A type of learning in which a stimulus or action become associated with fear

'Show me a man who is not a slave; one is a slave to lust, another to greed, another to ambition, and all men are slaves to fear' (Seneca 63-65). Fear drives fundamental responses to the world in individuals and societies alike (Durkheim 1895; Freud 1908). James (1890), influenced by Darwin (1872), considered fear merely as an instinct. He even thought that the need to exercise this instinct had diminished in evolution, and in a somewhat naive burst of trust in the virtues of human kind, remarked: '.the progress from brute to man is characterized by nothing so much as by the decrease in frequency of proper occasions for fear' (James 1890). Yet already in its early days, experimental psychology became interested in the ways in which fear is acquired and augmented by experience. Pavlov (1928) termed fear as a 'passive defensive reflex', and noted that memory of a traumatic situation lingers for long and can block the expression of other acquired behaviours. Whereas Pavlov experimented on dogs, Watson, in a chilling expression of pragmatic "behaviourism, did it on human infants (Watson and Rayner 1920).

He frightened them with unexpected noises or sudden removal of physical support. One of his subjects, Albert B., 9 months old, initially 'stolid and unfearful', came to fear a laboratory rat upon association with a sharp noise that caused the infant to jump violently, fall, and cry. The ordeal led Albert, involuntarily, into the scientific literature (ibid.; also Harris 1979) (Figure 29); nowadays, it would have probably led the author into disgrace.

Fear is an emotion. Over the years, 'emotions' were frequently considered as intimate feelings unfit for mechanistic analysis. Most discussions of brain systems of emotion were rather vague and converged on the idea that emotions are subserved by the so-called "limbic system. As in many other chapters in science, a major breakthrough in understanding the neural substrates of emotion was provided by a "reductionist analysis of a "simple system. In this case, the "system was "classical (alias Pavlovian) fear conditioning, and specifically its auditory version. A rat hears a tone (the conditioned stimulus, CS) in conjunction with electric shock to the foot (the unconditioned stimulus, US). The shock elicits a fear response (unconditioned response). The tone then comes to elicit a fear response in the absence of shock (conditioned response, CR). The CR is manifested in multiple physiological responses, including increased blood pressure, secretion of stress hormones, startle, and freezing. The latter is an especially rapid and robust measure of fear (Blanchard and Blanchard 1969), although not necessarily the easiest to quantify. Pavlovian fear conditioning has proven to be a fruitful experimental system (Davis 1992;

Fig. 29 Little Albert undergoes fear conditioning to a rat, as detailed in Watson and Rayner (1920; courtesy of Ben Harris, see also Harris 1979). Conditioning paradigms did change dramatically over the past 80 years: nowadays, the rat is the one that is conditioned, whereas the human *subject only observes.

Fig. 29 Little Albert undergoes fear conditioning to a rat, as detailed in Watson and Rayner (1920; courtesy of Ben Harris, see also Harris 1979). Conditioning paradigms did change dramatically over the past 80 years: nowadays, the rat is the one that is conditioned, whereas the human *subject only observes.

LeDoux 1996; Maren et al. 1996; Rogan and LeDoux 1996; Amorapanth et al. 2000). It has already contributed much to our understanding of circuits that subserve classical conditioning in general and emotion in particular in the mammalian brain. It has also cast light the role of "amygdala in learning, memory, modulation, and expression of emotional behaviour. And almost as a fringe benefit, fear conditioning became the first system in which a "long-term potentiation-like mechanism was shown to occur in learning in the behaving organism (Rogan et al. 1997).

A combination of studies using lesions, cellular physiology, and pharmacology led to a model of Pavlovian fear conditioning. According to this model, the CS and the US information reach the amygdala and associate in the lateral and basolateral nuclei. Amygdalar output, funnelled via the central nucleus, controls multiple effector systems involved in the expression of fear. After training, the CS alone, upon reaching the amygdala, elicits these responses. Although the circuit seems rather simple, several caveats are in place. First, although many laboratories agree that "acquisition and memory of fear conditioning occur in the amygdala, there are some who propose that the amygdala only modulates fear learning, while fear memory forms somewhere else (Cahill and McGaugh 1998). Second, when fear learning becomes more complex, the neuroanatomical map of this type of learning becomes more complex as well (Killcross et al. 1997; Nader and LeDoux 1997). In "real-life, the "context of the fearful situation is also of great importance, in which case the hippocampus becomes involved (Maren et al. 1998; but see McNish et al. 1997). The "cerebral neocortex is also expected to play a part. Yet, in approaching a complex system, one may be better off in adhering first to "Ockham's razor, and elemental Pavlovian fear conditioning offers an opportunity to do just that.

Fear conditioning unveils how the brain deals with the tension between speed and accuracy of response to danger. Analysis of even simple fear learning shows that the information about the CS reaches the amygdala via two different pathways (LeDoux 1996). A short one travels directly from the sensory thalamus to the amygdala and supplies information on general features of the stimulus but not on its detailed attributes. This short channel makes it possible for the organism to respond immediately. For a wandering rabbit, it is surely advisable to react as fast as possible to a fox-like-shadow and risk a false positive, rather than contemplate the fine "perceptual details of the predators' mouth from within. The other pathway runs from the thalamus to the cortex and from there to the amygdala. This somewhat slower route provides information about detailed sensory attributes of the CS and can modulate the initial response. "Functional neuroimaging studies of human volunteers subjected to fear learning show that what is true for the rat is true for "Homo sapiens. The amygdala is active when we acquire and express fear (Adolphs et al. 1995; LaBar et al. 1998),1 and subcortical, thalamo-amygdalar connections enable us to react to a fearful stimulus before we even get a chance to think about it (Morris et al. 1999).

Under certain circumstances fear conditioning situations could culminate in anxiety, neurosis and phobia. 'Fear' and 'anxiety' share many features (Davis 1992), to the point where some authors used them interchangeably (e.g. Mowrer 1938). However, 'fear' and 'anxiety' are not the same. The first is a response to a specific, identified event or situation; the second is abnormally heightened vigilance in anticipation of an event or situation that are construed, either consciously or subconsciously, as threatening (Rachman 1998). In a neurotic state, the mere fact that the threat can be logically deemed unreal doesn't alleviate the suffering. Our prefrontal cortex is normally capable of monitoring and assessing ongoing fearful and emotional situations ("'working memory' of fear and emotion; Davidson and Irwin 1999). This exerts some control over the response, and anticipates its consequences. However, when danger is subjectively appreciated as immediate and intense, "noradrenergic and "dopaminergic neuromodulation disrupts prefrontal cognitive functions (Arnsten 1998). Hence, when life is in peril, evolution clearly relies more on instinct than on reason, but unfortunately, this is also the case when the danger is only in the mental eyes of the beholder.

Selected associations: Amygdala, A Priori, Classical conditioning, Consolidation, Limbic system

1In a gender-dependent manner: in emotional situations, the right amygdala is preferentially activated in the male, the left amygdala in the female (Cahill et al. 2001).

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