Effects of cellular homeostatic intrinsic plasticity on dynamical and computational properties of biological recurrent neural networks.
Homeostatic intrinsic plasticity (HIP) is a ubiquitous cellular mechanism regulating neuronal activity, cardinal for the proper functioning of nervous systems. In invertebrates, HIP is critical for orchestrating stereotyped activity patterns. The functional impact of HIP remains more obscure in vertebrate networks, where higher order cognitive processes rely on complex neural dynamics. The hypothesis has emerged that HIP might control the complexity of activity dynamics in recurrent networks, with important computational consequences. However, conflicting results about the causal relationships between cellular HIP, network dynamics, and computational performance have arisen from machine-learning studies. Here, we assess how cellular HIP effects translate into collective dynamics and computational properties in biological recurrent networks. We develop a realistic multiscale model including a generic HIP rule regulating the neuronal threshold with actual molecular signaling pathways kinetics, Dale's principle, sparse connectivity, synaptic balance, and Hebbian synaptic plasticity (SP). Dynamic mean-field analysis and simulations unravel that HIP sets a working point at which inputs are transduced by large derivative ranges of the transfer function. This cellular mechanism ensures increased network dynamics complexity, robust balance with SP at the edge of chaos, and improved input separability. Although critically dependent upon balanced excitatory and inhibitory drives, these effects display striking robustness to changes in network architecture, learning rates, and input features. Thus, the mechanism we unveil might represent a ubiquitous cellular basis for complex dynamics in neural networks. Understanding this robustness is an important challenge to unraveling principles underlying self-organization around criticality in biological recurrent neural networks.
UMR CNRS 7102, Université Pierre et Marie Curie, 75005 Paris, France, NeuroMathComp Project Team, INRIA, 06902 Sophia Antipolis Cedex 2, France, BEAGLE, INRIA Rhône-Alpes, Université de Lyon, LIRIS, UMR5205, 69100 Villeurbanne, France, and Institut des Systèmes Intelligents et de Robotique, UMR CNRS 7222, Université Pierre et Marie Curie, 75005 Paris, France.
Jérémie
J
Naudé
Bruno
B
Cessac
Hugues
H
Berry
Bruno
B
Delord
D000200:Action Potentials / Q000502:physiology; D000818:Animals; D003198:Computer Simulation; D006706:Homeostasis / Q000502:physiology*; D006801:Humans; D008959:Models, Neurological; D009415:Nerve Net / Q000502:physiology; D016571:Neural Networks, Computer; D009473:Neuronal Plasticity / Q000502:physiology*; D009474:Neurons / Q000502:physiology*; D017711:Nonlinear Dynamics; D013569:Synapses / Q000502:physiology