Non-synaptic plasticity enables memory-dependent local learning

Abstract

Synaptic plasticity is essential for memory formation and learning in the brain. In addition, recent results indicate that non-synaptic plasticity processes such as the regulation of neural membrane properties contribute to memory formation, its functional role in memory and learning has however remained elusive. Here, we propose that non-synaptic and synaptic plasticity are both essential components to enable memory-dependent processing in neuronal networks. While the former acts on a fast time scale for rapid information storage, the latter shapes network processing on a slower time scale to harness this memory as a functional component. We analyse this concept in a network model where pyramidal neurons regulate their apical trunk excitability in a Hebbian manner. We find that local synaptic plasticity rules can be derived for this model and show that the interplay between this synaptic plasticity and the non-synaptic trunk plasticity enables the model to successfully accommodate memory-dependent processing capabilities in a number of tasks, ranging from simple memory tests to question answering. The model can also explain contextual fear conditioning experiments, where freezing responses could be recovered by optogenetic reactivation of memory engrams under amnesia. Author summaryHow memory is organized in the brain in order to enable cognitive processing is a central open question in systems neuroscience. Traditionally, synaptic plasticity is considered the key mechanism for the establishment of memory in the brain. Recently however, this view has been questioned, and it was proposed that non-synaptic plasticity mechanisms play a more prominent role as previously considered. In this article, we propose that both, synaptic and non-synaptic plasticity are central components for the formation and utilization of memory in biological neuronal networks. Our results show that non-synaptic plasticity can act on a fast time-scale to store important information, while synaptic plasticity can adapt network function on a slow time scale in order to facilitate memory-dependent cognitive processing.