Molecular Psychiatry ( IF 9.6 ) Pub Date : 2024-07-20 , DOI: 10.1038/s41380-024-02667-6 Nicole A. Zalasky , Feng Luo , Linda H. Kim , M. Sohail Noor , Elliot C. Brown , Ana P. Arantes , Rajamannar Ramasubbu , Aaron J. Gruber , Zelma H. T. Kiss , Darren L. Clark
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The subgenual anterior cingulate cortex (sgACC) has been identified as a key brain area involved in various cognitive and emotional processes. While the sgACC has been implicated in both emotional valuation and emotional conflict monitoring, it is still unclear how this area integrates multiple functions. We characterized both single neuron and local field oscillatory activity in 14 patients undergoing sgACC deep brain stimulation for treatment-resistant depression. During recording, patients were presented with a modified Stroop task containing emotional face images that varied in valence and congruence. We further analyzed spike-field interactions to understand how network dynamics influence single neuron activity in this area. Most single neurons responded to both valence and congruence, revealing that sgACC neuronal activity can encode multiple processes within the same task, indicative of multifunctionality. During peak neuronal response, we observed increased spectral power in low frequency oscillations, including theta-band synchronization (4–8 Hz), as well as desynchronization in beta-band frequencies (13–30 Hz). Theta activity was modulated by current trial congruency with greater increases in spectral power following non-congruent stimuli, while beta desynchronizations occurred regardless of emotional valence. Spike-field interactions revealed that local sgACC spiking was phase-locked most prominently to the beta band, whereas phase-locking to the theta band occurred in fewer neurons overall but was modulated more strongly for neurons that were responsive to task. Our findings provide the first direct evidence of spike-field interactions relating to emotional cognitive processing in the human sgACC. Furthermore, we directly related theta oscillatory dynamics in human sgACC to current trial congruency, demonstrating it as an important regulator during conflict detection. Our data endorse the sgACC as an integrative hub for cognitive emotional processing through modulation of beta and theta network activity.
中文翻译:

在难治性抑郁症的情绪面处理过程中,通过人类膝下扣带回细胞场相互作用整合效价和冲突处理
膝下前扣带皮层 (sgACC) 已被确定为参与各种认知和情绪过程的关键大脑区域。虽然 sgACC 与情绪评估和情绪冲突监测有关,但目前尚不清楚该领域如何整合多种功能。我们表征了 14 例接受 sgACC 脑深部刺激治疗难治性抑郁症患者的单神经元和局部场振荡活动。在记录过程中,向患者展示了一个修改后的 Stroop 任务,其中包含在效价和一致性方面变化的情绪化面部图像。我们进一步分析了尖峰场相互作用,以了解网络动力学如何影响该区域的单个神经元活动。大多数单个神经元对价和一致性都有反应,揭示了 sgACC 神经元活动可以编码同一任务中的多个过程,表明多功能性。在神经元峰值响应期间,我们观察到低频振荡中的频谱功率增加,包括 θ 波段同步 (4-8 Hz),以及 β 波段频率 (13-30 Hz) 的不同步。θ 活性受当前试验一致性的调节,在不一致的刺激后频谱功率增加更大,而 β 不同步发生,与情绪效价无关。刺突场相互作用表明,局部 sgACC 刺突对 β 波段的锁相最突出,而对 θ 波段的锁相发生在总体较少的神经元中,但对于对任务有反应的神经元,这种调控更强烈。我们的研究结果提供了与人类 sgACC 中的情绪认知处理相关的尖峰场相互作用的第一个直接证据。 此外,我们将人类 sgACC 中的 θ 振荡动力学与当前的试验一致性直接联系起来,证明它是冲突检测过程中的重要调节因子。我们的数据支持 sgACC 通过调节 beta 和 theta 网络活动作为认知情绪处理的综合枢纽。