Self-organization of multiple spatial and context memories in the hippocampus

One obstacle to understanding the exact processes unfolding inside the hippocampus is that it is still difficult to clearly define what the hippocampus actually does, at the system level. Associated for a long time with the formation of episodic and semantic memories, and with their temporary storage, the hippocampus is also regarded as a structure involved in spatial navigation. These two independent perspectives on the hippocampus are not necessarily exclusive: proposals have been put forward to make them fit into the same conceptual frame.We review both approaches and argue that three critical developments need consideration: (a) recordings of neuronal activity in rodents, revealing beautiful spatial codes expressed in entorhinal cortex, upstream of the hippocampus; (b) comparative behavioral results suggesting, in an evolutionary perspective, qualitative similarity of function across homologous structures with a distinct internal organization; (c) quantitative measures of information, shifting the focus from who does what to how much each neuronal population expresses each code.These developments take the hippocampus away from philosophical discussions of all-or-none cause–effect relations, and into the quantitative mainstream of modern neural science.

► We review theoretical perspectives on hippocampal function.
► The similarity of function across vertebrate phyla is contrasted with the specificity of hippocampal internal organization in mammals.
► Information measures are proposed as essential for addressing structure–function relations at the required quantitative level.
► Original measures of spatial and contextual information content are presented for mEC and CA3 model data and for CA3 real data.