Autonomous emergence of connectivity assemblies via spike triplet interactions

Non-random connectivity can emerge without structured external input driven by activity-dependent 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 pair-based 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.Author summary: Emergent non-random connectivity structures in different brain regions are tightly related to specific patterns of neural activity and support diverse brain functions. For instance, self-connected groups of neurons, known as assemblies, have been proposed to represent functional units in brain circuits and can emerge even without patterned external instruction. Here we investigate the emergence of non-random connectivity in recurrent networks using a particular plasticity rule, triplet STDP, which relies on the interaction of spike triplets and can capture higher-order statistical dependencies in neural activity. We derive the evolution of the synaptic strengths in the network and explore the conditions for the self-organization of connectivity into assemblies. We demonstrate key differences of the triplet STDP rule compared to the classical pair-based rule in terms of how assemblies are formed, including the realistic asymmetric shape and influence of novel connectivity motifs on network plasticity driven by higher-order correlations. Assembly formation depends on the specific shape of the STDP window and synaptic transmission function, pointing towards an important role of neuromodulatory signals on formation of intrinsically generated assemblies.