The subthalamic nucleus (STN) of the basal ganglia is key to the inhibitory control of movement. Consequently, it is a primary target for the neurosurgical treatment of movement disorders like Parkinson’s Disease, where modulating the STN via deep-brain stimulation (DBS) can release excess inhibition of thalamo-cortical motor circuits. However, the STN is also anatomically connected to other thalamo-cortical circuits, including those underlying cognitive processes like attention. Notably, STN-DBS can also affect these processes. This suggests that the STN may also contribute to the inhibition of non-motor activity, and that STN-DBS may cause changes to this inhibition. We here tested this hypothesis in humans. We used a novel, wireless outpatient method to record intracranial local field potentials (LFP) from STN DBS implants during a visual attention task (Experiment 1, N=12). These outpatient measurements allowed the simultaneous recording of high-density EEG, which we used to derive the steady-state visual evoked potential (SSVEP), a well-established neural index of visual attentional engagement. By relating STN activity to this neural marker of attention (instead of overt behavior), we avoided possible confounds resulting from STN’s motor role. We aimed to test whether the STN contributes to the momentary inhibition of the SSVEP caused by unexpected, distracting sounds. Furthermore, we causally tested this association in a second experiment, where we modulated STN via DBS across two sessions of the task, spaced at least one week apart (N=21, no sample overlap with Experiment 1). The LFP recordings in Experiment 1 showed that reductions of the SSVEP after distracting sounds were preceded by sound-related γ-frequency (>60Hz) activity in the STN. Trial-to-trial modeling further showed that this STN activity statistically mediated the sounds’ suppressive effect on the SSVEP. In Experiment 2, modulating STN activity via DBS significantly reduced these sound-related SSVEP reductions. This provides causal evidence for the role of the STN in the surprise-related inhibition of attention. These findings suggest that the human STN contributes to the inhibition of attention, a non-motor process. This supports a domain-general view of the inhibitory role of the STN. Furthermore, these findings also suggest a potential mechanism underlying some of the known cognitive side-effects of STN-DBS treatment, especially on attentional processes. Finally, our newly-established outpatient LFP recording technique facilitates the testing of the role of subcortical nuclei in complex cognitive tasks, alongside recordings from the rest of the brain, and in much shorter time than perisurgical recordings.

中文翻译：

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人类底丘脑核暂时抑制主动注意力过程

基底节的丘脑底核（STN）是运动抑制控制的关键。因此，它是神经外科治疗帕金森病等运动障碍的主要目标，通过深部脑刺激 (DBS) 调节 STN 可以释放丘脑皮质运动回路的过度抑制。然而，STN 在解剖学上也与其他丘脑皮质回路相连，包括那些潜在的认知过程，如注意力。值得注意的是，STN-DBS 也会影响这些过程。这表明 STN 也可能有助于抑制非运动活动，并且 STN-DBS 可能会导致这种抑制的改变。我们在这里在人类身上测试了这个假设。我们使用一种新颖的无线门诊方法在视觉注意任务期间记录 STN DBS 植入物的颅内局部场电位 (LFP)（实验 1，N=12）。这些门诊测量可以同时记录高密度脑电图，我们用它来推导稳态视觉诱发电位（SSVEP），这是一种完善的视觉注意力参与神经指数。通过将 STN 活动与这种注意力的神经标记（而不是明显的行为）联系起来，我们避免了 STN 的运动作用可能导致的混淆。我们的目的是测试 STN 是否有助于由意外的、分散注意力的声音引起的 SSVEP 的瞬时抑制。此外，我们在第二个实验中因果测试了这种关联，其中我们在两次任务中通过 DBS 调节 STN，间隔至少一周（N=21，与实验 1 没有样本重叠）。实验1中的LFP记录表明，在分散注意力的声音之后SSVEP的减少先于STN中与声音相关的γ频率(＞60Hz)活动。试验模型进一步表明，这种 STN 活性在统计上介导了声音对 SSVEP 的抑制作用。在实验 2 中，通过 DBS 调节 STN 活性显着减少了这些与声音相关的 SSVEP 降低。这为 STN 在意外相关的注意力抑制中的作用提供了因果证据。这些发现表明，人类 STN 有助于抑制注意力（一种非运动过程）。这支持了 STN 抑制作用的领域一般观点。此外，这些发现还表明 STN-DBS 治疗的一些已知认知副作用的潜在机制，特别是在注意力过程方面。最后，我们新建立的门诊 LFP 记录技术有助于测试皮质下核团在复杂认知任务中的作用，以及来自大脑其他部分的记录，并且比术前记录的时间短得多。