Fears born and bred: toward a more inclusive theory of fear acquisition

Alleged differences between associative and non-associative perspectives are sometimes more apparent than real. The non-associative model describes a pathway to fear that is complementary to associative pathways. It does not seek to usurp conditioning models as applied to evolutionary-neutral fear. We discuss vexing definitional issues surrounding what qualifies as a conditioning event and what characterises the non-associative pathway. Genetic findings are shown to be consistent with the non-associative model of fear. Following discussion of the relation between stress-diathesis models and the non-associative position we conclude by urging a developmental, life-course approach to the understanding of fear acquisition.     

The origins of height fear: an evaluation of neoconditioning explanations

The present research sought to establish a reliable and valid instrument for assessing the relevance of neoconditioning factors (e.g. latent inhibition, UCS inflation/revaluation, prior fear levels, prior expectancies of harm, fear and pain levels experienced during supposed learning events), in the development of human fear. Fifty-four undergraduate height-fearful students completed the new origins instrument (OQ-II), while 54 matched controls completed a modified version (OQM-II) that examined their prior experiences with heights. In general, few differences between groups were found. Height-fearful and control subjects did not differ on trait anxiety, the frequency of negative encounters with heights, the age at which these events had occurred, prior fear levels, prior expectancies of harm, or reports of UCS inflation/revaluation procedures. However, in a finding directly opposite to that expected from a conditioning account, the mean fear and pain scores reported by subjects who had experienced direct conditioning events were significantly higher in the non-fearful group than in the height-fearful group. These findings are discussed in terms of associative and non-associative models of fear.     

Dishabituation processes in height fear and dental fear: an indirect test of the non-associative model of fear acquisition

The fear dishabituation hypothesis described in the non-associative model of fear acquisition was tested in a longitudinal birth cohort study. Results were consistent with height fear and phobia dishabituation. That is, 're-emergence' of a fear of heights occurred between age 11 and 18 years among individuals who reported higher levels of non-specific stress at age 15. Interestingly, there was no evidence for dental fear dishabituation--a finding consistent with the non-associative model of fear acquisition. Strengths and weaknesses of the study were considered and the results discussed in relation to laboratory-based findings on (dis)habituation.     

The etiology of specific fears and phobias in children: a critique of the non-associative account

The non-associative account of phobic etiology assumes that a number of specific fears (e.g., fear of heights, water, spiders, strangers, and separation) have an evolutionary background and may occur in the absence of learning experiences (e.g., conditioning). By this view, these specific fears pertain to stimuli that once posed a challenge to the survival of our prehistoric ancestors. Accordingly, they would emerge spontaneously during the course of normal development and only in a minority of individuals, these specific fears would persist into adulthood. While the non-associative approach has generated interesting findings, several critical points can be raised. First, it capitalizes on negative findings, i.e., the failure to document learning experiences (e.g., conditioning, modeling) in the history of phobic children. Second, it largely ignores factors that have been found to be crucial for the acquisition of early childhood fears (e.g., the developmental level of the child, stimulus characteristics such as novelty, aversiveness, and unpredictability, and early experience with uncontrollable events). As an alternative to the non-associative account, we briefly describe a multifactorial model of childhood fears and phobias.     

The effect of amygdala lesions on conditional and unconditional vocalizations in rats

Electrolytic lesions centered on the amygdaloid central nucleus (ACe) resulted in the inability of rats to acquire a Pavlovian conditional vocalization response. Conditioning consisted of pairing a light conditional stimulus with a tailshock unconditional stimulus (US). The thresholds of three unconditional responses (URs) to tailshock were assessed prior to conditioning. These URs are organized at spinal (spinal motor reflexes), medullary (vocalizations during shock), and forebrain (vocalization afterdischarges, VADs) levels of the neuraxis. Compared to sham-lesioned controls, rats with amygdala lesions exhibited a selective elevation in the threshold of VADs. During conditioning the amplitude and duration of VADs were selectively reduced in amygdala-lesioned rats. These findings support earlier observations of that elicitation of VADs by tailshock correlates with the capacity of this US to support fear conditioning. The ACe may be involved in both associative and non-associative aspects of fear conditioning, but for progress in our understanding it is essential to evaluate its role in the generation of conditioning relevant URs.     

Motivation and learning: Neurophysiological mechanisms in a “model” system

The neurophysiological mechanisms underlying behavioral motivation and associative learning are described in an invertebrate “model” system, the carnivorous marine mollusc Pleurobranchaea. Feeding motivation can be controlled via nutritional history and is represented centrally in the feeding motor network as a change in the balance of synaptic excitation and inhibition at the level of interneurons that initiate feeding behavior, i.e., feeding “command” interneurons. Associative learning, induced by avoidance conditioning of feeding behavior, manifests identically at the level of the command interneurons, but is distinguished from non-associative motivational changes by processes that occur in identified neurons and pathways presynaptic to the command interneurons. Motivation and learning are therefore linked mechanistically by convergent neurophysiological mechanisms at the level of central neurons that initiate behavior.     

Trait Anxiety and Fear Responses to Safety Cues: Stimulus Generalization or Sensitization?

Abnormal fear responding to threat cues may contribute to the aetiology and maintenance of persistent fears and pathological anxiety. Chronic anxiety may also involve abnormal fear responding to ??safety?? cues, which do not signal danger. Yet investigations of fear responding to acquired safety cues are scarce and the basis of such responding remains unclear. Moreover, previous studies do not distinguish between stimulus generalization (an associative mechanism based on perceptual similarity between threat and safety cues) and sensitization (a non-associative mechanism whereby fear responses to any novel, intense, or fear-related stimulus are temporarily elevated). This study investigated responses to acquired safety cues in volunteers with varying trait anxiety, using a novel fear conditioning paradigm designed to distinguish between effects of trait anxiety on generalization and sensitization. The paradigm used three conditioned stimuli: a threat cue (CS+) and two safety cues (CS?), one perceptually similar to the CS+ and one perceptually dissimilar. Conditioned fear to these cues was indexed by fear potentiation of the startle blink reflex, skin conductance responses, and self-report. To examine how trait anxiety moderated responses to safety cues, participants were divided into high and low trait anxiety subgroups. Startle, skin conductance, and self-reported fear measures indicated that generalization of fear occurred for the safety cue which resembled the threat cue, but not for the perceptually dissimilar safety cue, consistent with the stimulus generalization hypothesis. There was some evidence that stimulus generalization was exaggerated in anxious individuals. The current study sheds light on the mechanism by which fear responses to safety cues arise in healthy individuals, and offers some insight into the influence of this mechanism in chronic anxiety.     

Learning to fear outgroups: An associative learning explanation for the development and reduction of intergroup anxiety

Pavlovian conditioning is a form of associative learning shown to contribute to the development and reduction of clinical anxiety and fear, and more recently, intergroup anxiety and fear. The current review provides a synthesis of the literature on associative learning of fear toward outgroups. Findings are reviewed that outline how fear toward the outgroup, relative to the ingroup, can be preferentially learnt and is resistant to extinction‐based techniques. Novel future research directions for intergroup anxiety are then identified based upon previous research on clinical anxiety. It is proposed that processes known to enhance the extinction of specific phobia should be investigated with social stimuli. Specifically, it is argued that exploring cognitive factors during extinction and conducting extinction in multiple contexts may provide new avenues to pursue intergroup harmony through reduced intergroup anxiety. The review concludes by suggesting innovative research designs are needed to validate an associative learning account of fear toward outgroups outside of experimental settings.     

Non-associative fear acquisition: a review of the evidence from retrospective and longitudinal research

It is axiomatic that the capacity to experience fear is adaptive, enabling rapid and energetic response to imminent threat or danger. Despite the generally accepted utility of functional fear, the nature of maladaptive fear remains controversial. There is still no consensus about how specific fears and phobias are acquired and modulated. Two major schools of thought are apparent: those suggesting dysfunctional fear arises largely as the result of associative-conditioning processes versus those who favour more biologically based etiological explanations. In this regard, the non-associative model of fear acquisition postulates the existence of a limited number of innate, evolutionary-relevant fears, while emphasising conditioning modes of onset for evolutionary-neutral fears. Recent retrospective and longitudinal studies have tested predictions from the non-associative model. In general, findings support non-associative hypotheses and are difficult to reconcile with neo-conditioning explanations of fear acquisition. These data suggest that four pathways to fear may provide the most parsimonious theory of fear etiology. The theoretical and practical implications of adding a fourth, non-associative path to Rachman's (Behav. Res. Ther. (1977) 15, 375-387) three 'associative' pathways are discussed. Unresolved issues requiring further investigation are considered.     

The development of skin conductance fear conditioning in children from ages 3 to 8 years

Although fear conditioning is an important psychological construct implicated in behavioral and emotional problems, little is known about how it develops in early childhood. Using a differential, partial reinforcement conditioning paradigm, this longitudinal study assessed skin conductance conditioned responses in 200 children at ages 3, 4, 5, 6, and 8 years. Results demonstrated that in both boys and girls: (1) fear conditioning increased across age, particularly from ages 5 to 6 years, (2) the three components of skin conductance fear conditioning that reflect different degrees of automatic and controlled cognitive processes exhibited different developmental profiles, and (3) individual differences in arousal, orienting, and the unconditioned response were associated with individual differences in conditioning, with the influence of orienting increasing at later ages. This first longitudinal study of the development of skin conductance fear conditioning in children both demonstrates that children as young as age 3 years evidence fear conditioning in a difficult acquisition paradigm, and that different sub-components of skin conductance conditioning have different developmental trajectories.     

Family influences on dysfunctional thinking in anxious children

Anxious children are found to interpret ambiguous stories in a negative way. The current study attempted to examine the possible influence of parental fear and parental interpretation bias on the maintenance of such an interpretation bias. Children varying in level of anxiety (n=25) and their parents, filled in a questionnaire to measure their own fears, and gave their interpretations concerning nine ambiguous stories, relevant for childhood ‘interactional’ anxieties: social anxiety, separation anxiety, and generalized anxiety. Then, parents were asked to talk with their children about three of the stories. After the family discussion the children had to give their final interpretations. Results indicated that parents' self‐reported fear level and interpretation bias were associated with children's interpretation bias before the family discussion. However, no evidence was found for the idea that parents maintain or enhance the interpretation bias of their children. That is, irrespective of parental fear and parental interpretation bias, children interpreted the ambiguous stories as less negative after discussing them with their parents. Copyright © 2003 John Wiley & Sons, Ltd.     

Learning history in fear of blushing

Two studies, investigating the learning history (i.e. traumatic conditioning experiences, vicarious learning, informational learning) of individuals with and without fear of blushing, are presented. In study 1, individuals high (n=61) and low (n=59) in fear of blushing completed the (revised) Phobic Origin Questionnaire [POQ; Öst, L. G., & Hugdahl, K. (1981). Acquisition of phobias and anxiety response patterns in clinical patients. Behavior Research and Therapy, 19, 439–447]. In study 2, individuals who applied for treatment for fear of blushing (n=31) and a nonfearful, matched control group (n=31) were interviewed with the same instrument, taking into account only specific memories. High fearful individuals reported more negative learning experiences in connection with blushing than low fearful individuals, irrespective of the type of questioning. Meanwhile, study 1 (written POQ) produced higher percentages of negative learning experiences for both high and low fearful individuals than study 2 (interview). It is concluded that the POQ interview showed a more realistic picture than the written POQ. The possible role of learning history in the acquisition of fear of blushing is discussed.     

Contingency theory and the distinction between associative and non-associative effects in classical conditioning

There is evidence to suggest that CS-US contingency is the variable that determines the associative effects of a CS. It has been claimed that experiments where contingency is manipulated allow us to distinguish between excitatory and inhibitory associative effects, and suggest a solution to the problem of finding a control procedure for non-associative effects. It is argued, however, that unless we can find a priori grounds for defining a level of contingency at which there are no associative effects, these claims are not justified. The reasons for this are that we have no way of distinguishing experimentally between associative and non-associative contributions to the effect of a CS, and that without such a technique there is no possibility of locating the point of associative neutrality empirically.     

The relevance of recent developments in classical conditioning to understanding the etiology and maintenance of anxiety disorders

Current etiological models of anxiety disorders emphasize both internal diatheses, or risk factors, and external stressors as important in the development and maintenance of clinical anxiety. Although considerable evidence suggests personality, genetic, and environmental variables are important to these diathesis-stress interactions, this general approach could be greatly enriched by incorporating recent developments in experimental research on fear and anxiety learning. In this article, we attempt to integrate the experimental literature on fear/anxiety learning and the psychopathology literature on clinical anxiety, identify areas of inconsistency, and recommend directions for future research. First, we provide an overview of contemporary models of anxiety disorders involving fear/anxiety learning. Next, we review the literature on individual differences in associative learning among anxious and non-anxious individuals. We also examine additional possible sources of individual differences in the learning of both fear and anxiety, and indicate where possible parallels may be drawn. Finally, we discuss recent developments in basic experimental research on fear conditioning and anxiety, with particular attention to research on contextual learning, and indicate the relevance of these findings to anxiety disorders.     

The development of cued versus contextual conditioning in a predictable and an unpredictable human fear conditioning preparation

In this human fear conditioning study, the online development of conditioned US-expectancy to discrete cues and background contexts was measured in two groups. In the paired group (n=30), the CS was systematically followed by an aversive shock (US). In the unpaired group (n=30), CS and US were presented explicitly unpaired. Using US-expectancy ratings, we replicated the basic finding already illustrated in humans with startle modulation. In the paired group, the CS elicited more US-expectancy than the context, whereas in the unpaired group, the context elicited more US-expectancy than the CS. Interestingly, we also observed a trial-by-trial development of conditioning to the context in the unpaired group as indicated by a significant linear trend. This gradual development and the evidence for the role of US-expectancy in contextual fear add to the idea that cued and contextual fear rely on the same basic associative processes.     

Failure to overcome 'innate' fear: a developmental test of the non-associative model of fear acquisition

The non-associative, Darwinian theory of fear acquisition proposes that some individuals fail to overcome biologically-relevant fears (e.g. height) because they (1) do not have sufficient safe exposure to the relevant stimuli early in life or (2) are poor habituators who have difficulty 'learning not to fear'. These two hypotheses were tested in a longitudinal birth cohort study. Study 1 found evidence for reduced exposure to height stimuli in childhood for individuals with a fear of heights compared to study members without fear. Study 2 found evidence for higher levels of stress reactivity (a proxy for habituation) in childhood and adolescence among 18-year-old height phobics compared to study members with dental phobia and those with no fear. The results were discussed in relation to recent findings suggesting that some evolutionary-relevant fears may appear in the absence of traumatic 'learning' experiences. The merits of adding a fourth, non-associative pathway to Rachman's [Rachman, S. (1977)]. The conditioning theory of fear acquisition: a critical examination. Behaviour Research and Therapy, 15, 375-387) three pathways model of fear acquisition were briefly considered.     

Nonassociative learning processes determine expression and extinction of conditioned fear in mice

Freezing to a tone following auditory fear conditioning is commonly considered as a measure of the strength of the tone-shock association. The decrease in freezing on repeated nonreinforced tone presentation following conditioning, in turn, is attributed to the formation of an inhibitory association between tone and shock that leads to a suppression of the expression of fear. This study challenges these concepts for auditory fear conditioning in mice. We show that acquisition of conditioned fear by a few tone-shock pairings is accompanied by a nonassociative sensitization process. As a consequence, the freezing response of conditioned mice seems to be determined by both associative and nonassociative memory components. Our data suggest that the intensity of freezing as a function of footshock intensity is primarily determined by the nonassociative component, whereas the associative component is more or less categorical. We next demonstrate that the decrease in freezing on repeated nonreinforced tone presentation following conditioning shows fundamental properties of habituation. Thus, it might be regarded as a habituation-like process, which abolishes the influence of sensitization on the freezing response to the tone without affecting the expression of the associative memory component. Taken together, this study merges the dual-process theory of habituation with the concept of classical fear conditioning and demonstrates that sensitization and habituation as two nonassociative learning processes may critically determine the expression of conditioned fear in mice.     

Metyrapone reveals that previous chronic stress differentially impairs hippocampal-dependent memory

Chronic stress facilitates fear conditioning in rats with hippocampal neuronal atrophy and in rats in which the atrophy is prevented with tianeptine, a serotonin re-uptake enhancer. The purpose of this study was to determine whether the lack of dissociation between fear conditioning performance and hippocampal integrity was masked by the presence of endogenous corticosteroids during training. As in previous studies, rats were stressed by daily restraint (6 h/day for 21 days), trained in the conditioning chamber (day 23), and then assessed for conditioned fear (day 25) at a time when hippocampal dendritic atrophy persists. On the training day, half of the control and stressed rats were. injected with metyrapone to reduce corticosterone release. Two hours later, two paired or unpaired presentations of tone and footshock were delivered. Although metyrapone reduced conditioned fear in all rats, only stressed rats showed dissociated fear conditioning (i.e. tone conditioning was reduced while contextual conditioning was eliminated). Chronically stressed rats, regardless of metyrapone treatment displayed more rearing in the open field when tested immediately after the completion of fear conditioning. These data support the hypothesis that increased emotionality and enhanced fear conditioning exhibited by chronically stressed rats maybe due to endogenous corticosterone secretion at the time of fear conditioned training. Moreover,these data suggest that chronic stress impairs hippocampal-dependent processes more robustly than hippocampal-independent processes after metyrapone to reduce corticosterone secretion during aversive training.