The fear module: An evolved module for fear and fear learning

Öhman and Mineka (2001) provided an important theoretical extension to preparedness theory. Ascribing a privileged evolutionary status to fear due to its central importance for survival, these authors assumed that natural selection has pressured animals and humans to shape adaptive mechanisms promoting preferential activation of defensive behaviors in response to cues that signal the occurrence of survival threats (e.g., Bolles, 1970; Seligman, 1970, 1971). In this context, they argued that humans have been biologically predisposed to (learn to) fear events and situations that have posed threats to the survival of their ancestors across evolution, thus aligning with the core hypothesis of preparedness theory (Seligman, 1971). Integrating evidence for this assumption with a wide range of findings from affective, cognitive, and behavioral neuroscience in humans and animals, Öhman and Mineka therefore proposed the existence of an evolved fear module implemented in the human brain dedicated to preferentially processing threat-relevant stimuli from phylogenetic origin, thereby subserving preferential Pavlovian aversive conditioning to these stimuli. The fear module is conceptualized as an apparatus that enables the organism to readily activate defensive behaviors and elicit associated psychophysiological responses to threat-related stimuli in aversive contexts (Öhman & Mineka, 2001; see Figure 2.5). It is conceived to have been specifically tailored by evolutionary pressures to help the organism adapt to survival-threatening situations frequently encountered by the species during its evolution (Mineka &

Öhman, 2002; Öhman & Mineka, 2001). The fear module presents four principal characteristics, each resulting from evolutionary contingencies: (a) input selectivity, (b) automaticity, (c) encapsulation, and (d) specific neural circuitry.

Characteristics of the fear module

Input selectivity. The fear module is proposed to be selective with regard to the input to which it responds. More specifically, it is assumed to be preferentially activated in aversive contexts by stimuli that have been correlated with fear through evolution. Pavlovian conditioning processes additionally allow for further expanding the range of stimuli that are able to activate the fear module, with a particular emphasis on stimuli that have been associated

with situations providing recurrent survival threats in an evolutionary perspective (Mineka &

Öhman, 2002; Öhman & Mineka, 2001). Although arbitrary cues can potentially activate the fear module through Pavlovian aversive conditioning under certain circumstances, associations between these stimuli and fear are thought to be more difficult to learn and less resistant to extinction as opposed to associations between evolutionary threat stimuli and fear (Öhman &

Mineka, 2001).

Automaticity. The fear module is proposed to be automatically activated by evolutionarily threat-relevant stimuli without requiring voluntary attention or conscious awareness. Such automaticity would be the result of evolutionary pressures that have encouraged the development of mechanisms enabling rapid processing and prioritization of stimuli related to survival threats with minimal neural computations (Öhman & Mineka, 2001);

thereby procuring an adaptive advantage that contributes to promoting the organism’s survival.

Encapsulation. Encapsulation refers to the fear module’s relative independence from cognition (Mineka & Öhman, 2002). More precisely, the fear module is supposed to be impervious and resistant to conscious cognitive control or higher cognitive influences, such as expectancies or language (Mineka & Öhman, 2002; Öhman & Mineka, 2001). This characteristic is consistent with the preparedness theory assumption of irrationality of phobias.

Even though the fear module is impenetrable to cognition, it may conversely exert an influence on cognitive processes (Öhman & Mineka, 2001; see Figure 2.5). Of note, encapsulation differs from automaticity in that automaticity relates to the activity initiation of the fear module even in the absence of conscious processing, whereas encapsulation pertains to the maintaining of the fear response independently of cognitive control once initiated (Mineka & Öhman, 2002;

Öhman & Mineka, 2001).

Specific neural circuitry. Öhman and Mineka (2001) proposed that the fear module has a dedicated neural implementation in a subcortical neural network centered on the amygdala. Following the traditional conception of the amygdala as the brain substrate for fear, this proposal primarily relied on animal research, which has shown that the amygdala – a subcortical ensemble of neural nuclei with partially distinct functional features located in the anterior medial temporal lobe (e.g., LeDoux, 2000) – is crucially involved in fear-related processes and behaviors (e.g., Weiskrantz, 1956) and, more particularly, in Pavlovian aversive conditioning (e.g., Davis & Whalen, 2001; Fendt & Fanselow, 1999; LeDoux, 1996, 2000;

Maren, 2001; Phelps & LeDoux, 2005). Strongly inspired by LeDoux’s (1996) dual-route model, Öhman (2005) further suggested that fear reactions triggered by threat stimuli are

mediated by an automatic and subcortical pathway passing through the superior colliculi and the pulvinar nucleus of the thalamus before accessing the amygdala. This neural circuitry would notably have an ancient evolutionary origin, as suggested by its subcortical location and high conservation across species (Öhman & Mineka, 2001). The fear module’s ancient origin and brain location would hence be responsible for its automaticity and relative impenetrability to cognition (LeDoux, 1996; Öhman & Mineka, 2001).

Empirical basis of the fear module

Input selectivity. The hypothesized differential sensitivity of the fear module to evolutionarily threat-relevant versus threat-irrelevant stimuli has been supported by findings from human Pavlovian conditioning experiments on preparedness. As mentioned previously (see chapter 2.3.1 here above), these experiments have demonstrated selective associations between threat-relevant stimuli from phylogenetic origin and aversive USs, as reflected by faster and more persistent Pavlovian aversive conditioning to these stimuli (e.g., Ho & Lipp, 2014; Öhman & Dimberg, 1978; Öhman, Eriksson, et al., 1975; Öhman et al., 1976; Öhman &

Mineka, 2001).

In addition, such selective associations have also been reported in non-human primates (e.g., M. Cook & Mineka, 1989, 1990; Mineka et al., 1984). Using a vicarious conditioning paradigm, these studies have shown that lab-reared observer monkeys selectively acquired fear

Figure 2.5. Schematic representation of the fear module and its hypothetical relations with other psychophysiological, behavioral, and cognitive systems. Adapted from Öhman and Wiens (2004).

of snakes after watching videotapes of wild-reared model monkeys behaving fearfully with a (real or toy) snake, but did not acquire fear of flowers when the snake was replaced with a flower in the videotapes (M. Cook & Mineka, 1989, 1990). Similar results have been likewise observed when (real or toy) crocodiles and rabbits were used as animal threat-relevant and threat-irrelevant stimuli, respectively (M. Cook & Mineka, 1989). In contrast, no preferential learning occurred when snake stimuli were used as discriminative stimuli for appetitive food rewards (M. Cook & Mineka, 1990). Importantly, the observer monkeys were all completely naive to the stimuli used in these experiments as they had never been exposed to them previously (Öhman & Mineka, 2001), hence suggesting the involvement of both a biological preparedness mechanism and selective associations (Öhman & Mineka, 2001; Seligman, 1970, 1971).

Empirical support in line with the fear module selectivity have also been provided by human experiments using a covariation bias paradigm (e.g., Tomarken, Mineka, & Cook, 1989). This paradigm assesses whether selective associations between evolutionarily threat-relevant stimuli and aversive outcomes can be evidenced in association or covariation judgments. Specifically, Tomarken et al. (1989) implemented an illusory correlation paradigm, in which participants were exposed to relevant stimuli (snakes or spiders) and threat-irrelevant stimuli (flowers and mushrooms), with each stimulus being randomly followed either with an electric stimulation, a tone, or no outcome. Participants were then asked to evaluate the degree of covariation between the stimulus categories and the outcomes. Results indicated that participants with a high level of fear of the threat-relevant stimuli largely overestimated the contingency between the threat-relevant stimuli and the electric stimulations, which was not the case for the other stimulus categories and outcomes; participants with a low level of fear exhibited a tendency in the same direction. Moreover, this covariation bias was specific to the electric stimulation’s aversiveness rather than its salience, as the effect did not occur in a second experiment to a nonaversive outcome that was rated as similarly salient as the electric stimulation. Subsequent studies have replicated and extended these initial findings to the comparison between phylogenetically and ontogenetically threat-relevant stimuli, generally reporting a covariation bias to the former but not to the latter (e.g., Amin & Lovibond, 1997;

Kennedy, Rapee, & Mazurski, 1997; Tomarken, Sutton, & Mineka, 1995).

Another related line of research has further shown that evolutionarily threat-relevant stimuli are more effective in capturing attention than threat-irrelevant stimuli (Öhman, Flykt,

& Esteves, 2001; Öhman, Lundqvist, & Esteves, 2001). More precisely, animal (snakes or

spiders; Öhman, Flykt, et al., 2001) and social (threatening faces; Öhman, Lundqvist, et al., 2001) threat-relevant stimuli, as well as simple geometric shapes conveying a threat meaning similar to angry faces (i.e., downward-pointing “V”; Larson, Aronoff, & Stearns, 2007), have been reported to be detected more quickly in a visual search paradigm than threat-irrelevant stimuli, such as flowers, friendly faces, or geometric shapes devoid of any threat meaning, respectively. This preferential attentional capture by threat-relevant stimuli from phylogenetic origin has been categorized as preattentive and concurs with the notion that the fear module is selectively activated by evolutionary threat stimuli in an automatic fashion (Öhman & Mineka, 2001).

Automaticity. Evidence for the view that the fear module is automatically activated by evolutionarily threat-relevant stimuli essentially stems from human Pavlovian aversive conditioning studies using backward masking. In this procedure, a target stimulus is presented very briefly (e.g., 30 ms) and is immediately followed by a masking stimulus with the aim of preventing the target stimulus from being consciously recognized (Öhman & Mineka, 2001).

Öhman and colleagues (e.g., Öhman & Soares, 1993; Soares & Öhman, 1993; see also Öhman, 1986) notably demonstrated that the CR to animal threat-relevant stimuli persisted even when they were masked during extinction, whereas masking led to extinction of the CR to threat-irrelevant stimuli. Resistance to extinction of the CR to angry faces was reported as well when they were masked with neutral faces during the extinction phase, which was not the case for happy and neutral faces (Esteves, Dimberg, & Öhman, 1994). In a similar vein, resistance to extinction effects were shown in response to unmasked animal threat-relevant (Öhman &

Soares, 1998) and angry faces (Esteves, Parra, Dimberg, & Öhman, 1994), but not to unmasked threat-irrelevant stimuli, when these stimuli were masked during the acquisition rather than the extinction phase. Altogether, Öhman and Mineka (2001) interpreted these results as showing that CRs to biologically threat-relevant stimuli are automatic and can be elicited independently from visual awareness, thereby supporting the fear module’s automaticity.

Encapsulation. Experiments by Hugdahl and Öhman (Hugdahl, 1978; Hugdahl &

Öhman, 1977; Öhman, Erixon, et al., 1975; see also Lipp & Edwards, 2002) provided support for the encapsulation of the fear module in showing that the CR to animal threat-relevant stimuli from evolutionary origin was resistant to extinction even after explicit verbal instructions emphasizing that the US would no longer be administered, whereas the CR to threat-irrelevant stimuli immediately extinguished after verbal instructions. Soares and Öhman (1993) furthermore extended these results by combining a backward masking procedure with

verbal instructions stressing that the US would no longer be presented during extinction. They observed that the CR to animal threat-relevant was persistent during extinction and remained unaffected neither by the masking procedure, nor by verbal instructions; by contrast, both manipulations eliminated the CR to threat-irrelevant stimuli. Thus, Öhman and Mineka (2001) interpreted these findings as corroborating the purported impenetrability of the fear module to influences from higher-level cognitive factors.

Specific neural circuitry. A crucial argument for the conception of the amygdala as the fear module’s center revolves around its fundamental role in Pavlovian aversive conditioning across animals and humans (e.g., LeDoux, 1996; Phelps & LeDoux, 2005).

Animal lesion studies (see Fendt & Fanselow, 1999, for a review) and human neuropsychological studies in patients with amygdala damage (e.g., Bechara et al., 1995;

LaBar, LeDoux, Spencer, & Phelps, 1995) have underlined that amygdalar lesions impair or abolish Pavlovian aversive conditioning. Relatedly, functional neuroimaging studies in humans have delineated the amygdala as a central neural correlate of Pavlovian aversive conditioning (e.g., Büchel et al., 1998; LaBar et al., 1998; Morris, Dolan, & Friston, 1998, 1999; Olsson &

Phelps, 2007; Phelps, 2006; Phelps et al., 2004). In particular, Morris et al. (1998) demonstrated that the amygdala was more activated in response to angry face CSs+ than angry face CSs- during extinction, both for masked and unmasked presentations. Morris et al. (1999) further reported that the heightened amygdala activations by masked stimuli, but not by unmasked stimuli, could be predicted by the superior colliculus and the pulvinar activations, which suggests a potential involvement of a subcortical route from the thalamus to the amygdala in processing threat-related stimuli without conscious awareness (see LeDoux, 1996). Accordingly, Öhman (2005) proposed that the amygdala corresponds to an automatic threat detector, thereby accentuating its conceptualization as a fear module.

Summary

The fear module theory (Öhman & Mineka, 2001) proposes that the preferential processing of, and enhanced Pavlovian aversive conditioning to, threat-relevant stimuli from evolutionary origin is subserved by an evolved fear module in the human brain (with a pivotal role of the amygdala hypothesized). These stimuli are assumed to preferentially and automatically activate the fear module in aversive contexts, and therefore readily enter into selective association with aversive events even when they are presented in a highly degraded manner, as substantiated by a large number of Pavlovian aversive conditioning studies in humans and monkeys (e.g., M. Cook & Mineka, 1989, 1990; Esteves, Parra et al., 1994; Öhman

& Dimberg, 1978; Öhman et al., 1976; Öhman & Mineka, 2001; Öhman & Soares, 1998). The fear module is considered encapsulated and impenetrable to cognitive control, as supported by experiments indicating that associations between animal threat-relevant stimuli and aversive outcomes are impervious to verbal instructions (e.g., Hugdahl & Öhman, 1978; Soares &

Öhman, 1993). Finally, the fear module is thought to reflect the operation of a specific neural network for fear elicitation and fear learning that is centered on the amygdala (Öhman &

Mineka, 2001), as highlighted by the central role of this phylogenetically conserved brain structure in Pavlovian aversive conditioning.

2.3.3. Criticisms of the biological preparedness models and alternative explanations