Abstract
Contextual fear conditioning is thought to involve the synaptic plasticity-dependent establishment in hippocampus of representations of to-be-conditioned contexts which can then become associated with USs in the amygdala. A conceptual and computational model of this process is proposed in which contextual attributes are assumed to be sampled serially and randomly during contextual exposures. Given this assumption, moment-to-moment information about such attributes will often be quite different from one exposure to another and, in particular, between exposures during which representations are created, exposures during which conditioning occurs, and during recall sessions. This presents challenges to current conceptual models of hippocampal function. In order to meet these challenges, our model's hippocampus was made to operate in different modes during representation creation and recall, and non-hippocampal machinery was constructed that controlled these hippocampal modes. This machinery uses a comparison between contextual information currently observed and information associated with existing hippocampal representations of familiar contexts to compute the Bayesian Weight of Evidence that the current context is (or is not) a known one, and it uses this value to assess the appropriateness of creation or recall modes. The model predicts a number of known phenomena such as the immediate shock deficit, spurious fear conditioning to contexts that are absent but similar to actually present ones, and modulation of conditioning by pre-familiarization with contexts. It also predicts a number of as yet unknown phenomena.
Highlights
During Pavlovian fear conditioning, animals become afraid of both specific cues that predict the imminent onset of aversive events such as foot shock, and the situation or “context” in which the shock occurred
Fear of context does not develop if shocks occur too soon after an animal is introduced into a situation; the shock must be delayed by at least some 30 s, and full conditionability does not develop for several minutes (Blanchard et al, 1976; Fanselow, 1986, 1990; Landeira-Fernandez et al, 2006)
We wanted the automaton to compare them to the recalled attributes of previously experienced contexts and use the comparison to decide whether the context is a known one, in which case existing associations to it should be expressed and new ones made, or a novel one, in which case a neural representation of it should be created and further associations made to that
Summary
During Pavlovian fear conditioning, animals become afraid of both specific cues that predict the imminent onset of aversive events such as foot shock, and the situation or “context” in which the shock occurred. Fear conditioning provides one of neuroscience’s most promising and active arenas for analyzing neural mechanisms of learning, generally. Both cue and context fear conditioning seem to be due to plastic change at synapses within the amygdala (reviewed by Fanselow and LeDoux, 1999; Blair et al, 2001), but there are striking differences in the phenomenology and the neural circuitry of cue and context fear conditioning. Development of context fear depends on synaptic plasticity within amygdala and within hippocampus (Kiernan and Cranney, 1992; Fanselow, 2000; Rudy and O’Reilly, 2001; Matus-Amat et al, 2004; Stote and Fanselow, 2004; Rudy, 2009). Fear of context does not develop if shocks occur too soon after an animal is introduced into a situation; the shock must be delayed by at least some 30 s, and full conditionability does not develop for several minutes (the so-called “immediate shock deficit”) (Blanchard et al, 1976; Fanselow, 1986, 1990; Landeira-Fernandez et al, 2006)
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