Emergence and maintenance of modularity in neural networks with Hebbian and anti-Hebbian inhibitory STDP

Abstract

The modular and hierarchical organization of the brain is believed to support the coexistence of segregated (specialization) and integrated (binding) information processes. A relevant question is yet to understand how such architecture naturally emerges and is sustained over time, given the plastic nature of the brain's wiring. Following evidences that the sensory cortices organize into assemblies under selective stimuli, it has been shown that stable neuronal assemblies can emerge due to targeted stimulation, embedding various forms of synaptic plasticity in presence of homeostatic and/or control mechanisms. Here, we show that simple spike-timing-dependent plasticity (STDP) rules, based only on pre- and post-synaptic spike times, can also lead to the stable encoding of memories in the absence of any control mechanism. We develop a model of spiking neurons, trained by stimuli targeting different sub-populations. The model satisfies some biologically plausible features: (i) it contains excitatory and inhibitory neurons with Hebbian and anti-Hebbian STDP; (ii) neither the neuronal activity nor the synaptic weights are frozen after the learning phase. Instead, the neurons are allowed to fire spontaneously while synaptic plasticity remains active. We find that only the combination of two inhibitory STDP sub-populations allows for the formation of stable modules in the network, with each sub-population playing a distinctive role. The Hebbian sub-population controls for the firing activity, while the anti-Hebbian neurons promote pattern selectivity. After the learning phase, the network settles into an asynchronous irregular resting-state. This post-learning activity is associated with spontaneous memory recalls which turn out to be fundamental for the long-term consolidation of the learned memories. Due to its simplicity, the introduced model can represent a test-bed for further investigations on the role played by STDP on memory storing and maintenance.

This work was supported (RB, GD and GZL) by the European Union's Horizon 2020 Framework Programme for Research and Innovation under the Specific [Grant Agreement No. 945539 (Human Brain Project SGA3)] and by an EUTOPIA funding [EUTOPIA-PhD-2020-0000000066 - NEUROAI]. AT received financial support by the Labex MME-DII [Grant No. ANR-11-LBX-0023-01] (together with MQ), by the ANR Project ERMUNDY [Grant No. ANR-18-CE37-0014] and by CY Generations (Grant No. ANR-21-EXES-0008) all part of the French program 'Investissements d'Avenir.' GD is supported by Grant PID2022-136216NB-I00 funded by MICIU/AEI/10.13039/501100011033 and by 'ERDF A way of making Europe,'ERDF. MQ is also partially supported by CNRS through the IPAL lab in Singapore. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.