Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning.

Abstract
The contribution of the amygdala and hippocampus to the acquisition of conditioned fear responses to a cue (a tone paired with footshock) and to context (background stimuli continuously present in the apparatus in which tone-shock pairings occurred) was examined in rats. In unoperated controls, responses to the cue conditioned faster and were more resistant to extinction than were responses to contextual stimuli. Lesions of the amygdala interfered with the conditioning of fear responses to both the cue and the context, whereas lesions of the hippocampus interfered with conditioning to the context but not to the cue. The amygdala is thus involved in the conditioning of fear responses to simple, modality-specific conditioned stimuli as well as to complex, polymodal stimuli, whereas the hippocampus is only involved in fear conditioning situations involving complex, polymodal events. These findings suggest an associative role for the amygdala and a sensory relay role for the hippocampus in fear conditioning. In classical fear conditioning, an emotionally neutral condi- tioned stimulus (CS), such as a light or tone, is paired with an aversive unconditioned stimulus (US), usually footshock. The CS, by virtue of its relationship with the US, acquires aversive properties and comes to elicit responses characteristically elicited by threatening stimuli. Thus, a tone that has previously been paired with footshock elicits "freezing," defecation, piloerection, stereotyped increases in arterial pressure and heart rate, and the release of adrenal hormones into the circulation (e.g., R. J. Blanchard & D. C. Blanchard, 1969; Bolles & Fanselow, 1980; LeDoux, 1987; Smith & DeVito, 1984). Because these "fear" or defense responses are not elicited by the CS before the temporal pairing of the CS with the US, they can be referred to as learned or conditioned emotional responses. Conditioned emotional responses are also elicited by placing an animal in a chamber in which an aversive US has previously been experienced (D. C. Blanchard & R. J. Blanchard, 1972; Bolles & Fanselow, 1980; McCarty, Kvetnansky, Lake, Thoa, & Kopin, 1978). In this situation, the conditioned emotional responses are elicited not by a stimulus that was explicitly paired with the US in a temporally specific manner but instead by some combination of the various background or contextual stimuli that were present in the chamber when the US occurred and remain present when the animal is returned to the chamber. Although the emotional responses elicited by contextual and cued CSs are identical, the information processing demands underlying the two forms of fear conditioning are very dif- ferent. First, in contextual conditioning the CS is not restricted