Beyond Fear Emotional Memory Mechanisms in the Human Brain

ABSTRACT— Neurobiological accounts of emotional memory have been derived largely from animal models investigating the encoding and retention of memories for events that signal threat. This literature has implicated the amygdala, a structure in the brain's temporal lobe, in the learning and consolidation of fear memories. Its role in fear conditioning has been confirmed, but the human amygdala also interacts with cortical regions to mediate other aspects of emotional memory. These include the encoding and consolidation of pleasant and unpleasant arousing events into long-term memory, the narrowing of focus on central emotional information, the retrieval of prior emotional events and contexts, and the subjective experience of recollection and emotional intensity during retrieval. Along with other mechanisms that do not involve the amygdala, these functions ensure that significant life events leave a lasting impression in memory.     

Anxiety-related biases in children's avoidant responses to a masked angry face

While anxious children often show escape and withdrawal behaviours towards threats, few studies have experimentally assessed avoidance. The present study examined whether children with high levels of anxiety showed more avoidant responses to a neutral conditioned cue (CS+) that was paired with an unconditioned threat stimulus (UCS), a masked angry facial expression. Thirty-six 10 and 11 year-olds participated in a task, which involved choosing between two CS card stimuli of different colours to win points. Whilst both cards awarded the same number of points, one colour was systematically paired with a masked angry face (CS+), whilst the other colour was paired with a masked neutral face (CS-). Children with higher anxiety scores had an overall tendency to choose the card associated with the neutral face, with some evidence suggesting that this tendency emerged gradually across trials. These results suggest a relationship between anxiety and stimulus-response learning for CS+-UCS associations that support behavioural avoidance.     

Fear conditioning in posttraumatic stress disorder: evidence for delayed extinction of autonomic, experiential, and behavioural responses

Aversive conditioning has been proposed as an important factor involved in the etiology of posttraumatic stress disorder (PTSD). However, it is not yet fully understood exactly which learning mechanisms are characteristic for PTSD. PTSD patients (n=36), and healthy individuals with and without trauma exposure (TE group, n=21; nTE group, n=34), underwent a differential fear conditioning experiment consisting of habituation, acquisition, and extinction phases. An electrical stimulus served as the unconditioned stimulus (US), and two neutral pictures as conditioned stimuli (CS+, paired; CS-, unpaired). Conditioned responses were quantified by skin conductance responses (SCRs), subjective ratings of CS valence and US-expectancy, and a behavioural test. In contrast to the nTE group, PTSD patients showed delayed extinction of SCRs to the CS+. Online ratings of valence and US-expectancy as well as the behavioural test confirmed this pattern. These findings point to a deficit in extinction learning and highlight the role of affective valence appraisals and cognitive biases in PTSD. In addition, there was some evidence that a subgroup of PTSD patients had difficulties in learning the CS-US contingency, thereby providing preliminary evidence of reduced discrimination learning.     

Interoceptive fear conditioning as a learning model of panic disorder: an experimental evaluation using 20% CO(2)-enriched air in a non-clinical sample

Despite the role afforded interoceptive fear conditioning in etiologic accounts of panic disorder, there are no good experimental demonstrations of such learning in humans. The aim of the present study was to evaluate the interoceptive conditioning account using 20% carbon dioxide (CO(2))-enriched air as an interoceptive conditioned stimulus (CS) (i.e., physiologically inert 5-s exposures) and unconditioned stimulus (US) (i.e., physiologically prepotent 15-s exposures). Healthy participants (N=42) were randomly assigned to one of three conditions: a CS-only, contingent CS-US pairings, or unpaired/non-contingent CS and US presentations. Electrodermal and self-report (e.g., distress, fear) served as indices of conditioned emotional responding. Results showed greater magnitude electrodermal and evaluative fear conditioning in the paired relative to the CS-only condition. The explicitly unpaired condition showed even greater electrodermal and evaluative responding during acquisition, and marked resistance to extinction. The latter results are consistent with the possibility that the unpaired procedure constituted a partial reinforcement procedure in which CO(2) onset was paired with more extended CO(2) exposure on 50% of the trials. Overall, the findings are consistent with contemporary learning theory accounts of panic.     

Second-order beliefs about intention and children's attributions of sociomoral judgment

Predicting how another person will evaluate the intention underlying an action involves consideration of second-order mental states. Children (ages 5-10 years) and college students (N=105) predicted an observer's belief about an actor's intention and evaluated the actor from both their own perspectives and the perspective of the observer. Younger children were more likely than older children and adults to attribute a belief to the observer that mismatched the actor's prior intention. Attributed beliefs about intention were more likely to match negative prior intentions than to match positive prior intentions and were also more likely to match prior intentions when the observer knew the actor's prior intention than when the observer did not know the actor's prior intention. The judgments attributed to the observer were based on the beliefs about intention attributed to the observer, showing use of second-order mental states to infer another's sociomoral judgments.     

Biphasic ERK1/2 activation in both the hippocampus and amygdala may reveal a system consolidation of contextual fear memory

There is accumulating evidences to suggest that memory consolidation in some conditions involves two waves of neuronal plastic change. Using two fear conditioning procedures in male C57BL/6J mice, we have recently shown that consolidation of the foreground contextual fear memory required two waves of ERK1/2 activation in hippocampal CA1, while consolidation of cue conditioning was only associated with the early phase of activation. The present experiment further showed that this bi-phasic pattern of ERK1/2 activation was not restricted to hippocampal CA1, but could also be observed in other fear memory-related brain areas. The unpaired conditioning procedure (context in foreground) induced two waves of ERK1/2 activation in hippocampal CA1 and CA3, as well as in the LA and BLA nuclei of the amygdala. In contrast, the paired conditioning procedure (context in background) led to a transient early phase only in hippocampal CA1 and LA. In addition, ERK1/2 phosphorylation in the hippocampus was found to correlate with that in the amygdala nuclei specifically after the unpaired procedure. Taken together, our data suggest that the observed biphasic pattern of neuronal plastic events may reflect the interplay between hippocampal and amygdala activity-dependent plasticity critical for the system consolidation of contextual fear memory.     

Second-order conditioning during a compound extinction treatment

Two conditioned taste aversion experiments with rats were conducted to establish if a target taste that had received a prior pairing with illness could be subject to second-order conditioning during extinction treatment in compound with a flavor that also received prior conditioning. In these experiments, the occurrence of second-order conditioning was indicated by protection from extinction of the aversion elicited by the target taste. This possibility, although intuitive, deserves attention because current associative models [e.g., Rescorla, R. A., & Wagner, A. R. (1972). A theory of Pavlovian conditioning: variations in the effectiveness of reinforcement and nonreinforcement. In A. H. Black & W. F. Prokasy (Eds.), Classical conditioning II: Current research and theory (pp. 64-99). New York: Appleton-Century-Crofts.] predict exactly the opposite outcome, namely, that compound extinction of two CSs should result in enhanced extinction.     

The resistance of renewal to instructions that devalue the role of contextual cues in a conditioned suppression task with humans

The renewal of extinguished conditioned behaviour appears to reflect context-dependent learning. The present research used a conditioned suppression task with humans to examine whether instructions concerning the context could influence renewal. Pairings of a conditional stimulus (CS) and unconditional stimulus (US) were made in one context, followed by extinction trials of CS alone in a second context, and test trials of CS alone upon return to the original learning context. Four experiments tested whether the renewal of conditioned suppression observed during test would be attenuated if participants were instructed that the context changes were irrelevant to the predictive relationship between the CS and US. Using a differential conditioning design, no attenuation was found when the instructions were given prior to conditioning (Experiment 1) or immediately prior to the test trials (Experiment 2). The latter result was replicated with a single-cue conditioning design and further controls for exposure to the extinction contexts (Experiment 3). The collection of on-line ratings about the relationship between the contextual changes and the predictive nature of the CS indicated that participants did attend to and believe the instructions (Experiment 4). The results point to the resistance of renewal to explicit instructions that attempt to devalue the role of the contextual cues.     

Of snakes and faces: An evolutionary perspective on the psychology of fear

Snakes and faces are unique stimuli because they are deeply grounded in evolutionarily shaped behavior systems. Snakes are the prototypical stimulus in a predatory defense system promoting escape from predators, which prepares primates for efficient processing, attentional priority, and rapid fear acquisition to snakes and other stimuli related to predation. The social submissiveness system plays a similar role on the social arena by promoting yielding to dominant individuals without jeopardizing the protection of the group. Supporting these theoretical propositions, empirical data from a research program spanning four decades demonstrate enhanced fear conditioning to snakes and threatening faces compared to neutral stimuli, as well as fast nonconscious processing of, and prioritized attention to, snakes and threatening faces. Human brain‐imaging data show that these effects are mediated by an extensive fear‐network centering on the amygdala.     

Context blocking in rat autoshaping: Sign-tracking versus goal-tracking

Prior experience of unsignaled food can interfere with subsequent acquisition by birds of autoshaped key-pecking at a signal light. This has been understood to indicate that unsignaled food results in context conditioning, which blocks subsequent learning about the keylight-food relationship. In the present experiment with rats lever insertion as the conditioned stimulus (CS) preceded sucrose delivery as the unconditioned stimulus (US). Half the rats initially received unsignaled USs in the conditioning context, while the remainder did not. Both lever-presses (sign-tracking) and magazine-entries (goal-tracking) were recorded. Under immediate reinforcement conditions, prior unsignaled US interfered with sign-tracking, but had no effect on goal-tracking. In two further groups, a trace condition prevented development of sign-tracking. In this case, prior context conditioning interfered with goal-tracking. These results suggest that interference with sign-tracking may reflect response competition, while interference with goal-tracking under trace conditions may reflect failure to acquire a CS-US association.