Attractor-Map Versus Autoassociation Based Attractor Dynamics in the Hippocampal Network

The autoassociative memory model of hippocampal field CA3 postulates that Hebbian associations among external input features produce attractor states embedded in a recurrent synaptic matrix. In contrast, the attractor-map model postulates that a two-dimensional continuum of attractor states is preconfigured in the network during development and that transitions among these states are governed primarily by self-motion information ("path-integration"), giving rise to the strong spatial characteristic of hippocampal activity. In this model, learned associations between "coordinates" on the attractor map and external cues can result in abrupt jumps between states, in the case of mismatches between the current input and previous associations between internal coordinates and external landmarks. Both models predict attractor dynamics, but for fundamentally different reasons; however, the two models are not a priori mutually exclusive. We contrasted these two models by comparing the dynamics of state transitions when two previously learned environmental shapes were morphed between their endpoints, in animals that had first experienced the environments either at the same location, or at two different locations, connected by a passageway through which they walked. As predicted from attractor-map theory, the latter animals expressed abrupt transitions between representations at the midpoint of the morph series. Contrary to the predictions of autoassociation theory, the former group expressed no evidence of attractor dynamics during the morph series; there was only a gradual transition between endpoints. The results of this critical test thus cast the autoassociator theory for CA3 into doubt and indicate the need for a new theory for this structure.