Noradrenergic neuromodulation of nonlinear bursting neurons controls critical dynamics

TL;DR

This study demonstrates how noradrenaline modulates neuronal criticality in the brain, balancing sensitivity and stability through nonlinear bursting neurons, with implications for understanding neuromodulatory control of brain dynamics.

Contribution

It provides empirical evidence linking noradrenaline levels to critical brain dynamics and introduces a dual-compartment neuron model to explain these effects.

Findings

Neuronal spiking in mice is near a critical point and fluctuates with neuromodulatory tone.

Noradrenaline modulates criticality in neurons, following an inverted-U profile.

Intermediate noradrenaline levels produce burst avalanches with power-law distributions.

Abstract

In order to remain adaptable to a dynamic environment, neural activity must be simultaneously both sensitive and stable. To solve this problem, the brain has been hypothesised to sit near a critical boundary. Yet, precisely how criticality and these opposing information processing modes are implemented in the brain remains elusive. A potential solution to this problem involves modulating intrinsically nonlinear neurons within the cerebral cortex with neuromodulatory neurotransmitters such as noradrenaline, a highly-conserved chemical released from the pontine locus coeruleus. Here we confirm that neuronal spiking in mice is poised close to the critical point of a branching process and that time-varying signatures of criticality fluctuate with neuromodulatory tone, as assessed by dynamic alterations in pupil diameter. We explore these results theoretically by creating a dual-compartment model of non-linear pyramidal neurons - capable of both regular spike and bursting modes - that replicates our main empirical findings of slightly subcritical dynamics. We then probe our model at a resolution impossible in vivo to demonstrate that noradrenaline differentially alters spiking- and bursting-criticality to facilitate sensitive and stable dynamics following an inverted-U profile that peaks at intermediate noradrenergic tone. Finally, we demonstrate that this intermediate noradrenergic regime displays burst avalanches with power-law size and duration distributions and scaling relationship belonging to the universality class of self-organized criticality. Our results confirm that the noradrenergic ascending arousal system acts as a control parameter for emergent critical dynamics in the brain. This methodology could be extended to explore other neuromodulators as control parameters of the brain.