Department of Psychology, Northeastern University, Boston, Massachusetts 02115.
Department of Neurology & Neurological Sciences, Stanford University, Stanford, California 94304
J Neurosci. 2020 Aug 5;40(32):6207-6218. doi: 10.1523/JNEUROSCI.0435-20.2020. Epub 2020 Jul 6.
Spontaneous activations within neuronal populations can emerge similarly to "task-evoked" activations elicited during cognitive performance or sensory stimulation. We hypothesized that spontaneous activations within a given brain region have comparable functional and physiological properties to task-evoked activations. Using human intracranial EEG with concurrent pupillometry in 3 subjects (2 males, 1 female), we localized neuronal populations in the dorsal anterior insular cortex that showed task-evoked activations correlating positively with the magnitude of pupil dilation during a continuous performance task. The pupillary response peaks lagged behind insular activations by several hundreds of milliseconds. We then detected spontaneous activations, within the same neuronal populations of insular cortex, that emerged intermittently during a wakeful "resting state" and that had comparable electrophysiological properties (magnitude, duration, and spectral signature) to task-evoked activations. Critically, similar to task-evoked activations, spontaneous activations systematically preceded phasic pupil dilations with a strikingly similar temporal profile. Our findings suggest similar neurophysiological profiles between spontaneous and task-evoked activations in the human insula and support a clear link between these activations and autonomic functions measured by dynamics of pupillary dilation. Most of our knowledge about activations in the human brain is derived from studies of responses to external events and experimental conditions (i.e., "task-evoked" activations). We obtained direct neural recordings from electrodes implanted in human subjects and showed that activations emerge spontaneously and have strong similarities to task-evoked activations(e.g., magnitude, temporal profile) within the same populations of neurons. Within the dorsal anterior insula, a brain region implicated in salience processing and alertness, activations that are either spontaneous or task-evoked are coupled with brief dilations of the pupil. Our findings underscore how spontaneous brain activity, a major current focus of human neuroimaging studies aimed at developing biomarkers of disease, is relevant to ongoing physiological and possibly self-generated mental processes.
神经元群体中的自发性激活可以类似于认知表现或感觉刺激期间引起的“任务诱发”激活。我们假设，给定脑区中的自发性激活具有与任务诱发激活相当的功能和生理特性。使用 3 名受试者（2 名男性，1 名女性）的颅内 EEG 和瞳孔测量同步，我们定位了背侧前岛叶皮层中的神经元群体，这些神经元群体的激活与连续性能任务期间瞳孔扩张的幅度呈正相关。瞳孔反应峰滞后于岛叶激活数百毫秒。然后，我们在同一岛叶皮层的神经元群体中检测到间歇性出现的自发性激活，这些激活在清醒的“休息状态”下出现，并且具有与任务诱发激活相当的电生理特性（幅度、持续时间和频谱特征）。至关重要的是，与任务诱发激活类似，自发性激活系统地先于相位性瞳孔扩张出现，具有惊人相似的时间模式。我们的发现表明，人类岛叶中的自发性和任务诱发激活具有相似的神经生理特征，并支持这些激活与瞳孔扩张动力学测量的自主功能之间的明确联系。我们对人类大脑激活的大部分了解都来自于对外界事件和实验条件（即“任务诱发”激活）的反应研究。我们从植入人体的电极中获得了直接的神经记录，并表明激活是自发出现的，并且与同一神经元群体中的任务诱发激活具有很强的相似性（例如，幅度、时间谱）。在背侧前岛叶中，一个涉及突显处理和警觉的大脑区域，自发或任务诱发的激活与瞳孔的短暂扩张有关。我们的发现强调了自发性脑活动（当前人类神经影像学研究的重点，旨在开发疾病的生物标志物）如何与正在进行的生理和可能的自我产生的心理过程相关。
