Principles underlying the input-dependent formation and organization of memories

Abstract

The neuronal system exhibits the remarkable ability to dynamically store and organize incoming information into a web of memory representations (items), which is essential for the generation of complex behaviors. Central to memory function is that such memory items must be (1) discriminated from each other, (2) associated to each other, or (3) brought into a sequential order. However, how these three basic mechanisms are robustly implemented in an input-dependent manner by the underlying complex neuronal and synaptic dynamics is still unknown. Here, we develop a mathematical framework, which provides a direct link between different synaptic mechanisms, determining the neuronal and synaptic dynamics of the network, to create a network that emulates the above mechanisms. Combining correlation-based synaptic plasticity and homeostatic synaptic scaling, we demonstrate that these mechanisms enable the reliable formation of sequences and associations between two memory items still missing the capability for discrimination. We show that this shortcoming can be removed by additionally considering inhibitory synaptic plasticity. Thus, the here-presented framework provides a new, functionally motivated link between different known synaptic mechanisms leading to the self-organization of fundamental memory mechanisms. Higher-order animals are permanently exposed to a variety of environmental inputs that have to be processed and stored such that the animal can react appropriately. 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 unidirectionally related (sequence). However, the neuronal and synaptic dynamics underlying the formation of such structures are mainly unknown. To investigate possible links between physiological mechanisms and the organization of memories, in this work, we develop a general mathematical framework enabling an 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.

Keywords

• Synaptic plasticity
• Memory
• Memory interaction
• Synaptic scaling
• Inhibition