Principles underlying the input-dependent formation and organization of memories

The brain of higher-order animals continuously and dynamically learns and adapts according to variable, complex environmental conditions. For this, the neuronal system of an agent exhibits the remarkable ability to dynamically store and organize the information of plenty of different environmental stimuli into a web of memories, which is essential for the generation of complex behaviors. The basic structures of this web are the functional organizations between two memories such as discrimination, association, and sequences. However, how these basic structures are formed robustly in an input-dependent manner by the underlying, complex and high-dimensional neuronal and synaptic dynamics is still unknown. Here, we develop a mathematical framework which reduces the complexity in several stages such that we obtain a low-dimensional mathematical description. This provides a direct link between the involved synaptic mechanisms, determining the neuronal and synaptic dynamics of the network, with the ability of the network to form diverse functional organizations. Given two widely-known synaptic mechanisms, correlation-based synaptic plasticity and homeostatic synaptic scaling, we use this new framework to identify that the interplay of these mechanisms enables the reliable formation of sequences and associations between two memory representations - missing the important functional organization of discrimination. We can show that this shortcoming can be compensated by considering a third mechanism as inhibitory synaptic plasticity. Thus, the here-presented framework and results provide a new link between diverse synaptic mechanisms and emerging functional organizations of memories. Furthermore, given our mathematical framework, one can now investigate the principles underlying the formation of the web of memories. AUTHOR SUMMARY Higher-order animals are permanently exposed to a variety of environmental inputs which have to be processed and stored such that the animal can react appropriate. Thereby, the ongoing challenge for the neuronal system is to continuously store novel and meaningful stimuli and, dependent on their content, to integrate them into the existing web of knowledge or memories. The smallest organizational entity of such a web of memories is described by the functional relation of two interconnected memories: They can be either unrelated (discrimination), mutually related (association), or uni-directionally related (sequence). However, the neuronal and synaptic dynamics underlying the formation of such structures is mainly unknown. To investigate possible links between physiological mechanisms and the organization of memories, in this work, we develop a general mathematical framework enabling analytical approach. Thereby, we show that the well-known mechanisms of synaptic plasticity and homeostatic scaling in conjunction with inhibitory synaptic plasticity enables the reliable formation of all basic relations between two memories. This work provides a further step in the understanding of the complex dynamics underlying the organization of knowledge in neural systems.