Center for Lifespan Psychology, Max Planck Institute for Human Development, Berlin, 14195, Germany.
Institute of Cognitive Neuroscience, Ruhr-Universität Bochum, Bochum, 44780, Germany.
J Neurosci. 2021 Apr 14;41(15):3499-3511. doi: 10.1523/JNEUROSCI.2038-20.2021. Epub 2021 Feb 26.
The distinctiveness of neural information representation is crucial for successful memory performance but declines with advancing age. Computational models implicate age-related neural dedifferentiation on the level of item representations, but previous studies mostly focused on age differences of categorical information representation in higher-order visual regions. In an age-comparative fMRI study, we combined univariate analyses and whole-brain searchlight pattern similarity analyses to elucidate age differences in neural distinctiveness at both category and item levels and their relation to memory. Thirty-five younger (18-27 years old) and 32 older (67-75 years old) women and men incidentally encoded images of faces and houses, followed by an old/new recognition memory task. During encoding, age-related neural dedifferentiation was shown as reduced category-selective processing in ventral visual cortex and impoverished item specificity in occipital regions. Importantly, successful subsequent memory performance built on high item stability, that is, high representational similarity between initial and repeated presentation of an item, which was greater in younger than older adults. Overall, we found that differences in representational distinctiveness coexist across representational levels and contribute to interindividual and intraindividual variability in memory success, with item specificity being the strongest contributor. Our results close an important gap in the literature, showing that older adults' neural representation of item-specific information in addition to categorical information is reduced compared with younger adults. A long-standing hypothesis links age-related cognitive decline to a loss of neural specificity. While previous evidence supports the notion of age-related neural dedifferentiation of category-level information in ventral visual cortex, whether or not age differences exist at the item level was a matter of debate. Here, we observed age group differences at both levels as well as associations between both categorical distinctiveness and item specificity to memory performance, with item specificity being the strongest contributor. Importantly, age differences in occipital item specificity were largely due to reduced item stability across repetitions in older adults. Our results suggest that age differences in neural representations can be observed across the entire cortical hierarchy and are not limited to category-level information.
神经信息表示的独特性对成功的记忆表现至关重要，但随着年龄的增长而下降。计算模型暗示了与年龄相关的神经去分化在项目表示水平上，但以前的研究主要集中在高级视觉区域的分类信息表示的年龄差异上。在一项年龄比较 fMRI 研究中，我们结合了单变量分析和全脑搜索光模式相似性分析，以阐明类别和项目水平的神经独特性的年龄差异及其与记忆的关系。35 名年轻（18-27 岁）和 32 名年老（67-75 岁）的女性和男性偶然地对人脸和房屋的图像进行了编码，然后进行了旧/新识别记忆任务。在编码过程中，年龄相关的神经去分化表现为腹侧视觉皮层的类别选择性处理减少和枕叶区域的项目特异性减少。重要的是，随后的记忆表现是基于项目的高稳定性建立的，即项目在初始和重复呈现之间的表示相似性高，在年轻成年人中比在年老成年人中更高。总的来说，我们发现，在表示水平上存在的表示独特性差异共同存在，并对记忆成功的个体间和个体内变异性做出贡献，其中项目特异性是最强的贡献者。我们的结果填补了文献中的一个重要空白，表明与年轻成年人相比，年老成年人对项目特异性信息的神经表示除了类别信息之外也减少了。一个长期存在的假设将与年龄相关的认知衰退与神经特异性的丧失联系起来。虽然以前的证据支持了腹侧视觉皮层中与年龄相关的类别水平信息去分化的概念，但在项目水平上是否存在年龄差异一直是一个争论的问题。在这里，我们在两个水平上观察到了年龄组差异，以及类别特异性和项目特异性与记忆表现之间的关联，其中项目特异性是最强的贡献者。重要的是，年老成年人枕叶项目特异性的差异主要是由于在重复过程中项目稳定性降低所致。我们的结果表明，神经表示的年龄差异可以在整个皮质层次结构中观察到，并且不限于类别水平的信息。
