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Integration of valence and conflict processing through cellular-field interactions in human subgenual cingulate during emotional face processing in treatment-resistant depression
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

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孔处理过程中,通过人类膝下扣带回的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感过程的关键大脑区域。虽然 sgACC 涉及情绪评估和情绪冲突监控,但目前尚不清楚该领域如何整合多种功能。我们对 14 名接受 sgACC 深部脑刺激治疗难治性抑郁症的患者的单神经元和局部场振荡活动进行了表征。在记录过程中,向患者呈现了一项修改后的斯特鲁普任务,其中包含情感面部图像,其效价和一致性各不相同。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效价和一致性都有反应,这表明 sgACC 神经元活动可以在同一任务中编码多个过程,表明其多功能性。在峰值神经元响应期间,我们观察到低频振荡的频谱功率增加,包括 θ 频段同步(4-8Hz)以及 β 频段频率(13-30Hz)的去同步。 Theta 活动受到当前试验一致性的调节,在非一致性刺激后光谱功率会有更大的增加,而 Beta 去同步化的发生与情绪效价无关。尖峰场相互作用表明,局部 sgACC 尖峰对 β 带的锁相最为显着,而对 θ 带的锁相发生在总体上较少的神经元中,但对任务响应的神经元的调节更强烈。我们的研究结果首次提供了与人类 sgACC 情绪认知处理相关的尖峰场相互作用的直接证据。 此外,我们将人类 sgACC 中的 theta 振荡动力学与当前的试验一致性直接相关,证明它是冲突检测期间的重要调节器。我们的数据支持 sgACC 作为通过调节 beta 和 theta 网络活动进行认知情感处理的综合中心。

更新日期:2024-07-20
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