Original articleThe defense system of fear: behavior and neurocircuitryLe système défensif de la peur : comportement et neurocircuiterie
Introduction
According to the biologist von Uexküll [127], living beings constitute subjective systems capable of initiating their own behaviors. Depending on the degree of evolution and complexity of the organisms, behaviors can take the form of reflexes and tropisms or much more complex and flexible activities such as social communications, specific tool-use practices, cultural transmissions. For von Uexküll, each species lives in its “own” environment (“Umwelt”) coextensive to its “subjectivity” (“Innenwelt”) i.e. the organization specified a priori by sensorial receptors and motor effectors. For a given being, all potential stimuli characterize its meaningful “world” (“Merkwelt”), whereas all potential responses determine its efficient “world” (“Wirkwelt”), the two together forming the “Umwelt”. Living beings spontaneously generate a limited range of innate behaviors, which can turn into robust habits and fixed routines [97]. However, in the more complex organisms, these innate behavioral patterns can be promoted, through epigenetic and learning processes, to a potentially infinite number of variants. Behaviors appear to be oriented, in terms of affective valence, by a basic bipolar motivational system [86], appetitive or defensive, releasing either approach or defense behaviors. For Epstein [41], it is inconceivable that behaviors, apart from reflexes, should occur without the participation of the three following components: innate, acquired and reactive. Within this framework, fear can be conceived as a set of behavioral defense sequences protecting individuals from environmental dangers, social aggressions or abiotic aversive stimuli [46]. Thus, fear appears to be a functional behavior system, a “complex control structure related to a particular function or need of the organism, such as feeding, reproduction, defense or body care” [126]. Defensive behavioral patterns can be released by various potential or actual threatening situations. In the first case, one may define their function as anticipatory, in the second as immediate. The concept of “anticipation” includes all organic processes, which prepare living beings to cope with their environment. These processes range from the more primitive levels of integration to the higher ones, from the monosynaptic reflex to the human capacity of planning complex activities. In unicellular organisms, behavior is generated by protein-based circuits, whereas in more developed ones it relies on neural activity.
Section snippets
Anticipatory defensive behaviors
Chitty and others [27] were the first to record systematically the behavior now widely known as new object reaction in commensal rats. The animals were shown to avoid any unfamiliar objects in their familiar home range: a box, a piece of metal, a heap of food and so on. It is also commonly observed that rodents tend to avoid the center of open fields by keeping close to the walls of the enclosure. These neophobic responses are generally considered as species-typical anticipatory defensive
Immediate defense behaviors
The antipredator defense behaviors in animals provide a comprehensive view of the organization of immediate defense responses and their adaptive roles. Flight, defensive fight, freezing, tonic immobilization, submissive postures, hypoalgesia as well as autonomic reactions are the most common responses elicited by the encounter with predators and more generally with aversive or stressful situations.
Neural mechanisms engaged in the fear defense behavior system
One of the first experimental results to shed light on the neurophysiological processes generating defense behaviors is known as the Klüver-Bucy syndrome [81]. After carrying out a bilateral temporal lobectomy in Rhesus monkeys, these authors observed, among other important behavioral impairments, the loss of defense responses: animals no longer showed freezing in presence of the experimenter, they did no longer flee into the corner when approached or exhibit innate avoidance reactions towards
Summary and conclusion
The aim of this paper has been to present fear as an adaptive defensive behavior system developed in the course of evolution to guarantee survival in dangerous environments. Thus, in order to survive, living beings are innately prepared to display a variety of behavioral patterns permitting them to cope with potential or actual threats, in particular predators. Besides specific goal-oriented movements such as avoidance, flight or fight, freezing, tonic immobility, startle and submissive
References (135)
The primate amygdala and the neurobiology of social behavior: implications for understanding social anxiety
Biol Psychiatry
(2002)Induction of rage following microinjections of glutamate into midbrain but not hypothalamus of cats
Neurosci Lett
(1982)- et al.
Behavioral and neurochemical changes following predatory stress in mice
Neuropharmacology
(2001) - et al.
Link between emotional memory and anxiety states: a study by principal component analysis
Physiol Behav
(1995) - et al.
Historical effects of stimulus exposure: readiness to eat and object exploration
Learning and Motivation
(1970) - et al.
Attack and defensive behaviour in the albino rat
Anim Behav
(1977) - et al.
Attack and defense in rodents as ethoexperimental models for the study of emotion
Prog Neuropsychopharmacol Biol Psychiatry
(1989) - et al.
Emotion and motivation: the role of the amygdala, ventral striatum and prefrontal cortex
Neurosci Biobehav Rev
(2002) Autoanalgesia: opiate and non-opiate mechanisms
Neurosci Biobehav Rev
(1980)- et al.
Genetic basis of anxiety-like behaviour: a critical review
Brain Res Bull
(2002)
Animal models of anxiety based on classical conditioning: the conditioned emotional response (CER) and the fear-potentiated startle effect
Phamacol Ther
Defensive behavior in rats towards predatory odors: a review
Neurosci Biobehav Rev
Tonic immobility and emergency time in pigs—more evidence for behavioural strategies
Appl Anim Behav Sci
Novel environment and cat odor change GABA and 5-HT release and uptake in the rat
Pharmacol Biochem Behav
Defensive responses to phobic stimuli
Biol Psychol
Conditional hypoalgesia is attenuated by naltrexone applied to the PAG
Brain Res
Stress-induced hypoalgesia and defensive freezing are attenuated by application of diazepam to the amygdala
Pharmacol Biochem Behav
Neurocircuitry of stress: central control of hypothalamo-pituitary-adrenocortical axis
Trends Neurosci
Food deprivation and locomotor exploration in the white rat
Anim Behav
Conspecific vocalizations, tonic immobility and fearfulness in the domestic fowl
Behav Process
Neurophysiologic studies of the immobility reflex (“animal hypnosis”)
Neurosci Res (New York)
Comparative study of emotional behaviour in three inbred strains of mice
Behav Process
Corticosteroids in relation to fear, anxiety and psychopathology
Neurosci Biobehav Rev
Emotion, motivation and anxiety: brain mechanisms and psychophysiology
Biol. Psychiatry
Fear and the brain: where have we been, and where are we going?
Biol Psychiatry
Effects of scopolamine, amphetamine and benzodiazepines on conditioned suppression
Pharmacol Biochem Behav
Active muscle vasodilatation produced by stimulation of the brain stem: its signification in the defence reaction
J Physiol (Lond)
Transfer of an escape response from tail shock to brain-stimulated attack behavior
J Exp Anal Behav
Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala
Nature
The human amygdala in social judgement
Nature
Affective influences on startle in 5-month-old infants: reactions to facial expression of emotion
Child Dev
Defense reactions and exploratory behavior in rats
J Comp Physiol Psychology
Crouching as an index of fear
J Comp Physiol Psychol
Innate and conditioned reactions to threat in rats with amygdaloid lesions
J Comp Physiol Psychol
Defensive reactions of laboratory and wild rats Rattus norvegicus
J Comp Physiol Psychol
Antipredator defensive behaviors in a visible burrow system
J Comp Psychol
Species-specific defensive reactions and avoidance learning
Psychol Rev
A perceptual-defensive-recuperative model of fear and pain
Behav Brain Sci
L’angoisse
Startle reflex modification: emotion or attention?
Psychophysiology
Conditioned fear as revealed by magnitude of startle response to an auditory stimulus
J Exp Psychol
Bodily changes in pain, hunger, fear and rage
Emotional stimulation of adrenal secretion
Am J Physiol
The control of rats and mice
The expression of the emotions in man and animals
Pharmacological and anatomical analysis of fear conditioning using the fear-startle paradigm
Behav Neurosci
The role of the amygdala in fear and anxiety
Annu Rev Neurosci
Amygdala and bed nucleus of the stria terminalis: differential roles in fear and anxiety measured with the acoustic startle reflex
Ann New York Acad Sci
Human heart rate responses during experimentally induced anxiety
J Exp Psychol
Organization of the subcortical system governing defence and flight reactions in the cat
J Physiol (Lond)
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