Cho Youngsun T, Fromm Stephen, Guyer Amanda E, Detloff Allison, Pine Daniel S, Fudge Julie L, Ernst Monique
Department of Neurobiology and Anatomy, University of Rochester Medical Center, NY, USA.
Section on Development and Affective Neuroscience Branch, National Institute of Mental Health, NIH, DHHS, MD, USA.
Neuroimage. 2013 Feb 1;66:508-21. doi: 10.1016/j.neuroimage.2012.10.013. Epub 2012 Oct 13.
Reward neurocircuitry links motivation with complex behavioral responses. Studies of incentive processing have repeatedly demonstrated activation of nucleus accumbens (NAc), thalamus, and anterior insula, three key components of reward neurocircuitry. The contribution of the thalamus to this circuitry in humans has been relatively ignored, a gap that needs to be filled, given the central role of this structure in processing and filtering information. This study aimed to understand how these three regions function as a network during gain or loss anticipation in adults and youth. Towards this goal, functional magnetic resonance imaging (fMRI) and dynamic causal modeling (DCM) were used to examine effective connectivity among these three nodes in healthy adults and adolescents who performed the monetary incentive delay (MID) task. Seven connectivity models, based on anatomic connections, were tested. They were estimated for incentive anticipation and underwent Bayesian Model Selection (BMS) to determine the best-fit model for each adult and adolescent group. Connection strengths were extracted from the best-fit model and examined for significance in each group. These variables were then entered into a linear mixed model to test between-group effects on effective connectivity in reward neurocircuitry. The best-fit model for both groups included all possible anatomic connections. Three main findings emerged: (1) Across the task, thalamus and insula significantly influenced NAc; (2) A broader set of significant connections was found for the loss-cue condition than the gain-cue condition in both groups; (3) Finally, between-group comparisons of connectivity strength failed to detect statistical differences, suggesting that adults and adolescents use this incentive-processing network in a similar manner. This study demonstrates the way in which the thalamus and insula influence the NAc during incentive processing in humans. Specifically, this is the first study to demonstrate in humans the key role of thalamus projections onto the NAc in support of reward processing. Our results suggest that anticipation of gain/loss involves an 'alerting' signal (thalamus) that converges with interoceptive information (insula) to shape action selection programs in the ventral striatum.
奖赏神经回路将动机与复杂的行为反应联系起来。对奖励处理的研究反复证明伏隔核（NAc）、丘脑和前脑岛会被激活，这三者是奖赏神经回路的关键组成部分。丘脑对人类这一神经回路的作用相对被忽视了，鉴于该结构在信息处理和过滤中的核心作用，这一空白需要填补。本研究旨在了解在成年人和青少年预期收益或损失期间，这三个区域如何作为一个网络发挥作用。为实现这一目标，功能磁共振成像（fMRI）和动态因果模型（DCM）被用于检查执行金钱激励延迟（MID）任务的健康成年人和青少年中这三个节点之间的有效连接。基于解剖连接测试了七个连接模型。对激励预期进行了模型估计，并进行贝叶斯模型选择（BMS）以确定每个成年人和青少年组的最佳拟合模型。从最佳拟合模型中提取连接强度，并检查每组中的显著性。然后将这些变量输入线性混合模型，以测试奖赏神经回路中组间对有效连接的影响。两组的最佳拟合模型都包括所有可能的解剖连接。出现了三个主要发现：（1）在整个任务过程中，丘脑和脑岛对伏隔核有显著影响；（2）两组中，与收益提示条件相比，损失提示条件下发现了更广泛的显著连接；（3）最后，连接强度的组间比较未发现统计学差异，这表明成年人和青少年以类似方式使用这一奖励处理网络。这项研究证明了在人类奖励处理过程中丘脑和脑岛对伏隔核的影响方式。具体而言，这是第一项在人类中证明丘脑投射到伏隔核在支持奖励处理中的关键作用的研究。我们的结果表明，对收益/损失的预期涉及一个“警报”信号（丘脑），它与内感受信息（脑岛）汇聚，以塑造腹侧纹状体中的行动选择程序。
