Temporal Signatures of Criticality in Human Cortical Excitability as Probed by Early Somatosensory Responses

• Published in: The Journal of neuroscience Vol. 40; no. 34; pp. 6572 - 6583
• Main Authors: Stephani, Tilman, Waterstraat, Gunnar, Haufe, Stefan, Curio, Gabriel, Villringer, Arno, Nikulin, Vadim V
• Format: Journal Article
• Language: English
• Published: United States Society for Neuroscience 19.08.2020
• Subjects: Adult; Alpha Rhythm; Brain; Cortical Excitability; Electric Stimulation; Evoked Potentials, Somatosensory; Excitability; Excitatory postsynaptic potentials; External stimuli; Fluctuations; Humans; Male; Median Nerve - physiology; Neural networks; Peripheral nerves; Phase transitions; Sensory stimuli; Signal Processing, Computer-Assisted; Signatures; Somatosensory Cortex - physiology; Somatosensory evoked potentials; Stimuli; Touch Perception - physiology; Variability; Young Adult; criticality; complexity; somatosensory; excitability; oscillations; EEG
• ISSN: 0270-6474; 1529-2401
• DOI: 10.1523/jneurosci.0241-20.2020

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 spatiotemporal 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 toward the phase transition between stability and instability as is reflected in scale-free fluctuations in spontaneous neural activity. Using a novel noninvasive approach in 33 male human participants, we tracked instantaneous cortical excitability by inferring the magnitude of excitatory postsynaptic 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 prestimulus 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. 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 spatiotemporal 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 spatiotemporal network dynamics of spontaneous activity on the other.