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Temporal signatures of criticality in human cortical excitability as probed by early somatosensory responses

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Stephani,  Tilman
Department Neurology, MPI for Human Cognitive and Brain Sciences, Max Planck Society;
International Max Planck Research School on Neuroscience of Communication: Function, Structure, and Plasticity, MPI for Human Cognitive and Brain Sciences, Max Planck Society;

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Villringer,  Arno
Department Neurology, MPI for Human Cognitive and Brain Sciences, Max Planck Society;
Berlin School of Mind and Brain, Humboldt University Berlin, Germany;
Clinic for Cognitive Neurology, University of Leipzig, Germany;

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Nikulin,  Vadim V.
Department Neurology, MPI for Human Cognitive and Brain Sciences, Max Planck Society;
Bernstein Center for Computational Neuroscience, Berlin, Germany;
Institute of Cognitive Neuroscience, National Research University Higher School of Economics, Moscow, Russia;

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Zitation

Stephani, T., Waterstraat, G., Haufe, S., Curio, G., Villringer, A., & Nikulin, V. V. (2020). Temporal signatures of criticality in human cortical excitability as probed by early somatosensory responses. The Journal of Neuroscience, 40(34), 6572-6583. doi:10.1523/JNEUROSCI.0241-20.2020.


Zitierlink: https://hdl.handle.net/21.11116/0000-0006-BFEF-7
Zusammenfassung
Brain responses vary considerably from moment to moment, even to identical sensory stimuli. This has been attributed to changes in instantaneous neuronal states determining the system’s excitability. Yet the spatio-temporal organization of these dynamics remains poorly understood. Here we test whether variability in stimulus-evoked activity can be interpreted within the framework of criticality, which postulates dynamics of neural systems to be tuned towards the phase transition between stability and instability as is reflected in scale-free fluctuations in spontaneous neural activity. Using a novel non-invasive approach in 33 male participants, we tracked instantaneous cortical excitability by inferring the magnitude of excitatory post-synaptic currents from the N20 component of the somatosensory evoked potential. Fluctuations of cortical excitability demonstrated long-range temporal dependencies decaying according to a power law across trials – a hallmark of systems at critical states. As these dynamics covaried with changes in pre-stimulus oscillatory activity in the alpha band (8–13 Hz), we establish a mechanistic link between ongoing and evoked activity through cortical excitability and argue that the co-emergence of common temporal power laws may indeed originate from neural networks poised close to a critical state. In contrast, no signatures of criticality were found in subcortical or peripheral nerve activity. Thus, criticality may represent a parsimonious organizing principle of variability in stimulus-related brain processes on a cortical level, possibly reflecting a delicate equilibrium between robustness and flexibility of neural responses to external stimuli.