Conjunctive representations, the hippocampus, and contextual fear conditioning

Abstract

The context in which events occur can be represented as both (1) a set of independent features, the feature representation view, and (2) a set of features bound into a unitary representation, the conjunction representationview. It is assumed that extrahippocampal (e.g., neocortical) areas provide a basis for feature representations, but the hippocampal formation makes an essential contribution to the automatic storage of conjunctive representations. We develop this dual-representation view and explore its implications for hippocampal contributions to contextual fear conditioning processes. To this end, we discuss how our framework can resolve some of the conflicts in the recent literature relating the hippocampus to contextual fear conditioning. We also present new data supporting the role of a key mechanism afforded by conjunctive representations-pattern completion (the ability of a subset of a memory pattern to activate the complete memory)-in contextual fear conditioning. As is implied by this mechanism, we report that fear can be conditioned to the memory representation of a context that is not actually present at the time of shock. Moreover, this result is predicted by our computational model of cortical and hippocampal function. We suggest that pattern completion demonstrated in animals and by our model provides a mechanistic bridge to human declarative memory.

Dorsal hippocampus and classical fear conditioning to tone and context in rats: Effects of local NMDA‐receptor blockade and stimulation

“…Thus, the complete anterograde amnesia of fear induced by NMDA in the dorsal hippocampus likely reflects disturbed neuronal processing within the dorsal hippocampus. This interpretation is in contrast to prevalent concepts, emphasizing the specific role of the dorsal hippocampus in contextual fear conditioning (Fanselow, 2000;Anagnostaras et al, 2001;Rudy and O'Reilly, 2001). Evidence supporting this interpretation was, however, provided by two experiments, in which electrolytic as well as cytotoxic lesions of the dorsal hippocampus impaired fear conditioning to a tone (Maren et al, 1997), and by preliminary results indicating deficits in fear conditioning to tone after temporary inhibition of dorsal hippocampal neurons by the GABA A agonist muscimol (Bellgowan and Helmstetter, 1995).…”

“…It is still commonly held, however, that the dorsal hippocampus, which indeed may differ functionally from the ventral hippocampus (Moser and Moser, 1998;Zhang et al, 2002), contributes to contextual fear conditioning by supporting a unified context representation, but is not required for fear conditioning to tone (Fanselow, 2000;Gale et al, 2001;Rudy and O'Reilly, 2001;Wallenstein and Vago, 2001; but see Maren et al, 1997). In particular, fear conditioning to context, similar to spatial and episodic-like learning (Morris et al, 1989;Steele and Morris, 1999;Lee and Kesner, 2002; but see Cain, 1997), has been suggested to require processes mediated by N-methyl-D-aspartate (NMDA)-type glutamate receptors in the dorsal hippocampus, and prevalent concepts of fear conditioning to context imply a central contribution of NMDA receptor-mediated synaptic plasticity in the dorsal hippocampus to context representa-tion Young et al, 1994;Anagnostaras et al, 2001;Stiedl et al, 2000;Gale et al, 2001).…”

The aging hippocampus: A multi-level analysis in the rat

“…Several theorists (Fanselow, 1999;Maren, 2001;Rudy et al, 2004;Rudy and O'Reilly, 2001) have proposed that that contextual fear conditioning can be supported by a hippocampus-dependent memory system that supports a configural/conjunctive representation of context and an elemental system that supports conditioning to the independent features that make up the context. This idea predicts that the damage to the hippocampus should not impair contextual fear in the anterograde direction because the residual elemental system can support conditioning.…”

Neural substrate for higher-order learning in an insect: Mushroom bodies are necessary for configural discriminations

“…As a consequence, solving configural tasks typically requires treating stimulus conjunctions as being different from the simple sum of their elemental components (5)(6)(7)(8). For example, in a negative patterning task (9)(10)(11), subjects have to discriminate a nonreinforced conjunction of two elements A and B from its reinforced elements (i.e., AB-vs. A+ and B+), which requires treating AB as being different from the simple sum of A and B (12,13). The ambiguity of the task lies in the fact that each element (A and B) is as often reinforced (when presented alone) as nonreinforced (when presented as a compound).…”