Psychology and Aging © 2018 American Psychological Association 2018, Vol. 33, No. 1, 144–157 0882-7974/18/$12.00 http://dx.doi.org/10.1037/pag0000234 Age Differences in Episodic Associative Learning Rachel Clark and Eliot Hazeltine Michael Freedberg University of Iowa The Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, Maryland Michelle W. Voss University of Iowa Compared with young adults, older adults demonstrate difficulty forming and retrieving episodic memories. One proposed mechanism is that older adults are impaired at binding information into nonoverlapping representations, which is a key function of the hippocampus. The current experiments evaluate age differences in acquiring new memories using a novel episodic associative learning (EAL) task designed to tap hippocampal-dependent binding. The task involved repeated exposure of stimuli pairs and required the formation of new representations of each stimulus pair, as each pair was mapped to a unique keypress response. Notably, individual stimuli appeared in multiple pairs, so pair retrieval was necessary for correct response production. Experiment 1 demonstrated that older adults learned more slowly, and less overall, than young adults on this task. We also found that older adults benefited less than young adults from correct responses and as the number of intervening pairs between repetitions of a pair increased, older adults showed larger decrements in accuracy than young adults. Experiment 2 replicated these findings while minimizing motor demands and providing more practice. We also measured processing speed and spatial reconstruction to determine the involvement of specific cognitive mecha- nisms in observed age effects. We found that young adults with better spatial reconstruction abilities performed better on the EAL task than young adults with lower abilities and older adults overall. These findings suggest that older adults’ lower performance on the task may be partly explained by a decline in hippocampal-supported binding processes and a greater reliance on extrahippocampal learning systems. Keywords: cognitive aging, episodic memory, learning, associative binding, hippocampus The ability to learn new information is essential to daily life and One core feature of episodic memory is the associative binding thus a critical component of healthy aging. There is substantial of relations among elements of an episode (Davachi & Wagner, research documenting aging-related decline in forming and retriev- 2002; Konkel & Cohen, 2009). The associative deficit hypothesis ing episodic memories (Addis, Roberts, & Schacter, 2011; Craik, (ADH; Naveh-Benjamin, 2000) posits that episodic memory de- 1994; Levine, Svoboda, Hay, Winocur, & Moscovitch, 2002; clines with aging due to impaired binding processes. The ADH Light, 1991; McIntyre & Craik, 1987). However, the precise emerges from findings that older adults are worse than young cognitive mechanisms that make episodic memories especially adults at creating and retrieving links between elements of a scene vulnerable to aging are not as clear. or episode, even though their memory for individual elements is not impaired (Chalfonte & Johnson, 1996; Naveh-Benjamin, 2000). Following these findings, the ADH predicts that older adults will perform more poorly on tasks that require the formation This document is copyrighted by the American Psychological Association or one of its allied publishers. Rachel Clark, Interdisciplinary Graduate Program in Neuroscience, Uni- of associations between items within an episode or scene. Multiple This article is intended solely for the personal use ofversity the individual user and is not to be disseminatedof broadly. Iowa; Eliot Hazeltine, Interdisciplinary Graduate Program in studies have shown that older adults demonstrate an associative Neuroscience and Department of Psychological and Brain Sciences, Uni- deficit for different types of pairs, such as word-word pairs versity of Iowa; Michael Freedberg, The Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, Maryland; Michelle W. (Naveh-Benjamin, 2000; Provyn, Sliwinski, & Howard, 2007), Voss, Interdisciplinary Graduate Program in Neuroscience, Department of picture-picture pairs (Guez & Lev, 2016; Naveh-Benjamin, Hus- Psychological and Brain Sciences, and Aging Mind and Brain Initiative sain, Guez, & Bar-On, 2003), and face-name pairs (Naveh- (AMBI), University of Iowa. Benjamin, Guez, Kilb, & Reedy, 2004; for a review, see Old & This research was funded by start-up funds provided to Michelle W. Naveh-Benjamin, 2008). Voss by the University of Iowa. We thank Joan Severson at Digital However, associative binding is not always impaired with aging Artefacts in Iowa City, IA for creation and use of the spatial reconstruction (Dennis, Howard, & Howard, 2006; Howard, Howard, Dennis, paradigm. Correspondence concerning this article should be addressed to Michelle Yankovich, & Vaidya, 2004), suggesting that we need a better W. Voss, Department of Psychological and Brain Sciences, University of understanding of the specific processes involved in binding that Iowa, 300 Iowa Avenue, Iowa City, IA 52245. E-mail: michelle-voss@ decline with aging. For instance, we also previously found that uiowa.edu older adults performed similarly to young adults at a configural 144 AGE DIFFERENCES IN EPISODIC ASSOCIATIVE LEARNING 145 learning task (Clark, Freedberg, Hazeltine, & Voss, 2015). In this Motivated by this prediction, we have created a novel Episodic task, each item was associated with a unique single keypress Associative Learning (EAL) task that capitalizes on characteristics response and the items were presented in pairs so that two-finger that place heavy demands on the relational and associative binding responses were required. Importantly, individual items could re- processes of the hippocampus. This EAL task requires that partic- peat across pairs, but certain pairs occurred more frequently than ipants intentionally learn, through a process of trial and error, others. Configural learning was assessed by comparing response configural keypress responses to specific stimulus pairs (i.e., pic- times (RTs) of frequently occurring pairs with RTs to infrequent tures of faces and buildings). This task follows our configural pairs. Relatively shorter RTs to the frequent pairs expresses mem- learning task (Clark et al., 2015) in that it tests the ability to make ory for distinct combinations of pairs, despite the overlapping distinct representations of pairs that have overlapping elements. items between pairs (Hazeltine, Aparicio, Weinstein, & Ivry, Moreover, it uses the same stimuli pairs and configural responses. 2007). Older adults demonstrated relatively shorter RTs to fre- However, to target relational and associative binding that should quently occurring pairs to the same extent as young adults, which rely on the hippocampus, rather than having a single key consis- indicates that older adults were as able as young adults to bind the tently associated with each individual stimulus, this task requires a distinct response components (Clark et al., 2015). These data distinct response associated with each item pair. As shown in suggest that some forms of associative binding are not affected by Figure 1A, each picture appears within three separate pairs. To aging. In turn, we view the configural learning task as an oppor- perform accurately, a representation of each unique pair must be tunity to examine specific components of the binding process that distinct from the representations of each element individually lead to impairment with aging. (Moses & Ryan, 2006). This places heavy demands on binding Clues as to why some forms of binding show impairment processes that differentiate among pairs sharing individual ele- whereas others appear preserved can be gleaned from cognitive ments. Further, because each item pair is associated with a unique neuroscience. Relational memory theory proposes that the hip- nonoverlapping response, the stimuli must be bound together be- pocampus rapidly encodes flexible relationships between elements fore the response can be produced. This places much greater in an episode (Konkel & Cohen, 2009), such that individual demands on binding processes than the previous task in which elements of an experience are linked in a flexible manner so that each individual stimulus was consistently mapped to a keypress. they can be recalled with respect to their relationship and over- Additionally, because the hippocampus has been implicated in lapping elements can be recombined during retrieval (for a review, rapid binding compared with slower learning that is more depen- see Eichenbaum, 2000). Because the hippocampus and hippocampal- dent on the caudate (Poldrack et al., 2001; Poldrack & Rodriguez, cortical systems implicated in relational memory typically experi- 2004), examining rate of learning adds a rich dimension of time ence decline with aging (Driscoll et al., 2009; Jack et al., 1998; that enables firmer links to cognitive processes that depend on the Kennedy et al., 2009; Raz et al., 2005; Raz, Rodrigue, Head, hippocampus. More specifically, early in learning the hippocam- Kennedy, & Acker, 2004), the relational memory theory provides pus is thought to be engaged to rapidly acquire new associations an avenue to further specify the associative binding processes that between stimuli (Poldrack & Packard, 2003; Simon, Vaidya, How- would be predicted to deteriorate with aging.