A role for primate subgenual cingulate cortex in sustaining autonomic arousal

A role for primate subgenual cingulate cortex in sustaining autonomic arousal
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DOI:
10.1073/pnas.1317695111
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发表时间:
2014-03
期刊:
Proceedings of the National Academy of Sciences
影响因子:
--
通讯作者:
P. Rudebeck;Philip T. Putnam;Teresa E. Daniels;Tianming Yang;A. Mitz;S. Rhodes;E. Murray
P. Rudebeck;Philip T. Putnam;Teresa E. Daniels;Tianming Yang;A. Mitz;S. Rhodes;E. Murray
中科院分区:
其他
文献类型:
--
作者:
P. Rudebeck;Philip T. Putnam;Teresa E. Daniels;Tianming Yang;A. Mitz;S. Rhodes;E. Murray

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重要性情绪调节障碍是情绪障碍的核心病因,如抑郁症。对神经结构如何调节情绪和唤醒的因果理解可能有助于改善这些精神疾病的治疗。对抑郁症患者的研究表明,额叶的一个特殊部分,即膝下扣带皮层,在情感处理中起着重要作用,尽管其确切的作用尚不清楚。在这里,我们表明,在猕猴中,额叶皮层的这一小部分是必要的,以维持预期积极情绪事件的高度觉醒。这一发现表明,这一区域对情感调节的贡献机制,包括对缺乏快乐和消极情绪的解释。膝下前扣带皮层(subgenual anterior cingulate cortex,ACC)在情绪调节中起重要作用,该区域的退化与抑郁情绪和快感缺乏有关。尽管有这样的理解,但我们仍然不知道前额叶皮层的这一部分是如何影响情绪的,尤其是积极情绪。在猕猴中使用巴甫洛夫条件反射程序,我们研究了膝下ACC与积极情绪事件相关的自主觉醒的贡献。在这样的条件反射之后,自主觉醒会对预测奖励的线索做出反应,猴子在奖励传递之前的一段时间内保持这种高度的觉醒状态。在这里,我们表明,虽然猴子与病变的膝下ACC显示初始的,线索诱发的觉醒,他们未能维持高水平的觉醒,直到预期的奖励交付。控制程序表明,这种损害并没有导致自主反应的差异奖励交付单独,无法学习之间的联系线索和奖励,或改变光反射。我们的数据表明,膝下前扣带可能有助于积极的影响,持续唤醒预期积极的情绪事件。未能保持积极的影响,预期愉快的事件可以提供洞察的病理生理学的心理障碍,其中负面情绪占主导地位的患者的情感体验。
Significance Dysregulation of emotion is central to the etiology of mood disorders, such as depression. A causal understanding of how neural structures regulate emotion and arousal could help to improve treatments for these psychiatric disorders. Studies of patients with depression indicate that a particular part of the frontal lobe, the subgenual cingulate cortex, plays an important role in affective processing, though its precise contribution remains unclear. Here we show that, in macaque monkeys, this small part of the frontal cortex is necessary for sustaining elevated arousal in anticipation of positive emotional events. This finding suggests a mechanism for the contribution of this area to affective regulation, including an account for the lack of pleasure and passivity that characterizes mood disorders. The subgenual anterior cingulate cortex (subgenual ACC) plays an important role in regulating emotion, and degeneration in this area correlates with depressed mood and anhedonia. Despite this understanding, it remains unknown how this part of the prefrontal cortex causally contributes to emotion, especially positive emotions. Using Pavlovian conditioning procedures in macaque monkeys, we examined the contribution of the subgenual ACC to autonomic arousal associated with positive emotional events. After such conditioning, autonomic arousal increases in response to cues that predict rewards, and monkeys maintain this heightened state of arousal during an interval before reward delivery. Here we show that although monkeys with lesions of the subgenual ACC show the initial, cue-evoked arousal, they fail to sustain a high level of arousal until the anticipated reward is delivered. Control procedures showed that this impairment did not result from differences in autonomic responses to reward delivery alone, an inability to learn the association between cues and rewards, or to alterations in the light reflex. Our data indicate that the subgenual ACC may contribute to positive affect by sustaining arousal in anticipation of positive emotional events. A failure to maintain positive affect for expected pleasurable events could provide insight into the pathophysiology of psychological disorders in which negative emotions dominate a patient’s affective experience.