P120 Critical neuronal avalanches emerge from excitation-inhibition balanced spontaneous activity
Maxime Janbon1, Mateo Amortegui1, Enrique Hansen1, Sarah Nourin1, Germán Sumbre1,Adrián Ponce-Alvarez*2,3,4
1Institut de Biologie de l’ENS (IBENS), Département de biologie, École normale supérieure, CNRS, INSERM, Université PSL, 75005 Paris, France
2Departament de Matemàtiques, Universitat Politècnica de Catalunya, 08028 Barcelona, Spain.
3Institut de Matemàtiques de la UPC - Barcelona Tech (IMTech), Barcelona, Spain.
4Centre de Recerca Matemàtica, Barcelona, Spain.
*Email : adrian.ponce@upc.edu
Introduction
Neural systems exhibit cascading activity patterns called neuronal avalanches that follow power-law statistics, a hallmark of critical systems. Theoretical models [1,2] and in vitro studies [3] suggest that the excitation-inhibition (E/I) balance is a key factor in the self-organization of criticality. However, how E and I dynamics evolve and interact during in vivo neuronal avalanches remains unclear.
Here, we investigated E and I neuron contributions to spontaneous neuronal avalanches using double-transgenic zebrafish expressing cell-type-specific fluorescence proteins and calcium indicators. Furthermore, we built a stochastic E-I network model to explore how critical avalanches depend on the E/I ratio.
Methods
We monitored spontaneous neuronal activity in the optic tectum of 10 zebrafish larvae using selective-plane illumination microscopy (SPIM). Double-transgenic larvae expressing GCaMP6f and mCherry under the Vglut2a promoter (glutamatergic) were combined with immunostaining for GABAergic and cholinergic neurons, allowing identification of excitatory (E), inhibitory (I), and cholinergic (Ch) neurons.
We modelled the collective activity of E and I neurons using a model of critical dynamics that combines stochastic Wilson-Cowan equations[1,4],spatial embedded neuronal connectivity,and a spike-to-fluorescence convolutional model. Critical avalanches arise throughbalanced amplification[1] at a phase transition.
Results
Our results show that spontaneous fluctuations in E and I activity influenced neuronal avalanche statistics in the zebrafish optic tectum. Neuronal avalanches approached criticality when excitatory and inhibitory activity were balanced. Notably, the model accurately captured the observed avalanche statistics and their sensitivity to E/I fluctuations around a critical point defined by balanced excitatory and inhibitory synaptic strengths. Furthermore, the model allowed us to evaluate the statistics of neuronal avalanches derived from different simulated signals, representing calcium events or spiking activity. For both signals, the model's critical exponents align with experimental findings from calcium imaging and electrophysiology [5].
Discussion
Extensive research underscores the functional benefits of E/I balance and critical dynamics. Balanced networks enhance signal amplification, response selectivity, noise reduction, stability, memory, and plasticity [6-8], while critical dynamics optimize information processing [9-11]. Here, we showed that neuronal avalanche statistics and their dependence on spontaneous E/I fluctuations in the zebrafish optic tectum align with a model reaching criticality for balanced E and I couplings. Our study provides a framework to dissect the relationship between criticality and E/I balance, by manipulating the E/I ratio in vivo. Future integration of optogenetics into the present experiments and model will further clarify this interplay.
Acknowledgements
This study was supported by the Project PID2022-137708NB-I00 funded by MICIU/AEI /10.13039/501100011033 and FEDER, UE.A. Ponce-Alvarezwas supported by a Ramón y Cajal fellowship (RYC2020-029117-I) funded by MICIU/AEI/10.13039/501100011033 and “ESF Investing in your future”. G. Sumbre was supported by ERC CoG 726280.
References
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