Distinguishing examples while building concepts in hippocampal and artificial networks

The hippocampal subfield CA3 is thought to function as an autoassociative network that stores experiences as memories. Information from these experiences arrives via the entorhinal cortex (EC), which projects to CA3 directly as well as indirectly through the dentate gyrus (DG). DG sparsifies and decorrelates the information before also projecting to CA3. The computational purpose for receiving two encodings of the same sensory information has not been firmly established. We model CA3 as a Hopfield-like network that stores both correlated and decorrelated encodings and retrieves them at low and high inhibitory tone, respectively. As more memories are stored, the dense, correlated encodings merge along shared features while the sparse, decorrelated encodings remain distinct. In this way, the model learns to transition between concept and example representations by controlling inhibitory tone. To experimentally test for the presence of these complementary encodings, we analyze the theta-modulated tuning of place cells in rat CA3. In accordance with our model’s prediction, these neurons exhibit more precise spatial tuning and encode more detailed task features during theta phases with sparser activity. Finally, we generalize the model beyond hippocampal architecture and find that feedforward neural networks trained in multitask learning benefit from a novel loss term that promotes hybrid encoding using correlated and decorrelated representations. Thus, the complementary encodings that we have found in CA3 can provide broad computational advantages for solving complex tasks.