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.

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 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.

大脑的反应有时甚至在相同的感觉刺激上也有很大差异。这是由于瞬时神经元状态的变化决定了系统的兴奋性。然而，这些动力的时空组织仍然知之甚少。在这里，我们测试是否可以在临界范围内解释刺激诱发活动的变异性，该临界度假定神经系统的动力学朝着稳定性和不稳定性之间的相变进行调整，这反映在自发性神经活动的无标度波动中。我们使用一种新颖的非侵入性方法对33位男性受试者进行了研究，我们通过从体感诱发电位的N20成分推断出兴奋性突触后电流的大小来跟踪瞬时皮质兴奋性。皮质兴奋性的波动表现出长期的时间依赖性随试验的幂律而衰减，这是系统处于临界状态的标志。由于这些动力学与α波段（8-13 Hz）中刺激前振荡活动的变化共变，因此我们通过皮层兴奋性在正在进行的活动和诱发的活动之间建立了机械联系，并指出常见的暂时幂定律的共同出现可能确实源自神经网络已接近临界状态。相反，在皮层下或周围神经活动中没有发现严重的征兆。因此，临界度可以代表皮层水平上与刺激相关的大脑过程的可变性的简约组织原理，

重要性声明初级感觉区域神经反应的变化令人困惑，因为这不利于刺激特征与神经活动之间的精确映射。但是，如果这种可变性具有特定的性质，也就是说，如果动力学处于以无标度的时空结构为特征的所谓的临界状态，则这种可变性对于神经网络中的信息处理可能是有益的。在这里，我们展示了通过皮层兴奋性在正在进行的和诱发的活动中的关键特征之间存在联系，这填补了神经变异性的两个主要研究方向之间的长期空白：瞬时大脑状态对刺激处理的影响。一方面是自发活动的时空网络动力学的无标度组织。