of an angry face in the other VHF, followed by shock as the unconditioned stimulus (UCS). To control for effects of sensitization, a new stimulus, never associated with the UCS, was introduced in the extinction phase. Dependent measures were phasic heart rate responses (HR) and skin conductance responses (SCR). The HR results showed a significant right hemisphere effect for the CS-UCS association, that was not attributable to UCS sensitization. No significant effects were found for the SCRs. The basic HR finding was a right hemisphere superiority for learning of a conditioned association.     

Nonaware classical conditioning to pictorial facial stimuli in a between-groups paradigm

The present experiment investigated the effects of aware and nonaware modes of extinction in classical conditioning to facial emotional stimuli. The subjects participated in three different experimental phases. In the first (habituation) phase they were presented with a 500 ms angry face. In the second (acquisition) phase, for half of the subjects the 500 ms face was paired with an aversive noise (experimental group) while for the other half of the subjects the face and the noise presentations were separated by 6–10 s intervals (sensitization control group). In the third (extinction) phase, these two groups were further divided into two subgroups. One subgroup of both the experimental and control group had the face stimulus presented for 30 ms, and immediately masked with a neutral picture. The other two subgroups had the face presented for 500 ms with no mask. The results showed that conditioning only occurred in the experimental subgroups which was indicated by a significant difference between skin conductance responses during habituation and corresponding responses during extinction. Secondly, comparing the experimental and control groups during the extinction phase, a significant conditioning effect was observed for both the aware and nonaware masked modes of extinction for the experimental group. The results suggest that conditioned autonomic responses may be elicited in a nonaware mode.     

Nonaware classical conditioning to pictorial facial stimuli in a between-groups paradigm.

The present experiment investigated the effects of aware and nonaware modes of extinction in classical conditioning to facial emotional stimuli. The subjects participated in three different experimental phases. In the first (habituation) phase they were presented with a 500 ms angry face. In the second (acquisition) phase, for half of the subjects the 500 ms face was paired with an aversive noise (experimental group) while for the other half of the subjects the face and the noise presentations were separated by 6-10 s intervals (sensitization control group). In the third (extinction) phase, these two groups were further divided into two subgroups. One subgroup of both the experimental and control group had the face stimulus presented for 30 ms, and immediately masked with a neutral picture. The other two subgroups had the face presented for 500 ms with no mask. The results showed that conditioning only occurred in the experimental subgroups which was indicated by a significant difference between skin conductance responses during habituation and corresponding responses during extinction. Secondly, comparing the experimental and control groups during the extinction phase, a significant conditioning effect was observed for both the aware and nonaware masked modes of extinction for the experimental group. The results suggest that conditioned autonomic responses may be elicited in a nonaware mode.     

Behold the wrath: Psychophysiological responses to facial stimuli

The complex musculature of the human face has been shaped by natural selection to produce gestures that communicate information about intentions and emotional states between senders and receivers. According to the preparedness hypothesis, different facial gestures are differentially prepared by evolution to become associated with different outcomes. As attested by psychophysiological responses in Pavlovian conditioning experiments, expressions of anger and fear more easily become signals for aversive stimuli than do expression of happiness. Consistent with the evolutionary perspective, the superior conditioning to angry faces is stronger for male than for female faces, for adult than for child faces, and for faces directed toward the receiver rather than directed away. Furthermore, it appears to be primarily located in the right cerebral hemisphere. The enhanced autonomic activity to angry faces signaling electric shock is not mediated by conscious cognitive activity, but is evident also when recognition of the facial stimulus is blocked by backward masking procedures. Similarly, conditioned responses can be established to masked angry, but not to masked happy faces. Electromyographic measurement of facial muscle activity reveals a tendency for emotional facial expression to rapidly and automatically elicit its mirror image in the face of the receiver, typically accompanied by the appropriate emotional experience. The research reviewed in this paper supports the proposition that humans have been evolutionarily tuned to respond automatically to facial stimuli, and it is suggested that such early automatic reactions shape the subsequent conscious emotional processing of the stimulus.The responsibility for this paper is shared equally between the authors. The research reviewed in the paper has been supported by separate grants to both authors from the Swedish Council for Research in the Humanities and Social Sciences, The Swedish Council for the Coordination and Planning of Research, and the Bank of Sweden Tercentennial Fund.     

Unpaired shocks during extinction weaken the contextual renewal of a conditioned discrimination

Extinction is generally more fragile than conditioning, as illustrated by the contextual renewal effect. The traditional extinction procedure entails isolated presentations of the conditioned stimulus. Extinction may be boosted by adding isolated presentations of the unconditioned stimulus, as this should augment breaking the contingency between the two stimuli. In a human conditioning experiment with on-line expectancy ratings and electrodermal responding as dependent variables, 32 participants were differentially conditioned to two neutral figures using electric shock. After a change of context, one group received normal extinction treatment whereas another group received explicitly unpaired presentations of the figures and shock. At test, the two figures were presented in the original context again. For both measures, only the group that received normal extinction showed renewal of the conditioned discrimination. These results suggest that unpaired shocks during extinction strengthen the extinction learning.     

Hemispheric asymmetry and human associative learning: Interactions with attention

In a previous study (Hugdahl & Brobeck, 1986) it was shown that Pavlovian conditioning to an auditory verbal conditioned stimulus (CS) initially presented only to the left cerebral hemisphere was stronger than when the same CS was presented to the right hemisphere. This was followed up in the present study by controlling for the possibility that the effect was caused by laterally biased attention. The study was performed using the “dichotic extinction paradigm,” which consists of three different phases. During the habituation phase, the CS+ and CS- were presented binaurally and separated in time. During the acquisition phase, the CS+ was followed by a white-noise unconditioned stimulus (UCS). During the dichotic extinction phase, the CS+ and CS- were presented dichotically, i.e., simultaneous presentations on each trial. Half of the subjects had the CS+ in the right ear, and half had the CS+ in the left ear. Each group was further divided into two subgroups, with one subgroup instructed to attend only to the right ear input, and the other subgroup to attend only to the left ear input. During acquisition, larger electrodermal responses were obtained to the CS+ than to the CS-. During dichotic extinction, the CS+ right ear group showed superior resistance to extinction compared to the CS+ left ear group, with no effect of the manipulation of attention. The effect was, however, attenuated when levels of acquisition was used as covariates in an analysis of covariance. There were overall larger responses from the left hand recording.     

Fear conditioning, meaning, and belongingness: a selective association analysis

Twenty-three subjects rated the belongingness of pairs of conditionable (photographic slides) and unconditioned (e.g., shock, tone, human scream) stimuli. Forty new subjects were then classically conditioned, using rating-defined high (angry face/scream) and low (landscape/scream) belongingness pairs. Finger-pulse responses to the high-belongingness pairs showed superior acquisition and resistance to extinction. Another 40 subjects were conditioned to compound stimuli: a slide (either landscape or angry face) that was the same over trials, and a yellow or blue background that was the discriminant cue for the unconditioned stimulus (scream). When the angry face (the high-belongingness slide) was the invariant part of the compound, relatively poorer differential pulse-volume and skin-conductance conditioning was observed. Thus, depending on the task, a priori belongingness rendered stimuli selectively conditionable, either enhancing or inhibiting visceral response associations.     

Non-differential return of fear in humans after a reinstatement procedure

The present experiment investigated reinstatement of fear in humans using a differential fear conditioning preparation. In this experiment, one neutral stimulus (conditioned stimulus; CS+) was paired with an aversive stimulus (unconditioned stimulus; US) during the acquisition phase, while another neutral stimulus was not (CS−). This procedure led to a difference in responding between the CS+ and the CS− (i.e., differential conditioning). After this acquisition phase, an extinction phase followed, during which both CSs were presented without the US, resulting in a decrease in differential conditioned responding. Reinstatement refers to the return of extinguished conditioned responses due to the experience of US-only trials after the extinction phase. This phenomenon was investigated by presenting half of the participants (reinstatement group) with unpredictable USs after the extinction phase. The control group did not receive these USs after the extinction procedure. The results show that return of fear was clearly apparent after the reinstating USs. This return of fear was, however, not limited to the CS+. An increase in ‘conditioned’ responding was also observed for the control stimulus. This interesting observation will be discussed against the background of a number of recent theoretical conceptualizations of reinstatement.     

Emotional face prediction in rejection sensitive individuals: Evidence from event-related potentials

Human beings live in an uncertain world, but they continuously generate top-down predictions about emotional face information of other people around them. Although the prediction processing has repeatedly been investigated in the literature of prediction, little is known about the impact of rejection sensitive (RS) on individuals’ emotional face prediction. To this end, high and low RS participants were asked to perform an identification task of emotional faces in which target faces were shown in either an angry or happy expression while their brain responses were recorded using an event-related potential (ERP) technique. The behavioral results suggested an effect of emotional face prediction. For the P100 component, low RS participants showed longer P100 peak latencies in the left than right hemisphere when they viewed predictable emotional faces. In addition, low RS participants showed larger N170 mean amplitudes for angry compared to happy faces when they perceived unpredictable faces, but not when these faces were predictable. This presumably reflected a sensibility to angry faces in the unpredictable trails. Interestingly, high RS participants did not demonstrate such a N170 difference, suggesting that high RS participants showed a reduced sensitivity to unpredictable angry faces. Furthermore, angry faces triggered increased LPP mean amplitudes compared to happy faces, which was consistent with the results of other ERP studies examining the processing of emotional faces. Finally, we observed significant negative correlations between behavioral and ERP prediction effect, indicating one consistency between the behavioral and electrophysiological data.     

Evaluative conditioning in the picture-picture paradigm with random assignment of conditioned stimuli to unconditioned stimuli

Human participants were allocated to 1 of 3 groups. In the conditioning group, each conditioned stimulus (CS)-unconditioned stimulus (US) pair was presented 7 times during the acquisition phase. Participants who were assigned to the extinction group saw 5 additional presentations of each CS in isolation after the 7 presentations of each CS-US pair. In the latent inhibition group, the CS-only trials were presented before the CS-US trials. Overall, a significant evaluative conditioning effect was observed. This effect cannot be dismissed on the basis of the arguments developed by A. P. Field and G. C. L. Davey (1997, 1998, 1999), and the results thus provide strong evidence for the associative nature of evaluative conditioning. The results are also in line with other findings, which showed that evaluative conditioning is resistant to extinction.     

Fear relevance and diminution of unconditioned skin conductance responses.

According to Donegan and Wagner's priming model [1987], a signalled UCS will elicit a smaller UCR than an unsignalled UCS. Assuming that fear-relevant CSs are good predictors of aversive UCSs, while fear-irrelevant CSs are relatively bad predictors of aversive UCSs, the present study examined the effect of fear relevance on electrodermal UCR diminution during the acquisition phase of a single cue conditioning procedure. Four groups were studied, each of which consisted of 12 subjects. Group 1 had a fear-relevant CS (a slide of an angry face) paired with a UCS (7 mA shock), whereas group 2 had a fear-irrelevant CS (a slide of a happy face) paired with a UCS. Groups 3 and 4 had unpaired presentations of the CS and UCS and served as control groups for 1 and 2. There were 4 habituation, 8 acquisition, 4 recovery (UCS-only), and 6 extinction (CS-only) trials. While overall UCR levels were lower in the paired than in the unpaired control groups, it was also found that the size of UCR decrement and subsequent recovery was greater in the angry face CS-paired group than in the happy face CS-paired group. This finding is in line with the predictions that flow from the Donegan and Wagner model.     

Left hemisphere specialization for response to positive emotional expressions: a divided output methodology

An extensive literature credits the right hemisphere with dominance for processing emotion. Conflicting literature finds left hemisphere dominance for positive emotions. This conflict may be resolved by attending to processing stage. A divided output (bimanual) reaction time paradigm in which response hand was varied for emotion (angry; happy) in Experiments 1 and 2 and for gender (male; female) in Experiment 3 focused on response to emotion rather than perception. In Experiments 1 and 2, reaction time was shorter when right-hand responses indicated a happy face and left-hand responses an angry face, as compared to reversed assignment. This dissociation did not obtain with incidental emotion (Experiment 3). Results support the view that response preparation to positive emotional stimuli is left lateralized.     

Fear develops to the conditioned stimulus and to the context during classical eyeblink conditioning in rats

In classical eyeblink conditioning, non-specific emotional responses to the aversive shock unconditioned stimulus (US), which are presumed to coincide with the development of fear, occur early in conditioning and precede the emergence of eyeblink responses. This twoprocess learning model was examined by concurrently measuring fear and eyeblink conditioning in the freely moving rat. Freezing served as an index of fear in animals and was measured during the inter-trial intervals in the training context and during a tone conditioned stimulus (CS) presented in a novel context. Animals that received CS-US pairings exhibited elevated levels of fear to the context and CS early in training that decreased over sessions, while eyeblink conditioned responses (CRs) developed gradually during acquisition and decreased during extinction. Random CS-US presentations produced a similar pattern of fear responses to the context and CS as paired presentations despite low eyeblink CR percentages, indicating that fear responding was decreased independent of high levels of learned eyeblink responding The results of paired training were consistent with two-process models of conditioning that postulate that early emotional responding facilitates subsequent motor learning, but measures from random control animals demonstrate that partial CS-US contingencies produce decrements in fear despite low levels of eyeblink CRs. These findings suggest, a relationship between CS-US contingency and fear levels during eyeblink conditioning, and may serve to clarify further the role that fear conditioning plays in this simple paradigm.     

Fear Develops to the Conditioned Stimulus and to the Context during Classical Eyeblink Conditioning in Rats

In classical eyeblink conditioning, non-specific emotional responses to the aversive shock unconditioned stimulus (US), which are presumed to coincide with the development of fear, occur early in conditioning and precede the emergence of eyeblink responses. This two-process learning model was examined by concurrently measuring fear and eyeblink conditioning in the freely moving rat. Freezing served as an index of fear in animals and was measured during the inter-trial intervals in the training context and during a tone conditioned stimulus (CS) presented in a novel context. Animals that received CS-US pairings exhibited elevated levels of fear to the context and CS early in training that decreased over sessions, while eyeblink conditioned responses (CRs) developed gradually during acquisition and decreased during extinction. Random CS-US presentations produced a similar pattern of fear responses to the context and CS as paired presentations despite low eyeblink CR percentages, indicating that fear responding was decreased independent of high levels of learned eyeblink responding. The results of paired training were consistent with two-process models of conditioning that postulate that early emotional responding facilitates subsequent motor learning, but measures from random control animals demonstrate that partial CS-US contingencies produce decrements in fear despite low levels of eyeblink CRs. These findings suggest a relationship between CS-US contingency and fear levels during eyeblink conditioning, and may serve to clarify further the role that fear conditioning plays in this simple paradigm.     

Extinction of an emotional response in the presence of facial expressions of emotion

Previous studies (Lanzetta & Orr, 1980, 1981; Orr & Lanzetta, 1980) have demonstrated that fear facial expressions have the functional properties of conditioned excitatory stimuli, while happy expressions behave as conditioned inhibitors of emotional responses. The present study uses a summation conditioning procedure to distinguish between associative and nonassociative (selective sensitizations, attentional) interpretations of these findings. A neutral tone was first established as a conditioned excitatory CS by reinforcing tone presentations with shock. In subsequent nonreinforced test trials the excitatory tone was paired with either fear, happy, or neutral facial expressions. A tone alone and a tone/nonface slide compound were used as controls. The results indicate that phasic and tonic skin conductance responses to the tone/fear expression compound were significantly larger during extinction than for all other experimental and control groups. No significant differences were found among these latter conditions. The findings support the assumption that the excitatory characteristics of fear expressions do not depend on associative mechanisms. In the presence of fear cues, fear facial expressions intensify the emotional reaction and disrupt extinction of a previously acquired fear response. Happy facial expressions however, do not function as conditioned inhibitors in the absence of reinforcement, suggesting that the previously found inhibition was associative in nature.This research was supported by NSF grant No. 77-08926 and by funds from the Lincoln Filene Endowment to Dartmouth College.     

Classical conditioning of the nictitating membrane response of the lemon shark (Negaprion brevirostris)

An experimental group of lemon sharks received 100 daily presentations of light flash as the conditioned stimulus (CS) and electric shock as the unconditioned stimulus (US) in a classical conditioning situation. The conditioned responses (CRs) and unconditioned responses (URs) under observation consisted of extensions of the nictitating membrane. Separate control groups received either (a) no CS or US, (b) CS-alone, or (c) completely random presentations of CS and US. Few CRs occurred in the experimental group at the outset of conditioning, but the percentage of CRs during the second half of the first acquisition session exceeded 95%. Conditioning stabilized above 95% CRs during Acquisition Sessions 3 through 7. These responses could not be attributed to pseudoconditioning, sensitization, or other nonassociative factors. When the experimental group was subsequently given six CS-alone sessions, the course of extinction was gradual. Most results seemed similar to those previously obtained during classical conditioning of the nictitating membrane in rabbits.     

The role of extinction and reinstatement in attentional bias to threat: a conditioning approach

We investigated the effects of extinction and reinstatement on attentional bias to fear-conditioned signals in healthy individuals using an emotional modification of a spatial cueing paradigm. Spatial cues were emotionally modulated using differential conditioning. The CS+ was sometimes followed by an aversive electrocutaneous stimulus (UCS), whereas the CS- was never followed by the UCS. During a subsequent extinction phase no UCS was presented anymore. The reinstatement phase started with one or four unpredicted UCS-only trials for half of the participants (reinstatement group). For the other half there were no additional UCS presentations (control group). We found that attention was biased to threat signals during acquisition. This biased attention largely disappeared during extinction. During the reinstatement phase attentional bias to threat signals re-emerged in the reinstatement group, but not in the control group.     

Return of fear in a human differential conditioning paradigm caused by a stimulus change after extinction

In a human fear conditioning experiment, 32 participants were trained in a differential conditioning procedure with geometrical shapes as CS+ and CS- (four presentations each), and an electric shock as US. Measures of conditioned responding were skin conductance response (SCR) and retrospective US-expectancy ratings. For half of the participants (Generalization Group, GG), the subsequent extinction phase consisted of four nonreinforced presentations of generalization stimuli (GS+ and GS-). Participants from the Extinction control Group received an equal amount of nonreinforced presentations of the CSs. Finally, all participants were tested with the original CSs. The results from both measures clearly show an increase in the size of the discrimination upon the stimulus change after extinction in the GG. Because this pattern is not observed in the Extinction control Group, extinction performance appears to be somehow restricted to the perceptual characteristics of the extinction stimulus. Interestingly, the size of the conditioned SCR discrimination in the GG is not influenced by the stimulus change after acquisition. This observation points to a differential impact of stimulus change after acquisition vs. extinction treatment. The findings are discussed from the theoretical perspective of renewal and the clinical perspective of Return of Fear.