Department of Psychiatry and Psychotherapy, Focus Program Translational Neuroscience (FTN), University Medical Center of the Johannes Gutenberg University Mainz, 55131 Mainz, Germany
Department of Psychiatry and Psychotherapy, Focus Program Translational Neuroscience (FTN), University Medical Center of the Johannes Gutenberg University Mainz, 55131 Mainz, Germany.
J Neurosci. 2021 Mar 17;41(11):2447-2456. doi: 10.1523/JNEUROSCI.1681-20.2020. Epub 2020 Dec 29.
Unexpected and thus surprising events are omnipresent and oftentimes require adaptive behavior such as unexpected inhibition or unexpected action. The current theory of unexpected events suggests that such unexpected events just like global stopping recruit a fronto-basal-ganglia network. A global suppressive effect impacting ongoing motor responses and cognition is specifically attributed to the subthalamic nucleus (STN). Previous studies either used separate tasks or presented unexpected, task-unrelated stimuli during response inhibition tasks to relate the neural signature of unexpected events to that of stopping. Here, we aimed to test these predictions using a within task design with identical stimulus material for both unexpected action and unexpected inhibition using functional magnetic resonance imaging (fMRI) for the first time. To this end, 32 healthy human participants of both sexes performed a cue-informed go/nogo task comprising expected and unexpected action and inhibition trials during fMRI. Using conjunction, contrast, and Bayesian analyses, we demonstrate that unexpected action elicited by an unexpected go signal and unexpected inhibition elicited by an unexpected nogo signal recruited the same fronto-basal-ganglia network which is usually assigned to stopping. Furthermore, the stronger the unexpected action-related activity in the STN region was the more detrimental was the effect on response times. The present results thus complement earlier findings and provide direct evidence for the unified theory of unexpected events while ruling out alternative task and novelty effects. This is the first study using functional magnetic resonance imaging (fMRI) to test whether unexpected events regardless of whether they require unexpected action or inhibition recruit a fronto-basal-ganglia network just like stopping. In contrast to previous studies, we used identical stimulus material for both conditions within one task. This enabled us to directly test predictions of the current theory of unexpected events and, moreover, to test for condition-specific neural signatures. The present results underpin that both processes recruit the same neural network while excluding alternative task and novelty effects. The simple task design thus provides an avenue to studying surprise as a pure form of reactive inhibition in neuropsychiatric patients displaying inhibitory deficits who often have a limited testing capacity.
意外事件是普遍存在的，而且往往需要适应行为，例如意外抑制或意外行动。当前关于意外事件的理论表明，这种意外事件就像全局停止一样，会招募一个额-基底-纹状体网络。一个影响正在进行的运动反应和认知的全局抑制效应，特别是归因于丘脑底核（STN）。以前的研究要么使用单独的任务，要么在反应抑制任务中呈现意外的、与任务无关的刺激，以将意外事件的神经特征与停止的神经特征联系起来。在这里，我们旨在使用相同的刺激材料，首次在功能磁共振成像（fMRI）中，通过一个任务内设计，来测试这些预测。为此，32 名健康的男性和女性参与者在 fMRI 中完成了一个线索告知的 Go/NoGo 任务，其中包括预期和意外的行动和抑制试验。使用结合、对比和贝叶斯分析，我们证明了由意外 Go 信号引起的意外行动和由意外 NoGo 信号引起的意外抑制，招募了相同的额-基底-纹状体网络，该网络通常被分配给停止。此外，STN 区域的意外行动相关活动越强，对反应时间的影响就越不利。因此，本研究结果补充了早期的发现，并为意外事件的统一理论提供了直接证据，同时排除了替代任务和新颖性效应。这是第一项使用功能磁共振成像（fMRI）来测试意外事件是否无论它们是否需要意外行动或抑制，都招募额-基底-纹状体网络，就像停止一样。与以前的研究不同，我们在一个任务中使用相同的刺激材料来测试两种条件。这使我们能够直接测试当前意外事件理论的预测，而且，还可以测试条件特异性的神经特征。本研究结果支持了这两种过程都招募相同的神经网络，同时排除了替代任务和新颖性效应。简单的任务设计因此为研究惊讶提供了一种途径，惊讶是一种纯反应抑制形式，在表现出抑制缺陷的神经精神患者中经常表现出抑制缺陷，而这些患者的测试能力往往有限。
