Observational Fear Conditioning Research Articles

A threat from within: Learning to fear by observing aversive bodily symptoms in others

Although observational fear learning has been implicated in the development of phobic-related fears, studies investigating observational learning of fear of bodily symptoms remain scarce. Therefore, the aim of the present study was to investigate whether fear in response to bodily symptoms can be acquired simply by observing a fearful reaction to provocation of aversive bodily symptoms in others. Forty healthy participants underwent an observational fear conditioning paradigm consisting of two phases. In the first phase, participants observed a demonstrator reacting to an aversive bodily symptom provocation (unconditioned stimulus or US, i.e., labored breathing) paired with one conditioned stimulus (CS+) but not with the other one (CS-, both CSs were geometric symbols presented on a screen the demonstrator was watching). In the second phase, participants were directly presented with the same conditioned stimuli, but in the absence of the US. Our results revealed enhanced conditioned fear responses in the beginning of the second phase to the CS + as compared to CS-, as indexed by greater skin conductance and subjective fear responses, as well as greater potentiation of startle eyeblink responses to the CS + as compared to the ITI. Taken together, these findings implicate that fear of bodily symptoms can be learned through observation of others, that is, without first-hand experience of bodily threat.

Learning about threat from friends and strangers is equally effective: An fMRI study on observational fear conditioning

Humans often benefit from social cues when learning about the world. For instance, learning about threats from others can save the individual from dangerous first-hand experiences. Familiarity is believed to increase the effectiveness of social learning, but it is not clear whether it plays a role in learning about threats. Using functional magnetic resonance imaging, we undertook a naturalistic approach and investigated whether there was a difference between observational fear learning from friends and strangers. Participants (observers) witnessed either their friends or strangers (demonstrators) receiving aversive (shock) stimuli paired with colored squares (observational learning stage). Subsequently, participants watched the same squares, but without receiving any shocks (direct-expression stage). We observed a similar pattern of brain activity in both groups of observers. Regions related to threat responses (amygdala, anterior insula, anterior cingulate cortex) and social perception (fusiform gyrus, posterior superior temporal sulcus) were activated during the observational phase, possibly reflecting the emotional contagion process. The anterior insula and anterior cingulate cortex were also activated during the subsequent stage, indicating the expression of learned threat. Because there were no differences between participants observing friends and strangers, we argue that social threat learning is independent of the level of familiarity with the demonstrator.

Effects of Septin-14 Gene Deletion on Adult Cognitive/Emotional Behavior.

While various septin GTPases have been reported for their physiological functions, their roles in orchestrating complex cognitive/emotional functions in adult mammals remained scarcely explored. A comprehensive behavioral test battery was administered to two sexes of 12-week-old Septin-14 (SEPT14) knockout (KO) and wild-type (WT) mice. The sexually dimorphic effects of brain SEPT14 KO on inhibitory avoidance (IA) and hippocampal mGluR5 expression were noticed with greater IA latency and elevated mGluR5 level exclusively in male KO mice. Moreover, SEPT14 KO appeared to be associated with stress-provoked anxiety increase in a stress-related navigation task regardless of animals’ sexes. While male and female WT mice demonstrated comparable cell proliferation in the dorsal and ventral hippocampal dentate gyrus (DG), both sexes of SEPT14 KO mice had increased cell proliferation in the ventral DG. Finally, male and female SEPT14 KO mice displayed dampened observational fear conditioning magnitude and learning-provoked corticosterone secretion as compared to their same-sex WT mice. These results, taken together, prompt us to conclude that male, but not female, mice lacking the Septin-14 gene may exhibit increased aversive emotion-related learning and dorsal/ventral hippocampal mGluR5 expressions. Moreover, deletion of SEPT14 may be associated with elevated ventral hippocampal DG cell proliferation and stress-provoked anxiety-like behavior, while dampening vicarious fear conditioning magnitudes.

Cognitive Reserve and Anxiety Interactions Play a Fundamental Role in the Response to the Stress

The aims of the present study were to assess the possible interaction between Cognitive Reserve (CR) and State Anxiety (SA) on adrenocortical and physiological responses in coping situations. Forty healthy, middle-aged men completed the Cognitive Reserve Scale and the State-Trait Anxiety Inventory. We used an Observational Fear Conditioning (OFC) paradigm in order to assess emotional learning and to induce stress. Electrodermal activity (EDA) and salivary cortisol concentrations were measured throughout the conditions. Our results indicate that those who indicated having higher state anxiety showed a lower capacity for learning the contingency, along with presenting higher salivary cortisol peak response following the observational fear-conditioning paradigm. The most prominent finding was the interaction between cognitive reserve and state anxiety on cortisol response to the post observational fear-conditioning paradigm. Thus, those who showed a high anxiety-state and, at the same time, a high cognitive reserve did not present an increased salivary cortisol response following the observational fear-conditioning paradigm. Given these results, we postulate that the state anxiety reported by participants, reflects emotional activation that hinders the attention needed to process and associate emotional stimuli. However, cognitive reserve has an indirect relation with conditioning, enabling better emotional learning. In this context, cognitive reserve demonstrated a protective effect on hormonal response in coping situations, when reported anxiety or emotional activation were high. These findings suggest that cognitive reserve could be used as a tool to deal with the effects of stressors in life situations, limiting development of the allostatic load.

Using a novel paradigm to examine observational fear-learning across development.

Fear-learning through observing others begins early in life. Yet, most observational fear-learning research has focused on adults. The current study used a novel developmentally appropriate observational fear conditioning paradigm to examine differences in observational fear-learning among children, adolescents, and adults. Thirty-six typically developing children, 41 typically developing adolescents, and 40 adults underwent differential observational fear conditioning followed by a direct exposure test. Skin conductance response (SCR) and self-reported fear were measured. Successful differential observational fear-learning was demonstrated in all three age groups as indexed by SCR, yet developmental differences emerged. Children showed overall higher physiological arousal during acquisition compared to adolescents and adults. Additionally, children reported less differential fear and were less successful at reporting the conditioned stimulus-unconditioned stimuluscontingency compared to adolescents and adults. Finally, adolescents tended to overgeneralize their fear compared with adults. This is the first study to compare observational fear-learning among children, adolescents, and adults. The novel task effectively induced observational fear-learning, particularly among adolescents and adults. Findings revealed developmental differences that have both theoretical and clinical implications.

Anxious behaviour in a demonstrator affects observational learning

Humans can acquire fear through the observation of others’ (learning models’) threat responses. These responses can be direct responses to aversive stimuli, or anticipatory responses to threats. Most research focuses on learning from observation of direct responses only. Here, we investigated how observational fear conditioning is influenced by a learning model’s typically anxious anticipatory responses. High anxiety individuals often display typically anxious anticipatory behaviour, such as worsened discrimination between safe and unsafe stimuli, characterized by increased threat responses to safe stimuli. We hypothesized that observation of an anxiously behaving model would worsen discriminatory learning. To this end, we developed an observational conditioning paradigm where a learning model was exposed to one safe and one unsafe stimuli. The learning model displayed anticipatory aversion to either to the unsafe stimulus only (Non-Anxious Model group) or to both the safe and unsafe stimuli (Anxious Model group) in addition to reacting directly to an aversive stimulus paired with the unsafe stimulus. Contrary to expectations, discriminatory learning was not worsened in the Anxious Model group compared to the Non-Anxious Model group. Rather, we saw more robust discriminatory learning in the Anxious Model group. The study provides a first step towards understanding the effect of other’s anticipatory responses in general and typically anxious anticipatory responses in particular, on observational fear learning.

Corticoamygdala Transfer of Socially Derived Information Gates Observational Learning

Observational learning is a powerful survival tool allowing individuals to learn about threat-predictive stimuli without directly experiencing the pairing of the predictive cue and punishment. This ability has been linked to the anterior cingulate cortex (ACC) and the basolateral amygdala (BLA). To investigate how information is encoded and transmitted through this circuit, we performed electrophysiological recordings in mice observing a demonstrator mouse undergo associative fear conditioning and found that BLA-projecting ACC (ACC→BLA) neurons preferentially encode socially derived aversive cue information. Inhibition of ACC→BLA alters real-time amygdala representation of the aversive cue during observational conditioning. Selective inhibition of the ACC→BLA projection impaired acquisition, but not expression, of observational fear conditioning. We show that information derived from observation about the aversive value of the cue is transmitted from the ACC to the BLA and that this routing of information is critically instructive for observational fear conditioning. VIDEO ABSTRACT.

Assessment of social transmission of threats in humans using observational fear conditioning.

Across the human life span, fear is often acquired indirectly by observation of the emotional expressions of others. The observational fear conditioning protocol was previously developed as a laboratory model for investigating socially acquired threat responses. This protocol serves as a suitable alternative to the widely used Pavlovian fear conditioning, in which threat responses are acquired through direct experiences. In the observational fear conditioning protocol, the participant (observer) watches a demonstrator being presented with a conditioned stimulus (CS) paired with an aversive unconditioned stimulus (US). The expression of threat learning is measured as the conditioned response (CR) expressed by the observer in the absence of the demonstrator. CRs are commonly measured as skin conductance responses, but behavioral and neural measures have also been implemented. The experimental procedure is suitable for divergent populations, can be administered by a graduate student and takes ∼40 min. Similar protocols are used in animals, emphasizing its value as a translational tool for studying socioemotional learning.

Elevated emotional contagion in a mouse model of Alzheimer\u2019s disease is associated with increased synchronization in the insula and amygdala

Emotional contagion, a primitive form of empathy, is heightened in patients with Alzheimer’s disease (AD); however, the mechanism underlying this attribute has not been thoroughly elucidated. In this study, observational fear conditioning was performed to measure emotional contagion levels in a mouse model of AD. Simultaneous recording of local field potentials in the bilateral anterior insula, basolateral amygdala, anterior cingulate cortex, and retrosplenial cortex was also conducted to investigate related brain network changes. Consistent with the results obtained with AD patients, 11-month-old AD model mice exhibited significantly higher freezing levels in observational fear conditioning, indicating elevated emotional contagion compared to age-matched wild-type mice. Furthermore, the left anterior insula and right basolateral amygdala of 11-months-old AD model mice indicated sustained increases in synchronization when they observed the suffering of conspecifics. These changes did not appear in other age groups or wild-type controls. Additionally, the amyloid plaque burden within the anterior insula was significantly correlated with the freezing levels in observational fear conditioning. Taken together, this study reveals increased and sustained network synchrony between the anterior insula and basolateral amygdala, which comprise a salience network in humans, as a potential mechanism for elevated emotional contagion in a mouse model of AD.

Post-weaning social isolation impairs observational fear conditioning

Many mammals can utilize social information to learn by observation of conspecifics (social learning). Social learning of fear is expected to be especially advantageous for survival. However, disruption of social development in early life can impair social cognition and might also be expected to disrupt social learning. Social isolation during a critical period of adolescence disrupts social development. The purpose of this study was to determine whether disruption of social development through post-weaning social isolation leads to impairments of social fear learning. Rats were reared in isolation or pair-housed from immediately post-weaning, for 3 weeks. Social fear learning in rats was acquired by observation of tone-footshock pairings administered to a conspecific. Isolation-reared rats displayed less conditioned freezing than pair-housed rats when tested the next day. This reduction of conditioned freezing was correlated with conspecific-oriented behaviors during conditioning, was measured despite similarities in demonstrator behaviors, and occurred despite a manipulation that equalized freezing during conditioning between the pair-housed and isolation-reared rats. The results could not be explained by abnormal sensitization to a repeated tone or deficits in freezing or direct fear conditioning. These results demonstrate that observational fear conditioning is impaired by social isolation, and provide a model to study impaired social affective learning. Impaired social cognition, manifested as inability to recognize or appropriately interpret social cues, is a symptom of several psychiatric disorders. Better understanding of the mechanisms of impaired social fear learning can lead to novel treatments for social cognition symptoms of psychiatric disorders.

Social deficits in the AY-9944 mouse model of atypical absence epilepsy

Atypical absence epilepsy (AAE) showing slow spike-and-wave discharges (SWD) is characterized by severely abnormal cognition and neurodevelopmental or neurological outcomes in humans. However, despite the severe behavioral outcomes in AAE, the relationship between AAE and social-behavioral dysfunctions has not defined well, either experimentally or in patients with AAE. Experimentally, AAE can be produced by administering AY-9944 (AY), a cholesterol biosynthesis inhibitor. In this study, we characterized social behavior in the AY mouse model of AAE. AAE in the mouse was induced by repeated postnatal administration of AY every 6 days from postnatal day (P) 2 to P20. AY-treated mice exhibited spontaneous, recurrent, and synchronous SWD (4–5Hz) in electroencephalographic recordings. AY-treated mice performed tasks involving sociability/social novelty preference, social interaction with a juvenile conspecific, observational fear, and resident–intruder aggression. They showed behavioral dysfunction in social interactions with a juvenile conspecific and sociability/social novelty preference tasks. They also exhibited reduced social fear learning in observational fear conditioning. Interestingly, they showed increased levels of offensive behaviors in a resident–intruder task. However, AY-treated mice displayed normal levels of anxiety in light/dark transition and the elevated plus maze tasks, and showed slightly increased locomotor activity in an open-field task. These results demonstrate social dysfunction in the AY-induced AAE model. Our study of social behavior can also provide valuable information about Lennox–Gastaut syndrome, in which AAE is a component. Thus, our findings may help to understand behavioral pathogenesis or characteristics of patients with AAE.

Emotional face processing in neurotypicals with autistic traits: Implications for the broad autism phenotype

The present study investigated emotional face processing in neurotypicals selected for autistic traits (AT). Participants (N=81), who obtained scores one standard deviation above or below average on the Autism Spectrum Quotient, were tested using observational fear conditioning (FC), a face version of the attention probe task, and the “Reading the Mind in the Eyes” test. The results indicated that high AT participants displayed enhanced observational FC, no attentional bias to fearful faces, and increased latency (but normal accuracy) to recognizing the mental state of another. To a certain extent, this pattern resembles the social–emotional phenotype that was previously described in autism spectrum disorders. Therefore, these results may contribute to the broad autism phenotype perspective.

Sex Differences in Response to an Observational Fear Conditioning Procedure

The present study evaluated sex differences in observational fear conditioning using modeled “mock” panic attacks as an unconditioned stimulus (UCS). Fifty-nine carefully prescreened healthy undergraduate participants (30 women) underwent 3 consecutive differential conditioning phases: habituation, acquisition, and extinction. It was expected that participants watching a confederate display mock panic attacks (UCS) paired with a previously neutral stimulus (CS +) would learn to respond fearfully to the CS +, but not to the CS − (i.e., a stimulus never associated with displays of panic). Women also were expected to report more distress and ratings of panic to the CS + than the CS − compared to men, but no sex differences were anticipated on autonomic indices of conditioning (i.e., electrodermal responses). Consistent with expectation, aversive conditioning was demonstrated by greater magnitude electrodermal and verbal-evaluative (e.g., subjective units of distress scale, panic ratings) responses to the CS + over the CS −, with women reporting more distress to the CS + over the CS −, but not greater autonomic conditioning, compared to men. Overall, the results support the notion that modeled panic attacks can serve as a potent UCS for both men and women. Discussion focuses on sex differences in observational fear conditioning and its relation to the clinical presentation of anxiety disorders.

Observational fear conditioning in the acquisition and extinction of attentional bias for threat: An experimental evaluation.

Anxious persons show automatic and strategic attentional biases for threatening information. Yet, the mechanisms and processes that underlie such biases remain unclear. The central aim of the present study was to elucidate the relation between observational threat learning and the acquisition and extinction of biased threat processing by integrating emotional Stroop color naming tasks within an observational differential fear conditioning procedure. Forty-three healthy female participants underwent several consecutive observational fear conditioning phases. During acquisition, participants watched a confederate displaying mock panic attacks (UCS) paired with a verbal stimulus (CS+), but not with a second nonreinforced verbal stimulus (CS-). As expected, participants showed greater magnitude electrodermal and verbal-evaluative (e.g., distress, fear) conditioned responses to the CS+ over the CS- word. Participants also demonstrated slower color-naming latencies to CS+ compared to the CS- word following acquisition and showed attenuation of this preferential processing bias for threat following extinction. Findings are discussed broadly in the context of the interplay between fear learning and processing biases for threat as observed in persons suffering from anxiety disorders.

Training vervet monkeys to avoid electric wires: Is there evidence for social learning?

Before being released into a large park enclosed by an electric fence, a wild-caught vervet group (Chlorocebus aethiops) had to learn to avoid electrified wires in a smaller cage. During this training, we observed the group continuously for 12 consecutive days to investigate if social learning was involved in the learning process. Results showed that all monkeys received an electric shock (average=2.5 shocks/individual). Most contacts with the wires occurred during the first few days of training and the vervets were never observed to come into contact with the electric fence in the 18 months after their release into the large park. This suggests that the vervets learned to avoid the electrified wires by trial-and-error learning. It is possible that local and stimulus enhancement may have played a role, but we could not carry out the necessary control experiments to quantify the role of these components. Observational conditioning of fear can be ruled out, however, because the vervets did not show fearful behavior toward the wires. Zoo Biol 24:145–151, 2005. © 2005 Wiley-Liss, Inc.

Mechanisms involved in the observational conditioning of fear.

Three experiments support the hypothesis that mechanisms involved in observational conditioning (OC) of fear are similar to those of direct classical conditioning and involve the organism attempting to detect the causal structure of its environment. Experiment 1, a correlational analysis, shows that model monkeys' fear behaviors on snake trials (unconditioned stimulus [US]) were highly correlated with observer monkeys' fear (unconditioned response) while watching the models' fear. In Experiment 2, all observers showed distress while watching the model's fear during Session 1 of OC, but only observers who could see the snake to which the model was reacting continued to show fear during subsequent OC sessions, suggesting that the model's fear is an easily habituable US. In Experiment 3, observers acquired significant fear of snakes after 1 OC session, indicating that the continued fear of those Experiment 2 observers that could see the snake may reflect their own acquired fear of snakes.

Mechanisms involved in the observational conditioning of fear.

Three experiments support the hypothesis that mechanisms involved in observational conditioning (OC) of fear are similar to those of direct classical conditioning and involve the organism attempting to detect the causal structure of its environment. Experiment 1, a correlational analysis, shows that model monkeys' fear behaviors on snake trials (unconditioned stimulus [US]) were highly correlated with observer monkeys' fear (unconditioned response) while watching the models' fear. In Experiment 2, all observers showed distress while watching the model's fear during Session 1 of OC, but only observers who could see the snake to which the model was reacting continued to show fear during subsequent OC sessions, suggesting that the model's fear is an easily habituable US. In Experiment 3, observers acquired significant fear of snakes after 1 OC session, indicating that the continued fear of those Experiment 2 observers that could see the snake may reflect their own acquired fear of snakes.

Selective associations in the observational conditioning of fear in rhesus monkeys.

Three experiments explored the issue of selective associations in the observational conditioning of fear. Experiment 1 results indicated that observer rhesus monkeys acquired a fear of snakes through watching videotapes of model monkeys behaving fearfully with snakes. In Experiment 2, observers watched edited videotapes that showed models reacting either fearfully to toy snakes and nonfearfully to artificial flowers (SN+/FL-) or vice versa (FL+/SN-). SN+/FL- observers acquired a fear of snakes but not of flowers; FL+/SN- observers did not acquire a fear of either stimulus. In Experiment 3, monkeys solved complex appetitive discriminative (PAN) problems at comparable rates regardless of whether the discriminative stimuli were the videotaped snake or the flower stimuli used in Experiment 2. Thus, monkeys appear to selectively associate snakes with fear.

Selective associations in the observational conditioning of fear in rhesus monkeys.

Selective associations in the observational conditioning of fear in rhesus monkeys.

Observational conditioning of fear to fear-relevant versus fear-irrelevant stimuli in rhesus monkeys.

Two experiments examined whether superior observational conditioning of fear occurs in observer rhesus monkeys that watch model monkeys exhibit an intense fear of fear-relevant, as compared with fear-irrelevant, stimuli. In both experiments, videotapes of model monkeys behaving fearfully were spliced so that it appeared that the models were reacting fearfully either to fear-relevant stimuli (toy snakes or a toy crocodile), or to fear-irrelevant stimuli (flowers or a toy rabbit). Observer groups watched one of four kinds of videotapes for 12 sessions. Results indicated that observers acquired a fear of fear-relevant stimuli (toy snakes and toy crocodile), but not of fear-irrelevant stimuli (flowers and toy rabbit). Implications of the present results for the preparedness theory of phobias are discussed.