Abstract
Formation of new synapses between neurons is an essential mechanism for learning and encoding memories. The vast majority of excitatory synapses occur on dendritic spines, therefore, the growth dynamics of spines is strongly related to the plasticity timescales. Especially in the early stages of the developing brain, there is an abundant number of long, thin and motile protrusions (i.e., filopodia), which develop in timescales of seconds and minutes. Because of their unique morphology and motility, it has been suggested that filopodia can have a dual role in both spinogenesis and environmental sampling of potential axonal partners. I propose that filopodia can lower the threshold and reduce the time to form new dendritic spines and synapses, providing a substrate for fast learning. Based on this proposition, the functional role of filopodia during brain development is discussed in relation to learning and memory. Specifically, it is hypothesized that the postnatal brain starts with a single-stage memory system with filopodia playing a significant role in rapid structural plasticity along with the stability provided by the mushroom-shaped spines. Following the maturation of the hippocampus, this highly-plastic unitary system transitions to a two-stage memory system, which consists of a plastic temporary store and a long-term stable store. In alignment with these architectural changes, it is posited that after brain maturation, filopodia-based structural plasticity will be preserved in specific areas, which are involved in fast learning (e.g., hippocampus in relation to episodic memory). These propositions aim to introduce a unifying framework for a diversity of phenomena in the brain such as synaptogenesis, pruning and memory consolidation.
Highlights
Learning and memory encoding in the brain are based on changes in synaptic connections between neurons
According to Watson et al (2016), long-term potentiation (LTP) in the adult hippocampus produces synapse enlargement and prevents the formation of new dendritic spines. These findings support the view that LTP is fundamentally a form of synaptic plasticity rather than a process that promotes the rewiring of the neural network
The physiological processes underlying structural plasticity can be orders of magnitude slower than the mechanisms involved in synaptic plasticity
Summary
Learning and memory encoding in the brain are based on changes in synaptic connections between neurons. According to Watson et al (2016), LTP in the adult hippocampus produces synapse enlargement and prevents the formation of new dendritic spines These findings support the view that LTP is fundamentally a form of synaptic plasticity rather than a process that promotes the rewiring of the neural network. I hypothesize that both fast (single trial) and slow (many trial) learning in the developing brain are governed by a single-stage memory system, where filopodiumguided synaptogenesis (for excitatory synapses) provides a global and rapid mechanism of plasticity, supported by the rapid generation and elimination of filopodia. The idea that filopodia and spines can play two different roles in rapid plasticity and stability is a type of metaplasticity argument This is a metabolically expensive solution as it results in generating high numbers of new synapses and considering that most brain energy is used on synaptic transmission (Harris et al, 2012). Given the developing understanding of brain’s energy budget, more detailed models and measurements are needed to make more conclusive comments on this issue
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