Integration of exteroceptive and interoceptive information within the hippocampus: a computational study

Randa Kassab, Frédéric Alexandre

Many episodic memory studies have critically implicated the hippocampus in the rapid binding of sensory information from the perception of the external environment, reported by exteroception. Other structures in the medial temporal lobe, especially the amygdala, have been more specifically linked with emotional dimension of episodic memories, reported by interoception. The hippocampal projection to the amygdala is proposed as a substrate important for the formation of extero-interoceptive associations, allowing adaptive behaviors based on past experiences. Recently growing evidence suggests that hippocampal activity observed in a wide range of behavioral tasks could reflect associations between exteroceptive patterns and their emotional valences. The hippocampal computational models, therefore, need to be updated to elaborate better interpretation of hippocampal-dependent behaviors. In earlier models, interoceptive features, if not neglected, are bound together with other exteroceptive features through autoassociative learning mechanisms. This way of binding integrates both kinds of features at the same level, which is not always suitable for example in the case of pattern completion. Based on the anatomical and functional heterogeneity along the septotemporal and transverse axes of the hippocampus, we suggest instead that distinct hippocampal subregions may be engaged in the representation of these different types of information, each stored apart in autoassociative memories but linked together in a heteroassociative way. The model is developed within the hard constraint of rapid, even single trial, learning of episodic memories. The performance of the model is assessed quantitatively and its resistance to interference is demonstrated through a series of numerical experiments. An experiment of reversal learning in patients with amnesic cognitive impairment is also reproduced.