University of Geneva.
Campus Biotech, Geneva, Switzerland.
J Cogn Neurosci. 2021 Mar;33(3):402-421. doi: 10.1162/jocn_a_01660. Epub 2020 Dec 16.
Offering reward during encoding typically leads to better memory [Adcock, R. A., Thangavel, A., Whitfield-Gabrieli, S.,Knutson, B., & Gabrieli, J. D. E. Reward-motivated learning: Mesolimbic activation precedes memory formation. , , 507-517, 2006]. Whether such memory benefit persists when tested in a different task context remains, however, largely understudied [Wimmer, G. E., & Buechel, C. Reactivation of reward-related patterns from single past episodes supports memory-based decision making. , , 2868-2880, 2016]. Here, we ask whether reward at encoding leads to a generalized advantage across learning episodes, a question of high importance for any everyday life applications, from education to patient rehabilitation. Although we confirmed that offering monetary reward increased responses in the ventral striatum and pleasantness judgments for pictures used as stimuli, this immediate beneficial effect of reward did not carry over to a subsequent and different picture-location association memory task during which no reward was delivered. If anything, a trend for impaired memory accuracy was observed for the initially high-rewarded pictures as compared to low-rewarded ones. In line with this trend in behavioral performance, fMRI activity in reward (i.e., ventral striatum) and in memory (i.e., hippocampus) circuits was reduced during the encoding of new associations using previously highly rewarded pictures (compared to low-reward pictures). These neural effects extended to new pictures from same, previously highly rewarded semantic category. Twenty-four hours later, delayed recall of associations involving originally highly rewarded items was accompanied by decreased functional connectivity between the hippocampus and two brain regions implicated in value-based learning, the ventral striatum and the ventromedial PFC. We conclude that acquired reward value elicits a downward value-adjustment signal in the human reward circuit when reactivated in a novel nonrewarded context, with a parallel disengagement of memory-reward (hippocampal-striatal) networks, likely to undermine new associative learning. Although reward is known to promote learning, here we show how it may subsequently hinder hippocampal and striatal responses during new associative memory formation.
在编码过程中提供奖励通常会导致更好的记忆[Adcock，RA，Thangavel，A.，Whitfield-Gabrieli，S.，Knutson，B.，& Gabrieli，JD。奖励驱动的学习：中脑边缘系统的激活先于记忆形成。 ， ，507-517，2006]。然而，当在不同的任务环境中进行测试时，这种记忆益处是否仍然存在，在很大程度上仍未得到充分研究[Wimmer，GE，& Buechel，C.。从单个过去事件中重新激活与奖励相关的模式可支持基于记忆的决策。 ， ，2868-2880，2016]。在这里，我们想知道在编码时提供奖励是否会导致学习过程中的普遍优势，这对于从教育到患者康复的任何日常生活应用都非常重要。尽管我们确认提供金钱奖励会增加腹侧纹状体的反应和对用作刺激的图片的愉悦度判断，但奖励的这种直接有益效果并未延续到随后的不同图片-位置关联记忆任务中，在此任务中没有提供奖励。如果有的话，与低奖励图片相比，最初高奖励图片的记忆准确性趋势受到损害。与行为表现的这种趋势一致，使用先前高度奖励的图片进行新关联的编码过程中，奖励（即腹侧纹状体）和记忆（即海马体）回路的 fMRI 活动减少（与低奖励图片相比）。这些神经效应扩展到来自同一先前高度奖励语义类别的新图片。24 小时后，与最初高度奖励的项目相关联的关联的延迟回忆伴随着海马体与两个涉及基于价值的学习的大脑区域（腹侧纹状体和腹内侧前额叶皮质）之间的功能连接减少。我们得出的结论是，在新的非奖励环境中重新激活获得的奖励值会在人类奖励回路中引起向下的价值调整信号，同时记忆-奖励（海马-纹状体）网络平行脱离，可能破坏新的联想学习。尽管奖励已知可促进学习，但在这里我们展示了它如何随后在新的联想记忆形成过程中阻碍海马体和纹状体的反应。
