[Paper Review] Self-Organized Criticality Explains Readiness Potential

Katsushi Kagaya, Tomoyuki Kubota+1 more|arXiv (Cornell University)|Sep 19, 2022

Neural dynamics and brain function4 citations

TL;DR

This paper demonstrates that dendritic activity in crayfish motor neurons exhibits self-organized criticality (SOC), with neuronal avalanches following power-law distributions in size and duration, and satisfying the crackling noise relation. The readiness potential—observed before voluntary behavior—emerges from these scale-invariant avalanches, suggesting SOC as a universal mechanism for volition across species.

ABSTRACT

Readiness potential is a widely observed brain activity in several species including crayfish before the spontaneous behavioral initiation. However, it is poorly understood how this spontaneous activity is generated. The hypothesis that some specific, dedicated site is responsible for the spontaneity has been questioned. Here, by using intracellular recording and staining of the brain neurons in crayfish and modeling using the sandpile, which is the original model of self-organized criticality (SOC), we show that readiness potential can emerge everywhere in the brain because it is a SOC system. Despite the diversity in neurons and their morphology, brain neurons showed signatures of criticality and readiness potential. We find that the previously known readiness potential in a neuron is a consequence of the critical behavior of the entire network. Indeed, seemingly unrelated membrane potential activity in neurons in different animals can shape readiness potential when its time series are averaged after their alignment with respect to the spontaneous behavioral initiation. We show that the sandpile model not made for the potential, can form the premovement buildup activity similar to readiness potential. Scaling properties of the synaptic avalanches are in line with those of vertebrate species; thus, not only is the critical brain hypothesis supported in crayfish, but our findings might also provide a unified view of the basis of spontaneity in animal behavior.

Motivation & Objective

• To investigate whether dendritic neuronal activity in crayfish exhibits signatures of self-organized criticality (SOC).
• To determine if the readiness potential, a pre-movement brain signal observed across species, arises from SOC dynamics.
• To test whether the same critical dynamics underlie both voluntary and reflexive behaviors in the same nervous system.
• To extend the critical brain hypothesis to single neurons and invertebrate systems using intracellular recordings.
• To establish universality of SOC in neural dynamics by comparing with vertebrate extracellular data and theoretical models.

Proposed method

• Performed intracellular recordings from identified readiness potential neurons in crayfish during spontaneous, behaviorally silent states.
• Defined dendritic neuronal avalanches based on synaptic summation size and duration, using thresholding and detrending of recorded signals.
• Applied power-law fitting to avalanche size and duration distributions to test for scale-invariance.
• Evaluated the crackling noise relation: (τ−1)/(α−1) = γ, where α and τ are power-law exponents of size and duration, and γ is the spectral exponent.
• Used robustness to initial conditions and natural variations in dendritic morphology to assess self-organization.
• Compared scaling functions and exponents with the BTW sandpile model, stochastic random walk model of readiness potential, and vertebrate neuronal avalanche data.

Experimental results

Research questions

• RQ1 Do dendritic activities in crayfish motor neurons exhibit power-law distributed avalanches characteristic of self-organized criticality?
• RQ2 Is the readiness potential in crayfish shaped by scale-invariant neuronal avalanches rather than a deterministic trigger?
• RQ3 Do both voluntary and reflexive neural circuits in crayfish exhibit the same critical scaling behavior?
• RQ4 Can the universality of the critical brain hypothesis be extended to single neurons in invertebrates using intracellular data?
• RQ5 Is the emergence of the readiness potential a direct consequence of SOC dynamics without fine-tuned parameters?

Key findings

• Dendritic neuronal avalanches in crayfish readiness potential neurons follow power-law distributions in size and duration, with exponents consistent with criticality.
• The crackling noise relation (τ−1)/(α−1) = γ was satisfied, confirming the presence of scale-invariant dynamics across multiple individuals.
• Scaling functions for avalanche shapes were universal across crayfish individuals, despite natural variations in dendritic morphology.
• The same critical dynamics were observed in both voluntary walking circuits and reflexive escape circuits, indicating a shared underlying mechanism.
• The readiness potential emerged spontaneously from SOC dynamics without a single trigger neuron or external stimulus.
• The findings support the universality of self-organized criticality as a default neural mechanism for volition across the animal phylogenetic tree.