Noradrenergic neuromodulation of nonlinear bursting neurons controls critical dynamics

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.