Hall Julie M, Shahnazian Danesh, Krebs Ruth M
Department of Experimental Psychology, Ghent University, Ghent, Belgium.
Department of Health, Medical and Neuropsychology, Leiden University, Leiden, the Netherlands.
Imaging Neurosci (Camb). 2024 Oct 28;2. doi: 10.1162/imag_a_00336. eCollection 2024.
Dopaminergic neurons in the substantia nigra and the ventral tegmental area (SN/VTA) are classically viewed as key mediators in reward processing, while noradrenergic cells in the locus coeruleus (LC) are thought to modulate (negative) saliency processing. However, this conventional distinction is being revised by more recent research in animals. To explore the respective contributions of both the LC and SN/VTA in reward and valence processing in humans, we assessed fMRI data during stimulus encoding and response phase of a rewarded emotion-discrimination task (n = 38). Participants responded significantly faster to reward predicting and negative valence stimuli compared with their non-salient counterparts. LC activity was overall higher during trials involving reward prospect, and in particular for reward trials featuring positive valence, demonstrating an additive effect of reward and positive valence in LC. Moreover, LC activity was differentially increased for negative compared with positive valence in the response phase, indexing its role in invigorating responses to negative events. The SN/VTA showed increased activity in the response phase of reward trials (neutral valence) and negative valence trials (no reward), which aligns with coding relative saliency of these events in their respective contexts. LC modulations were accompanied by covariations in occipital cortex, suggesting noradrenergic contributions to visual prioritization of salient events. The findings underscore the sensitivity of both LC and SN/VTA to reward prospects and negative valence, challenging the dominant view of SN/VTA's involvement in merely positive events and emphasizing their essential role in action invigoration above and beyond mere stimulus encoding. The intricate roles of the DA and NA system in reward and emotional valence processing in humans warrant further exploration and validation, given the limitations inherent to neuroimaging of deep brain structures.
黑质和腹侧被盖区(SN/VTA)中的多巴胺能神经元传统上被视为奖励处理的关键介质,而蓝斑(LC)中的去甲肾上腺素能细胞则被认为可调节(负性)显著性处理。然而,动物方面的最新研究正在修正这种传统的区分。为了探究LC和SN/VTA在人类奖励和效价处理中的各自贡献,我们评估了一项奖励性情绪辨别任务(n = 38)的刺激编码和反应阶段的功能磁共振成像(fMRI)数据。与非显著性刺激相比,参与者对奖励预测和负性效价刺激的反应明显更快。在涉及奖励预期的试验中,LC的活动总体上更高;特别是对于具有正性效价的奖励试验,这表明奖励和正性效价在LC中具有累加效应。此外,在反应阶段,与正性效价相比,LC对负性效价的活动差异增加,表明其在增强对负性事件的反应中的作用。SN/VTA在奖励试验(中性效价)和负性效价试验(无奖励)的反应阶段显示出活动增加,这与在各自情境中对这些事件的相对显著性编码一致。LC的调节伴随着枕叶皮质的协变,表明去甲肾上腺素能对显著性事件的视觉优先化有贡献。这些发现强调了LC和SN/VTA对奖励预期和负性效价的敏感性,挑战了SN/VTA仅参与积极事件的主流观点,并强调了它们在单纯刺激编码之外的行动激活中的重要作用。鉴于深部脑结构神经成像固有的局限性,多巴胺(DA)和去甲肾上腺素(NA)系统在人类奖励和情绪效价处理中的复杂作用值得进一步探索和验证。