The interplay of synaptic plasticity and scaling enables self-organized formation and allocation of multiple memory representations

Abstract

It is commonly assumed that memories about experienced stimuli are represented in the brain by groups of highly interconnected neurons called Hebbian cell assemblies. This requires allocating and storing information in the neural circuitry, which happens through synaptic weight adaptation. It remains, however, largely unknown how memory allocation and storage can be achieved and coordinated to allow for a faithful representation of multiple memories without disruptive interference between them. In this theoretical study, we show that the interplay between conventional Hebbian synaptic plasticity and homeostatic synaptic scaling organizes synaptic weight adaptations such that, on the one hand, a new stimulus forms a new memory while, on the other hand, different stimuli are assigned to distinct Hebbian cell assemblies. We show that the resulting dynamics can reproduce experimental in-vivo data focusing on how other neuronal and synaptic factors, such as neuronal excitability and network connectivity, influence memory formation. Thus, the here presented model suggests that a few fundamental synaptic mechanisms may suffice to implement memory allocation and storage in neural circuitry. Author summaryThe survival in a changing environment requires the reliable learning, storage, and organization of relevant stimuli in the neuronal circuit. This theoretical work addresses the important issue of how a neuronal circuit coordinates the learning-related synaptic adaptations to properly assign new information to groups of neurons and to form long-lasting memory representations of multiple stimuli. We show that this requires only three synaptic properties -homosynaptic potentiation paired with heterosynaptic depression both driven by the postsynaptic activity level. These properties naturally arise from the generic interplay between conventional Hebbian synaptic plasticity and homeostatic synaptic scaling. Therefore, this study shows that the complex processes of memory allocation and storage can be attributed to ubiquitous synaptic mechanisms in the neural circuitry.

Homeostatic mechanisms regulate distinct aspects of cortical circuit dynamics

“…Other modeling studies have investigated the interaction between Hebbian and homeostatic plasticity for the stable formation and maintenance of Hebbian assemblies in the context of memory storage and recall (43)(44)(45), which are different from the sensory deprivation paradigm studied here. Interestingly, a recent modeling framework for the homeostatic recovery from visual deprivation proposed that the disinhibitory effect of inhibitory plasticity, rather than synaptic scaling, can drive the recovery of firing rates and correlations in specific subnetworks of excitatory neurons (46), based on experimental results (40).…”

The Interplay of Synaptic Plasticity and Scaling Enables Self-Organized Formation and Allocation of Multiple Memory Representations

“…We thank Florentin Wörgötter for fruitful comments. This manuscript has been released as a pre-print at bioRxiv (Auth et al, 2018).…”