Organization of complex memories in the mammalian brain - testing basic assumptions of systems consolidation theories

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Memory for experiences encompasses various sensory modalities that are stored in distinct brain areas. For example, a memory of a remarkable dinner may contain knowledge about how the food tasted, which is stored in the gustatory system, or of how a vase on the table looked like, which is supported by the system mediating object knowledge. Although the bits and pieces that together make up the experience were stored in a distributed manner, our memory of the event is an integrated whole. How the brain achieves this integration is referred to as the binding problem. Current theories propose a hierarchical memory system in which distributed neocortical sites are indirectly associated by ways of a central hub , which itself approximates an auto associative network with dense interconnections among its constituting neurons. The two most recent models based on this idea - the standard model of systems consolidation (SMC, e.g., Alvarez & Squire, 1994) and multiple-trace theory (MTT, e.g., Nadel & Moscovitch, 1997) - suggest that, due to its anatomy and connectivity, the hippocampus links the neocortical areas, which encode the stimuli that together constitute memory for an event.These memory models have not been explicitly developed to account for the binding problem, but to explain retrograde amnesia, i.e., the observation that recent but not remote memories critically depend on the hippocampus {e.g., Zola-Morgan & Squire, 1990). Both theories suggest that over time associations between the distributed neocortical areas that store the various elements of a memory are formed with the help of the hippocampus. The theories differ in respect to the role of the hippocampus in remote memories. While the standard model proposes that remote memories are lacking a corresponding hippocampal component, MTT ascribes to it a role for the entire lifetime of a memory in providing the spatial context.What has received little empirical attention are the assumptions regarding the distributed nature of memory, and the predictions regarding qualitative changes in memory over time and as a function of hippocampal damage. For example, so far no behavioral test reliably assesses whether a distributed functional network mediates memories, whether memories qualitatively change over time, and the qualitative and time-dependent contribution of the hippocampus to these memories. We exploit advanced concepts in systems neuroscience with new behavioral paradigms that permit testing whether the qualitative nature of memories changes with time. In addition, we propose an innovative task to study whether the hippocampus plays a binding role, and if so, if its role is transient until the connections between neocortical areas contributing to memory have matured. This paradigm is based on recognition memory for stimuli that are composed of two modalities. According to theory, for recent memories presentation of one modality on a retention test should activate the other modality via the hippocampus. However, for remote memories, presentation of one modality should lead to activation of the second one in a manner independent of the hippocampus. Together, these experiments will directly test behaviorally the postulated functional role of the hippocampus as a transient binding agent.