Neural organization of the defensive behavior system responsible for fear

Abstract

This paper applies the behavior systems approach to fear and defensive behavior, examining the neural circuitry controlling fear and defensive behavior from this vantage point. The defensive behavior system is viewed as having three modes that are activated by different levels offear. Low levels of fear promote pre-encounter defenses, such as meal-pattern reorganization. Moderate levels of fear activate post-encounter defenses. For the rat, freezing is the dominant post-encounter defensive response. Since this mode of defense is activated by learned fear, forebrain structures such as the amygdala playa critical role in its organization. Projections from the amygdala to the ventral periaqueductal gray activate freezing. Extremely high levels of fear, such as those provoked by physical contact, elicit the vigorous active defenses that compose the circa-strike mode. Midbrain structures such as the dorsolateral periaqueductal gray and the superior colliculus playa crucial role in organizing this mode of defense. Inhibitory interactions between the structures mediating circa-strike and post-encounter defense allow for the rapid switching between defensive modes as the threatening situation varies.The functional behavior systems paradigm provides a structural framework that can aid analysis of the environmental control, response topography, and neural mechanisms that determine behavior. One major characteristic of the behavior systems approach is that it views an animal as having a set of several genetically determined, prepackaged behaviors that it uses to solve a particular functional problem (e.g., feeding). If the current conditions demand that this problem must be solved immediately, the animal's behavioral repertoire may become restricted to that set of prepackaged behaviors. Bolles (1970) outlined a strikingly clear example of this in his species-specific defense reaction (SSDR) theory. SSDRs are the rat's innately determined defensive behaviors; freezing, fighting, and flight are examples. When the rat is confronted by a natural environmental threat (e.g., a predator) or an artificial one (e.g., an electric shock), its behavioral repertoire becomes restricted to its SSDRs. In such situations the rat finds it difficult, if not impossible, to execute a response that does not resemble an SSDR. However, the animal does have some flexibility, in that it has several SSDRs from which to choose. The assumption of an adaptationist approach, such as the behavioral systems

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“…Freezing was used to measure the conditional emotional fear response, and was defined as the cessation of all movement with the exception of respiration-related movement and non-awake or rest body posture (McAllister and McAllister, 1971;Fanselow, 1994). Freezing was videotaped and later scored offline with a digital stopwatch by recording the total time spent freezing during every 30-s tone CS.…”

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