Emotion and Learning

Conditioned Fear: Behavior and Brain Mechanisms

Fear is an emotional state induced by the anticipation of an impending aversive event that can potentially cause pain, harm, or discomfort (see Chapters 5 and 6). Training procedures involving stimuli that cause peripheral pain, such as electric foot shocks, lead to fear conditioning, or the acquisition of an internal response induced by a signal for pain that can influence the organism’s behavior (e.g., induce freezing responses) and physiology (e.g., elevate stress

Table 9.3 Fear in the conditioned suppression preparation with infant rats

Note: In the experiment by Coulter, Collier, and Campbell (1976) described in the text, this design was applied to four groups of different ages. EUP: explicitly unpaired training; LP: lever pressing; RI: retention interval.

Figure 9.9 Recall of fear conditioning in infant rats as measured by the conditioned suppression technique. See Table 9.3 for a description of the design. In conditioned suppression, the rate of responding to the lever during the CS is compared to the rate of responding before the CS in terms of a so-called suppression ratio. A ratio equal to 0.5 implies no change from the pre-CS to the CS periods and, thus, no conditioning. The closer the suppression ratio is to zero, the greater the suppression of lever pressing and the stronger the fear conditioned to the CS. Rats given paired training at 11—16 days of age demonstrated no evidence of fear conditioning after a 32-day retention interval, when compared with explicitly unpaired controls. By contrast, rats trained at 17—22 days of age exhibited a strong suppression of appetitive lever-pressing performance after the 32-day retention interval. The suppression decreases across trials because no shock was administered during the test (i.e., fear extinction).

Source: Coulter, Collier, and Campbell (1976); reproduced with permission from the American Psychological Association.

hormones). Signals inducing fear also tend to suppress ongoing appetitive behavior, thus providing a measure of conditioning in a preparation known as conditioned suppression.

In an ontogenetic study involving conditioned suppression, rats that were 11-13, 14-16, 17-19, or 20-22 days old received Pavlovian CS^US training, followed by a constant retention interval of 32 days, and finally by instrumental response^reinforcer training (Table 9.3). Other experiments demonstrate that rats of these ages rapidly learn to suppress food-reinforced behavior when confronted with a signal for shock. However, the question in this study was whether learning was equally strong after a constant retention interval. Figure 9.9 shows that rats failed to exhibit retention of fear conditioning when acquisition occurred at 11-16 days of age, but retention improved when acquisition occurred at 17-22 days of age. Therefore, an immature mammal can learn a fear response but not remember it later in life (Coulter, Collier, & Campbell, 1976).

Figure 5.15 shows the brain circuit responsible for fear conditioning in adult mammals. Importantly, key brain areas develop at different rates in the rodent CSN. This implies that different forms of fear should develop at different rates (Tallot, Doyere, & Sullivan, 2016). Before an infant rat is 6 days old, the amygdala is not sufficiently mature to support fear conditioning. Starting at postnatal day 7, levels of stress hormones increase rapidly, and by day 10 they reach a critical level that permits amygdala-dependent fear conditioning to be expressed in freezing responses. During the 7- to 10-day period, fear conditioning can be induced if levels of stress hormones are increased by exogenous administration (e.g., corticosterone). At this point, the rat hippocampus starts developing gradually. As a result, contextual fear conditioning is expressed behaviorally later than signal conditioning. Around weaning, after postnatal day 21, rats begin to exhibit contextual fear conditioning.