Lesions of the Perirhinal Cortex Interfere With Conditioned Excitation but Not With Conditioned Inhibition of Fear
Northern Illinois University Posttraining lesions of the perirhinal cortex (Prh) have been shown to interfere with the expression of fear. This study assessed whether Prh lesions would also disrupt the inhibition of fear as measured with conditioned inhibition of fear-potentiated startle. Following light + shock, noise ~ light-no shock conditioned-inhibition training, rats were given Prh lesions. The lesions interfered with the expression of fear-potentiated startle to the light. To assess whether conditioned inhibition was affected, the rats were given light + retraining without additional noise --* light - training. The noise-conditioned inhibitor retained its ability to inhibit fear-potentiated startle to the retrained light. These results suggest that the areas of the Prh that are essential for the initial expression of conditioned fear are not important for the expression of conditioned inhibition of fear. Considerable progress has been made in identifying the neural systems that are involved in conditioned fear (Davis, Campeau, Kim, & Falls, 1995; LeDoux, 1987; Mishkin & Appenzeller, 1987). With very few exceptions, these studies have focused on investigating the neural systems involved in the acquisition and expression of conditioned fear. However, fear is not only acquired and expressed, but under some circumstances fear can be reduced or inhibited. Very little is known about the neural systems that are involved in the inhibition of fear. Clearly, to more fully understand the neural systems involved in conditioned fear, it is necessary to also evaluate the neural systems that are involved in the inhibition of fear. Falls and Davis (1997) have detailed a procedure that may be particularly well suited for evaluating the neural systems that are involved in the inhibition of fear: conditioned inhibition of fear-potentiated startle. In the basic fear- potentiated startle paradigm, conditioned fear is operation- ally defined as elevated startle amplitude in the presence of a light that has been previously paired with shock (Davis & Astrachan, 1978). Conditioned inhibition of fear-potentiated startle was produced by giving rats training in which a light was paired with shock (i.e., light+), and a serial noise and light compound was presented without shock (i.e., noise---* light-). Following this training the rats showed fear-potentiated startle to the light, and significantly less fear-potentiated startle to the light when it was preceded by the noise-conditioned inhibitor, suggesting that the noise had acquired the ability to inhibit fear. Control experiments revealed that neither a novel noise nor a noise nonreinforced William A. Falls, Karl T. Bakken, and Scott A. Heldt, Depart- ment of Psychology, Northern Illinois University. We are grateful to Gary Coover and James Corwin for their comments on a draft of this article. Correspondence concerning this article should be addressed to William A. Falls, Department of Psychology, Northern Illinois University, De Kalb, Illinois 60115. Electronic mail may be sent via Internet to wfalls @ niu.edu. separately from the light (i.e., following light+, noise-, light- training) inhibited fear-potentiated startle to the light. These results suggest that the inhibitory effect of the noise was acquired through nonreinforcement of the serial noise --* light compound and cannot be explained solely in terms of an unconditioned effect of the noise on fear- potentiated startle to the light (cf. Papini & Bitterman, 1993; Swartzentruber, 1995). Additional experiments revealed that the noise-conditioned inhibitor passed both the transfer and retardation tests for conditioned inhibition (Rescorla, 1969). Specifically, following light+, noise ---* light- training, fear-potentiated startle to a separately trained conditioned stimulus (CS; e.g., a tactile CS) was also inhibited by the noise (transfer) and subsequent acquisition of conditioned fear to the noise was retarded (retardation). Similar results were obtained when the stimulus modalities were reversed. Together these results suggest that the inhibitory effect of the noise cannot be understood solely in terms of an increase in attention to the noise, generalization decrement, external inhibition, or a modality-specific effect of a noise stimulus on fear produced by a light (cf. Papini & Bitterman, 1993). Rather, these results strongly suggest that the noise acquired the ability to inhibit fear produced by the light (Falls, 1993; Falls & Davis, 1997). Hence, this procedure may be well suited for evaluating the neural systems that are involved in the inhibition of fear. Much is known about the neural systems involved in the expression of fear-potentiated startle (Davis et al., 1995). Although the details have not been worked out, it is believed that the conditioned stimulus is processed through various subcortical sensory structures (Campeau & Davis, 1995a) to either the perirhinal cortex or primary sensory cortex and on to the lateral and basolateral nuclei of the amygdala (Cam- peau & Davis, 1995a; Rosen et al., 1991; Sananes & Davis, 1992). These amygdala nuclei project to the central nucleus of the amygdala, which in turn projects to the sensorimotor interface of the startle reflex pathway (Hitchcock & Davis, 1991; Koch & Ebert, 1993; Yeomans & Polard, 1993). Falls and Davis (1995b) suggest that one way to approach 476