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

View ORCID ProfileT. Stephani, G. Waterstraat, S. Haufe, G. Curio, A. Villringer, V. V. Nikulin
doi: https://doi.org/10.1101/809285
T. Stephani
1Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany, 04103
2International Max Planck Research School NeuroCom, Leipzig, Germany, 04103
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  • ORCID record for T. Stephani
  • For correspondence: stephani@cbs.mpg.de nikulin@cbs.mpg.de
G. Waterstraat
3Neurophysics Group, Department of Neurology, Charité – Universitätsmedizin Berlin, Berlin, Germany, 12200
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S. Haufe
4Berlin Center for Advanced Neuroimaging, Charité – Universitätsmedizin Berlin, Berlin, Germany, 10117
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G. Curio
3Neurophysics Group, Department of Neurology, Charité – Universitätsmedizin Berlin, Berlin, Germany, 12200
5Bernstein Center for Computational Neuroscience, Berlin, Germany, 10115
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A. Villringer
1Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany, 04103
6Berlin School of Mind and Brain, Humboldt-Universität zu Berlin, Berlin, Germany, 10117
7Clinic for Cognitive Neurology, University Hospital Leipzig, Leipzig, Germany, 04103
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V. V. Nikulin
1Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany, 04103
8Center for Cognition and Decision Making, National Research University Higher School of Economics, Moscow, Russian Federation, 101000
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  • For correspondence: stephani@cbs.mpg.de nikulin@cbs.mpg.de
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Abstract

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.

Significance Statement Variability of neural responses in primary sensory areas is puzzling, as it is detrimental to the exact mapping between stimulus features and neural activity. However, such variability can be beneficial for information processing in neural networks if it is of a specific nature, namely if dynamics are poised at a so-called critical state characterized by a scale-free spatio-temporal structure. Here, we demonstrate the existence of a link between signatures of criticality in ongoing and evoked activity through cortical excitability, which fills the long-standing gap between two major directions of research on neural variability: The impact of instantaneous brain states on stimulus processing on the one hand and the scale-free organization of spatio-temporal network dynamics of spontaneous activity on the other.

Footnotes

  • Conflict of interest statement: The authors declare no competing financial interests.

  • Figures revised and text refined.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted January 31, 2020.
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Temporal signatures of criticality in human cortical excitability as probed by early somatosensory responses
T. Stephani, G. Waterstraat, S. Haufe, G. Curio, A. Villringer, V. V. Nikulin
bioRxiv 809285; doi: https://doi.org/10.1101/809285
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Temporal signatures of criticality in human cortical excitability as probed by early somatosensory responses
T. Stephani, G. Waterstraat, S. Haufe, G. Curio, A. Villringer, V. V. Nikulin
bioRxiv 809285; doi: https://doi.org/10.1101/809285

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