The birth, death and resurrection of avoidance: a reconceptualization of a troubled paradigm

Abstract

Research on avoidance conditioning began in the late 1930s as a way to use laboratory experiments to better understand uncontrollable fear and anxiety. Avoidance was initially conceived of as a two-factor learning process in which fear is first acquired through Pavlovian aversive conditioning (so-called fear conditioning), and then behaviors that reduce the fear aroused by the Pavlovian conditioned stimulus are reinforced through instrumental conditioning. Over the years, criticisms of both the avoidance paradigm and the two-factor fear theory arose. By the mid-1980s, avoidance had fallen out of favor as an experimental model relevant to fear and anxiety. However, recent progress in understanding the neural basis of Pavlovian conditioning has stimulated a new wave of research on avoidance. This new work has fostered new insights into contributions of not only Pavlovian and instrumental learning but also habit learning, to avoidance, and has suggested that the reinforcing event underlying the instrumental phase should be conceived in terms of cellular and molecular events in specific circuits rather than in terms of vague notions of fear reduction. In our approach, defensive reactions (freezing), actions (avoidance) and habits (habitual avoidance) are viewed as being controlled by unique circuits that operate nonconsciously in the control of behavior, and that are distinct from the circuits that give rise to conscious feelings of fear and anxiety. These refinements, we suggest, overcome older criticisms, justifying the value of the new wave of research on avoidance, and offering a fresh perspective on the clinical implications of this work.

Figure 1

Active avoidance: the shuttlebox learning paradigm. Top panel: initially, subjects undergo Pavlovian threat conditioning, in which a conditioned stimulus (CS; tone) is paired with an aversive unconditioned stimulus (US; shock). Middle panel: once the CS–US association is acquired, subjects learn that the US can be inactivated by shuttling—this is an escape response. On subsequent trials, subjects learn that shuttling during the CS causes the inactivation of the CS and the omission of the US—this is an avoidance response. Bottom panel: once behavior becomes well-trained, the behavior is preformed in the presence of the CS, even though the US does not result. With continued training the behavior persists habitually in spite of the fact that US is no longer predicted by the CS.

Figure 2

Auditory pavlovian threat conditioning. Top panel: an auditory conditioned stimulus (CS) is paired with a foot shock unconditioned stimulus (US). Middle panel: when the CS is presented in a novel context, it elicits a conditioned reaction, freezing. Bottom panel: if the CS is not paired with the US it does not elicit freezing during the test.

Figure 3

Neural circuits underlying defensive reactions (freezing) and actions (avoidance). The behavioral illustrations show the performance of previously acquired reactions (freezing) and actions (avoidance). (a) Reactive freezing is underpinned by a progression of information through the amygdala. Information about the auditory conditioned stimulus (CS) arrives in the lateral amygdala (LA) from auditory thalamus and/or cortex. CS information then proceeds to the central amygdala (CeA), either directly through LA projections to the central lateral CeA (CL), or indirectly via the basal amygdala (BA) and/or the intercalated cell masses (ITC). Medial CeA (M) projections to the brainstem coordinate CS-evoked reactions, such as freezing. (b) Active avoidance is underpinned by a different amygdalar output pathway. CS information is processed through LA and BA, before progressing to the nucleus accumbens (NAcc), which supports CS-prompted actions, such as shuttling to avoid. This behavior is regulated by the infralimbic prefrontal cortex (PFCIL), which suppresses CeA-mediated freezing.