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.     

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.     

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.     

A longitudinal study of the etiology of separation anxiety

A longitudinal examination of the relation between separation experiences and the development of separation anxiety at age 3, 11 and 18 years was conducted. Three associative pathways (Rachman, S.J. (1978). Fear and courage. San Francisco: W.H. Freeman) were assessed. Conditioning events were not related to separation anxiety at age 3. Vicarious learning (modelling) in middle childhood (age 9 years) was the conditioning variable most strongly related to separation anxiety at age 11, accounting for 1.8% of the variance in symptoms. Separation experiences (hospitalisations) before the age of 9 were inversely correlated with separation anxiety at age 18. That is, more overnight hospital stays in childhood were related to less separation anxiety in late adolescence. However, none of these conditioning correlates remained significant predictors of separation anxiety in adjusted regression models. In contrast, certain “planned” separations in early–mid childhood were associated with lower levels of separation anxiety at later ages. Generally, the findings were consistent with predictions from the non-associative theory of fear acquisition. That vicarious learning processes appeared to modulate, albeit to a minor degree, the expression of separation anxiety during mid–late childhood suggests that there may be critical periods during which some individuals are susceptible to the interactive effects of both associative and non-associative processes. These findings serve to illustrate the complexity of fear acquisition, the relevance of developmental factors and the likely interplay between associative and non-associative processes in the etiology of fear and anxiety.     

Different mechanisms of fear extinction dependent on length of time since fear acquisition

Fear extinction is defined as a decline in conditioned fear responses (CRs) following nonreinforced exposure to a feared conditioned stimulus (CS). Behavioral evidence indicates that extinction is a form of inhibitory learning: Extinguished fear responses reappear with the passage of time (spontaneous recovery), a shift of context (renewal), and unsignaled presentations of the unconditioned stimulus (reinstatement). However, there also is evidence to suggest that extinction is an "unlearning" process corresponding to depotentiation of potentiated synapses within the amygdala. Because depotentiation is induced more readily at short intervals following LTP induction and is not inducible at all at a sufficient delay, it may be that extinction initiated shortly following fear acquisition preferentially engages depotentiation/"unlearning," whereas extinction initiated at longer delays recruits a different mechanism. We investigated this possibility through a series of behavioral experiments examining the recoverability of conditioned fear following extinction. Consistent with an inhibitory learning mechanism of extinction, rats extinguished 24-72 h following acquisition exhibited moderate to strong reinstatement, renewal, and spontaneous recovery. In contrast, and consistent with an erasure mechanism, rats extinguished 10 min to 1 h after acquisition exhibited little or no reinstatement, renewal, or spontaneous recovery. These data support a model in which different neural mechanisms are recruited depending on the temporal delay of fear extinction.     

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.     

Heart rate reactivity in HAD and LAD rats during Pavlovian fear conditioning

Recently, we reported that High-Alcohol-Drinking (HAD) rats exhibited selective deficits in active avoidance learning under alcohol-naive conditions, and that administration of moderate doses of alcohol (0.5 and 1.0 g/kg) facilitated learning in these rats (Blankenship et al., 2000; Rorick et al., 2003b). We hypothesized that the deficits resulted from excessive fear in the aversive learning context and that the anxiolytic properties of alcohol may have contributed to the improved learning that was observed after alcohol administration. This hypothesis was supported by a recent study in which prolonged freezing in HAD rats was seen after a classical fear conditioning procedure (Rorick et al., 2003a). To provide additional evidence that HAD rats indeed exhibit behaviors consistent with the expression of increased fear in aversive learning contexts, we employed a Pavlovian fear conditioning task to measure heart rate in HAD and Low-Alcohol-Drinking (LAD) rats. In this study, HAD (HAD-1 and HAD-2) and LAD (LAD-1 and LAD-2) rats were assigned to one of three pre-exposure conditions: Context Only, Context/Tone, or Sequential (Context Only followed by Context/Tone) Pre-Exposure. Following pre-exposure, fear conditioning acquisition and extinction procedures were identical for all groups. Results indicated that although no baseline differences were observed between HAD and LAD rats, HAD rats receiving Context-Only pre-exposure exhibited excessive heart rate reactivity to the tone conditional stimulus during fear conditioning acquisition, compared to LAD rats receiving the same pre-exposure conditions. These findings support the hypothesis that HAD rats exhibit behaviors consistent with increased fear in aversive learning contexts, as measured by autonomic conditioning.     

Origins of childhood fears: an evaluation of Rachman's theory of fear acquisition

This study explored Rachman's (1977) theory of fear acquisition in a large sample of Australian and American children and adolescents. Participants completed a questionnaire that addressed different pathways of fear acquisition for 10 highly prevalent fears. The majority of children attributed the onset of their fears to vicarious and instructional factors, although these indirect sources of fear were often combined with direct conditioning experiences. Also examined were effects for gender, age, and nationality. Boys and preadolescents were found to report more direct and vicarious experiences than girls or adolescents. Effects due to nationality were minimal. Methodological limitations attendant to self-reports were acknowledged.     

The effect of the NMDA receptor antagonist MK-801 on the acquisition and extinction of learned fear in the developing rat

Recent findings reveal qualitative developmental differences in extinction of learned fear. The present study explored potential developmental differences in the role of NMDA in acquisition and extinction. Rats were injected with MK-801 prior to fear conditioning or extinction training. Acquisition was found to be NMDA dependent in both age groups, whereas extinction was found to be NMDA dependent in 23-day-old rats, but NMDA independent in 16-day-old rats. These results illustrate another fundamental developmental difference in extinction as well as a dissociation in the role of NMDA in the acquisition and extinction of fear early in development.     

Excitatory strength of expressive faces: effects of happy and fear expressions and context on the extinction of a conditioned fear response

In a recent study, Orr and Lanzetta (1984) showed that the excitatory properties of fear facial expressions previously described (Lanzetta & Orr, 1981; Orr & Lanzetta, 1980) do not depend on associative mechanisms; even in the absence of reinforcement, fear faces intensify the emotional reaction to a previously conditioned stimulus and disrupt extinction of an acquired fear response. In conjunction with the findings on acquisition, the failure to obtain extinction suggests that fear faces have some of the functional properties of "prepared" (fear-relevant) stimuli. In the present study we compared the magnitude of conditioned fear responses to happy and fear faces when a potent danger signal, the shock electrodes, are attached or unattached. If fear faces are functionally analogous to prepared stimuli, then, even in the absence of veridical support for an expectation of shock, they should retain excitatory strength, whereas happy faces should not. The results are consistent with this view of fear expressions. In the absence of reinforcement, and with shock electrodes removed, conditioned fear responses and basal levels of arousal were of greater magnitude for the fear-face condition than for the happy-face condition.     

Single prolonged stress disrupts retention of extinguished fear in rats

Clinical research has linked post-traumatic stress disorder (PTSD) with deficits in fear extinction. However, it is not clear whether these deficits result from stress-related changes in the acquisition or retention of extinction or in the regulation of extinction memories by context, for example. In this study, we used the single prolonged stress (SPS) animal model of PTSD and fear conditioning procedures to examine the effects of prior traumatic stress on the acquisition, retention, and context-specificity of extinction. SPS administered one week prior to fear conditioning had no effect on the acquisition of fear conditioning or extinction but disrupted the retention of extinction memories for both contextual and cued fear. This SPS effect required a post-stress incubation period to manifest. The results demonstrate that SPS disrupts extinction retention, leading to enhanced fear renewal; further research is needed to identify the neurobiological processes through which SPS induces these effects.     

The origins of fear of snakes

In the present study, a questionnaire about the nature and origin of fear of snakes was administered to 60 Phobic, 82 Low Fear and 35 High Fear college students. Phobic and High Fear subjects reported greater fear on a variety of components of snake fear. There was little evidence supporting the role of direct conditioning experiences in the acquisition of fear of snakes. Rather, the results suggested a variety of observational and instructional learning experiences as related to the acquisition of snake fear. Although preparedness for direct conditioning does not seem relevant, a preparedness for observational and instructional learning is possible.     

Contextual control of human fear associations in a renewal paradigm

The original model of behavior change suggests that extinction is context dependent whereas fear acquisition is context independent [Bouton, M. E. & Ricker, S. T. (1994). Renewal of extinguished responding in a second context. Animal Learning and Behavior, 22, 317-324]. Supportive evidence stems mainly from animal studies, showing that after acquisition (conditioned stimulus-unconditioned stimulus (CS-US)) in Context A and extinction in Context B, fear is renewed by presenting the CS in acquisition Context A (ABA renewal) or in a novel Context C (ABC renewal). By implication, the model predicts equal ABA and ABC renewal. However, there is also evidence to suggest that the context dependency of extinction and the context independency of acquisition may be less stringent than originally proposed. The present study investigated renewal in humans using a differential fear conditioning paradigm with a shock US and online shock expectancy ratings and electrodermal responses as dependent variables. Experiment 1 compared an ABA condition with an AAA condition. Experiment 2 compared three conditions: ABA, ABC, and AAA. Both experiments demonstrated ABA renewal. Most importantly, Experiment 2 showed larger ABA than ABC renewal. Overall, results for expectancy ratings were more convincing than for electrodermal responses. In line with the extinction model, the present findings support the context dependency of extinction in humans. In contrast to the model, the findings suggest that in humans not only extinction learning, but also fear acquisition is controlled by its current context.     

Pathways to fear in spider phobic children

Twenty-two children with spider phobia were interviewed about the origins of their fear. More specifically, children were asked about conditioning events, modeling experiences, and negative information transmission. To evaluate the reliability of the information provided by the children, parents were independently interviewed about the origins of their children's phobias. While 46% of the children claimed to have always been afraid, 41% ascribed the onset of their fear to aversive conditioning events. The large majority of these events were confirmed by parents. These findings cast doubts on a strong version of the non-associative account of spider phobia, i.e. the idea that spider phobia is acquired in the complete absence of learning experiences.     

Methylene blue facilitates the extinction of fear in an animal model of susceptibility to learned helplessness

The objectives were to (1) extend previous findings on fear extinction deficits in male congenitally helpless rats (a model for susceptibility to learned helplessness) to female congenitally helpless rats, and (2) attempt a therapeutic intervention with methylene blue, a metabolic enhancer that improves memory retention, to alleviate the predicted extinction deficits. In the first experiment, fear acquisition (four tone-shock pairings in operant chamber) was followed by extinction training (60 tones in open field). Congenitally helpless rats showed fear acquisition similar to controls but had dramatic extinction deficits, and did not display the gradual extinction curves observed in controls. Congenitally helpless rats demonstrated greater tone-evoked freezing as compared to controls in both the acquisition and extinction contexts one week after extinction training, and also in the extinction probe conducted one month later. In the second experiment (which began one month after the first experiment) congenitally helpless subjects were further exposed to tones for 5 days, each followed by 4 mg/kg methylene blue or saline IP, and had a fear renewal test in the acquisition context. Methylene blue administration improved retention of the extinction memory as demonstrated by significant decreases in fear renewal as compared to saline-administered congenitally helpless subjects. The impaired ability to extinguish fear to a traumatic memory in congenitally helpless rats supports the validity of this strain as an animal model for vulnerability to post-traumatic stress disorder, and this study further suggests that methylene blue may facilitate fear extinction as an adjunct to exposure therapy.     

Characteristics of individuals with fear of spiders

Abstract

This paper reports the results of two studies which investigated some of the factors that differentiated individuals with fear of spiders from those without such fears. The main results suggested that (a) there was little evidence that fear of spiders in nonclinical subjects is normally acquired through direct conditioning experiences; (b) there was some evidence for a familial component to spider fears; (c) there was no support for the view that individuals reporting a fear of spiders were especially sensitized to the movement cues possessed by spiders; (d) fear of spiders was not associated either with higher levels of trait anxiety or with an increased predisposition to other fears in general; but (e) fear of spiders did appear to be associated with increased fear of other animals, but only animals that are normally considered fear-evoking or disgust-evoking. These results provide little support for a traditional conditioning view of spider fears, and they are not entirely consistent with some preparedness accounts of the acquisition of specific fears. However, the results do suggest that fear of spiders is part of a functionally integrated set of animal fears, and it is argued that the present results could be better understood by attempting to integrate predator-defence and disease-avoidance models of animal fears.     

Mother knows best: effects of maternal modelling on the acquisition of fear and avoidance behaviour in toddlers

The present study was conducted to investigate the influence of parental modelling on the acquisition of fear and avoidance towards novel, fear-relevant stimuli in a sample of 30 toddlers. The toddlers were shown a rubber snake and spider, which were alternately paired with either negative or positive facial expressions by their mothers. Both stimuli were presented again after a 1- and a 10-min delay, while mothers maintained a neutral expression. The children showed greater fear expressions and avoidance of the stimuli following negative reactions from their mothers. This was true for both genders although the degree of modelled avoidance was greater in girls than in boys. The strong observational learning results are consistent with views that modelling constitutes a mechanism by which fear may be acquired early in life.     

Olfactory fear conditioning paradigm in rats: Effects of midazolam,propranolol or scopolamine

In rodents, fear conditioned responses are more pronounced toward olfactory stimulus, since olfaction is a dominant sense in these subjects. The present study was outlined to investigate if the association between coffee odor (CS1) and electrical footshock (US) would be an effective model for the study of fear-induced behavior and whether compounds used in humans for emotional-related disorders such as midazolam, propranolol, or scopolamine, applied during the different stages of fear conditioning (acquisition, consolidation and expression), affect the defensive responses to both, the olfactory CS1, and the context (CS2) where the CS1 had been presented (second order conditioning). The results revealed that five pairings between coffee odor (CS1) and electrical footshock (US) were able to elicit consistent defensive responses and a second order conditioning to the context (CS2). Midazolam (0.375–0.5 mg/kg; i.p.) treatment was able to interfere with the CS1–US association and with the consolidation of the aversive information. The propranolol (5–10 mg/kg; i.p.) treatment interfered with the CS1–US association, with the retention of fear memory and with the CS1–CS2 association. Propranolol also attenuated the expression of conditioned fear responses when applied before the CS1 test session. Scopolamine (0.6–1.2 mg/kg; i.p.) treatment impaired the acquisition of CS1–US and CS1–CS2 associations, and also disrupted the expression of conditioned fear responses when injected prior to the CS1 test session. These findings have pointed out the usefulness for the olfactory fear conditioning paradigm to investigate drug effects on the acquisition, consolidation and expression of fear conditioned responses.     

Predictability and heritability of individual differences in fear learning

Our objective was to characterize individual differences in fear conditioning and extinction in an outbred rat strain, to test behavioral predictors of these individual differences, and to assess their heritability. We fear-conditioned 100 Long-Evans rats, attempted to extinguish fear the next day, and tested extinction recall on the third day. The distribution of freezing scores after fear conditioning was skewed, with most rats showing substantial freezing; after fear extinction, the distribution was bimodal with most rats showing minimal freezing, but a substantial portion showing maximal freezing. Longer rearing episodes measured prior to conditioning predicted less freezing at the beginning of extinction, but differences in extinction learning were not predicted by any baseline exploratory behaviors. We tested the heritability of extinction differences by breeding rats from the top and bottom 20 % of freezing scores during extinction recall. We then ran the offspring through the same conditioning/extinction procedure, with the addition of recording ultrasonic vocalizations throughout training and testing. Only a minority of rats emitted distress vocalizations during fear acquisition, but the incidence was less frequent in the offspring of good extinguishers than in poor extinguishers or randomly bred controls. The occurrence of distress vocalizations during acquisition predicted higher levels of freezing during fear recall regardless of breeding line, but the relationship between vocalization and freezing was no longer evident following extinction training, at which point freezing levels were influenced only by breeding and not by vocalization. The heritability (h ²) of extinction recall was estimated at 0.36, consistent with human estimates.     

Learning to fear a second-order stimulus following vicarious learning

Vicarious fear learning refers to the acquisition of fear via observation of the fearful responses of others. The present study aims to extend current knowledge by exploring whether second-order vicarious fear learning can be demonstrated in children. That is, whether vicariously learnt fear responses for one stimulus can be elicited in a second stimulus associated with that initial stimulus. Results demonstrated that children's (5–11 years) fear responses for marsupials and caterpillars increased when they were seen with fearful faces compared to no faces. Additionally, the results indicated a second-order effect in which fear-related learning occurred for other animals seen together with the fear-paired animal, even though the animals were never observed with fearful faces themselves. Overall, the findings indicate that for children in this age group vicariously learnt fear-related responses for one stimulus can subsequently be observed for a second stimulus without it being experienced in a fear-related vicarious learning event. These findings may help to explain why some individuals do not recall involvement of a traumatic learning episode in the development of their fear of a specific stimulus.