Autonomous emergence of connectivity assemblies via spike triplet interactions

Abstract

Non-random connectivity can emerge without structured external input driven by activitydependent mechanisms of synaptic plasticity based on precise spiking patterns. Here we analyze the emergence of global structures in recurrent networks based on a triplet model of spike timing dependent plasticity (STDP), which depends on the interactions of three precisely-timed spikes, and can describe plasticity experiments with varying spike frequency better than the classical pair-based STDP rule. We derive synaptic changes arising from correlations up to third-order and describe them as the sum of structural motifs, which determine how any spike in the network influences a given synaptic connection through possible connectivity paths. This motif expansion framework reveals novel structural motifs under the triplet STDP rule, which support the formation of bidirectional connections and ultimately the spontaneous emergence of global network structure in the form of self-connected groups of neurons, or assemblies. We propose that under triplet STDP assembly structure can emerge without the need for externally patterned inputs or assuming a symmetric pairbased STDP rule common in previous studies. The emergence of non-random network structure under triplet STDP occurs through internally-generated higher-order correlations, which are ubiquitous in natural stimuli and neuronal spiking activity, and important for coding. We further demonstrate how neuromodulatory mechanisms that modulate the shape of the triplet STDP rule or the synaptic transmission function differentially promote structural motifs underlying the emergence of assemblies, and quantify the differences using graph theoretic measures.

Memories in a network with excitatory and inhibitory plasticity are encoded in the spiking irregularity

“…It is not completely clear, however, what exactly drives the formation of assemblies in the brain. It has been recently proposed that correlated input could drive assembly formation even in the absence of rate-based plasticity mechanisms [6] and that assemblies could also form spontaneously in the absence of structured external stimulation [7]. Future work could extend our current analysis and form silent EI assemblies without the transient increase in mean firing rate by stimulation of assembly neurons.…”

“…How exactly cell assemblies are formed and how their synapses and firing activity encode information, however, is yet to be fully understood. Theoretical work [2][3][4][5][6][7][8] has shown it is possible to create such assemblies by combining different forms of synaptic plasticity. In some of these models [3,4], when strongly connected assemblies are formed, spontaneous activity is characterized by an overall stable firing rate across the excitatory population, but with the firing rate of individual assemblies transitioning between periods of high and low activity.…”

Sequence memory in recurrent neuronal network can develop without structured input

“…Previous studies have analysed the development of mainly excitatory networks with spike-timing dependent plasticity under spontaneous activity, and some speculated on its impact on sequence memory: Analytical studies showed that STDP can autonomously develop feed-forward structures [Ocker et al, 2015, Ravid Tannenbaum and Burak, 2016, Montangie et al, 2020]. Numerical studies confirm this result: Networks equipped with STDP and a form of synaptic normalisation converge to form multiple synfire chains under both sequence and noise input [Fiete et al, 2010, Weissenberger et al, 2017].…”

Balanced networks under spike-time dependent plasticity

“…Higher order interactions are at the heart of triplet rules [47,[68][69][70], and other types of interactions may also be important, e.g. for calcium-based update rules [71,72].…”

“…In particular, Ravid Tannenbaum et al showed that in networks of Poisson neurons synfire chains and self connected assemblies can emerge autonomously in recurrent networks [46]. Montangie et al showed that a more realistic form of STDP based on spike triplets also leads to autonomous emergence of assemblies [47].…”