Ontogeny of Contextual Fear Conditioning in Rats: Implications for Consolidation, Infantile Amnesia, and Hippocampal System Function
The authors present developmental evidence that contextual fear conditioning is supported by a short-term memory system that supports conditioning immediately after a shock and by a long-term memory system that supports contextual conditioning 24 hr after training. This is based on the finding that after 1 conditioning trial, rats 18 to 32 days old show the same amount of conditioned freezing when tested immediately after conditioning but 18-day-old rats show much less conditioned freezing than the older rats when the retention interval is 24 hr. The data also suggest that the long-term memory representation of context that mediates conditioned fear is not available until several hours after the conditioning trial. Implications of these findings for memory consolidation processes, infantile amnesia, and hippocampal formation development are discussed. Two views of how the experimental context in which the events of a conditioning experience occur can be identified. One view (e.g., Rescorla & Wagner, 1972) is that the context is just the sum of its elements (the individual auditory, visual, olfactory, and tactile cues that the rat experiences) and that these cues have the same associative properties as the phasic events that constitute the conditioned stimulus. The alternative view is that the elements of the context are conjoined into a unitary representation, a spatial map (Nadel & Willner, 1980; Nadel, Willner, & Kurz, 1985), a configuration (Rudy, 1993), or dynamic stereotype (Fanselow, 1990; Pavlov, 1962). The first view implies that conditioning to context and to the conditioned stimulus (CS) are mediated by the same neural systems, but the second view suggests that they depend on different systems. Studies of conditioned fear, as assessed by the rat's tendency to crouch or freeze (Blanchard & Blanchard, 1969), recently have provided evidence for the second view. In these studies, rats were exposed to pairings of an auditory cue and an electrical-shock unconditioned stimulus (US) and subsequently were tested for their fear to both the context and to the auditory cue. Normal adult rats showed a conditioned fear response to both the context in which the shock occurred and to the auditory cue. Both Kim and Fanselow (1992) and Phillips and LeDoux (1992), however, report that damage to the hippocampal formation impairs contextual fear conditioning but has no effect on fear conditioning to the auditory cue. Rudy (1993) has reported a similar dissociation during development. Rats 18 and 23 days old display equivalent fear conditioning to an auditory cue paired with shock, but 18-day