Leathers Marvin L, Olson Carl R
Center for the Neural Basis of Cognition, Carnegie Mellon University, Pittsburgh, Pennsylvania; and
Department of Neuroscience, University of Pittsburgh, Pittsburgh, Pennsylvania.
J Neurophysiol. 2017 Apr 1;117(4):1499-1511. doi: 10.1152/jn.00564.2016. Epub 2017 Jan 11.
Neurons in the lateral intraparietal (LIP) area of macaque monkey parietal cortex respond to cues predicting rewards and penalties of variable size in a manner that depends on the motivational salience of the predicted outcome (strong for both large reward and large penalty) rather than on its value (positive for large reward and negative for large penalty). This finding suggests that LIP mediates the capture of attention by salient events and does not encode value in the service of value-based decision making. It leaves open the question whether neurons elsewhere in the brain encode value in the identical task. To resolve this issue, we recorded neuronal activity in the amygdala in the context of the task employed in the LIP study. We found that responses to reward-predicting cues were similar between areas, with the majority of reward-sensitive neurons responding more strongly to cues that predicted large reward than to those that predicted small reward. Responses to penalty-predicting cues were, however, markedly different. In the amygdala, unlike LIP, few neurons were sensitive to penalty size, few penalty-sensitive neurons favored large over small penalty, and the dependence of firing rate on penalty size was negatively correlated with its dependence on reward size. These results indicate that amygdala neurons encoded cue value under circumstances in which LIP neurons exhibited sensitivity to motivational salience. However, the representation of negative value, as reflected in sensitivity to penalty size, was weaker than the representation of positive value, as reflected in sensitivity to reward size. This is the first study to characterize amygdala neuronal responses to cues predicting rewards and penalties of variable size in monkeys making value-based choices. Manipulating reward and penalty size allowed distinguishing activity dependent on motivational salience from activity dependent on value. This approach revealed in a previous study that neurons of the lateral intraparietal (LIP) area encode motivational salience. Here, it reveals that amygdala neurons encode value. The results establish a sharp functional distinction between the two areas.
猕猴顶叶皮质外侧顶内（LIP）区域的神经元对预测大小可变的奖励和惩罚的线索作出反应，其方式取决于预测结果的动机显著性（对大奖励和大惩罚都强烈），而非其价值（大奖励为正，大惩罚为负）。这一发现表明，LIP介导了显著事件对注意力的吸引，并且在基于价值的决策中并不编码价值。这就留下了一个问题，即大脑其他部位的神经元在相同任务中是否编码价值。为了解决这个问题，我们在LIP研究中使用的任务背景下记录了杏仁核中的神经元活动。我们发现，两个区域对奖励预测线索的反应相似，大多数对奖励敏感的神经元对预测大奖励的线索反应比对预测小奖励的线索更强。然而，对惩罚预测线索的反应却明显不同。在杏仁核中，与LIP不同，很少有神经元对惩罚大小敏感，很少有对惩罚敏感的神经元更喜欢大惩罚而非小惩罚，并且放电率对惩罚大小的依赖性与其对奖励大小的依赖性呈负相关。这些结果表明，在LIP神经元对动机显著性表现出敏感性的情况下，杏仁核神经元编码线索价值。然而，对惩罚大小的敏感性所反映的负价值表征，比对奖励大小的敏感性所反映的正价值表征要弱。这是第一项描述猴子在进行基于价值的选择时，杏仁核神经元对预测大小可变的奖励和惩罚的线索的反应特征的研究。操纵奖励和惩罚大小能够区分依赖于动机显著性的活动和依赖于价值的活动。这种方法在之前的一项研究中揭示了外侧顶内（LIP）区域的神经元编码动机显著性。在此，它揭示了杏仁核神经元编码价值。结果在这两个区域之间建立了鲜明的功能区别。
