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Abstract
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.
Highlights
The explanation lies in the fact that the number of exteroceptive features far outnumbers that for valence, interoceptive features are much more willing to be shared between stored patterns
The binding of exteroceptive features is accomplished, as it is usually the case, through a separate autoassociative network, subserving pattern completion of exteroceptive patterns. Along with this first autoassociative memory, a second one is employed to serve a similar function for valence features
While autoassociative learning has long been ascribed to CA3 because of its recurrent connections (Marr, 1971), heteroassociative learning has been reported to occur at the Schaffer collaterals projecting from CA3 to CA1 (Miyata et al, 2013), at CA3 backprojections on hilar mossy cells and dentate gyrus (DG) granule cells (Lisman and Otmakhova, 2001)
Summary
Since Tulving’s (1972) proposal to consider the concept of episodic memory as a specific form of declarative memory that allows us to explicitly remember individually experienced events within their context, a consensus has been emerging that the hippocampus, a medial temporal lobe structure, is crucially involved in the encoding, storage and retrieval of spatial and nonspatialIntegration of exteroceptive and interoceptive information episodic memories (Cohen and Eichenbaum, 1993; Eichenbaum et al, 2012; Rolls, 2013). Memory of the context in which a reward or punishment has been received can become reactivated through explicit or implicit recall processes (Lisman and Redish, 2009) This reactivation is thought of as a prospective use of episodic memory traces for anticipating future events and selecting strategic actions (Lee et al, 2006; Shohamy et al, 2009). In both cases, the specific contribution of the hippocampus is related to its unique ability to rapidly learn and use bindings of arbitrary relations among separate perceptual features of an experience (Cohen and Eichenbaum, 1993; O’Reilly and Rudy, 2001). Both CA3a and CA3b (close to CA1) have strong recurrent connections and relatively few connections with CA1, whereas CA3c (close to the DG) has relatively few recurrent connections but sends strong projections to CA1 (Hunsaker et al, 2008)
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