Optimal noise level for coding with tightly balanced networks of spiking neurons in the presence of transmission delays

• Published in: PLoS computational biology Vol. 18; no. 10; p. e1010593
• Main Authors: Timcheck, Jonathan, Kadmon, Jonathan, Boahen, Kwabena, Ganguli, Surya
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 01.10.2022; Public Library of Science (PLoS)
• Subjects: Action Potentials - physiology; Analysis; Biology and Life Sciences; Channel noise; Circuits; Coding; Computational neuroscience; Computer and Information Sciences; Dynamic tests; Efficiency; Error analysis; Firing pattern; Ion channels; Mathematical analysis; Medicine and Health Sciences; Methods; Models, Neurological; Nerve Net - physiology; Neural circuitry; Neural coding; Neural networks; Neural Networks, Computer; Neurons; Neurons - physiology; Noise control; Noise levels; Noise prediction; Noise propagation; Spiking; Synaptic transmission; Synaptic Transmission - physiology; Synchronism; Synchronization; Israel
• ISSN: 1553-7358; 1553-734X; 1553-7358
• DOI: 10.1371/journal.pcbi.1010593

Neural circuits consist of many noisy, slow components, with individual neurons subject to ion channel noise, axonal propagation delays, and unreliable and slow synaptic transmission. This raises a fundamental question: how can reliable computation emerge from such unreliable components? A classic strategy is to simply average over a population of N weakly-coupled neurons to achieve errors that scale as 1 / N . But more interestingly, recent work has introduced networks of leaky integrate-and-fire (LIF) neurons that achieve coding errors that scale superclassically as 1/ N by combining the principles of predictive coding and fast and tight inhibitory-excitatory balance. However, spike transmission delays preclude such fast inhibition, and computational studies have observed that such delays can cause pathological synchronization that in turn destroys superclassical coding performance. Intriguingly, it has also been observed in simulations that noise can actually improve coding performance, and that there exists some optimal level of noise that minimizes coding error. However, we lack a quantitative theory that describes this fascinating interplay between delays, noise and neural coding performance in spiking networks. In this work, we elucidate the mechanisms underpinning this beneficial role of noise by deriving analytical expressions for coding error as a function of spike propagation delay and noise levels in predictive coding tight-balance networks of LIF neurons. Furthermore, we compute the minimal coding error and the associated optimal noise level, finding that they grow as power-laws with the delay. Our analysis reveals quantitatively how optimal levels of noise can rescue neural coding performance in spiking neural networks with delays by preventing the build up of pathological synchrony without overwhelming the overall spiking dynamics. This analysis can serve as a foundation for the further study of precise computation in the presence of noise and delays in efficient spiking neural circuits.