Memory Efficiency & Alzheimer’s Disease 1 Running Head: Value-Directed Remembering in Alzheimer’s Disease Aging, Memory Efficiency and the Strategic Control of Attention at Encoding: Selective Impairments of Value-Directed Remembering in Alzheimer’s Disease

Selecting what is important to remember, attending to this information, and then later recalling it can be thought of in terms of the strategic control of attention and encoding, and can lead to the efficient use of memory. The present study used a selectivity task, where items were paired with varying point values, to examine how the ability to selectively and strategically remember information of differing value is influenced by aging and Alzheimer’s disease. Younger adults and healthy older adults were able to strategically and efficiently encode and remember high value items, but AD led to a specific impairment in selectivity. Although individuals with AD recalled high value items, they also recalled lower value items, and did not efficiently maximize memory performance (as measured by a selectivity index), relative to healthy older adults. Complex working memory span measures were especially predictive of the recall of the high value items. This pattern suggests that AD leads to deficits in attentional control, which can lead to impairments in value-directed remembering. Memory Efficiency & Alzheimer’s Disease 3 The ability to attend to important information is critical in order to later recall this information. Selecting what is important to remember, attending to this information, and then recalling it can be thought of in terms of the strategic control of attention, and can lead to the efficient use of memory (Castel, 2007). Although Alzheimer’s disease (AD) is most often characterized in terms of loss of memory function, there is accumulating evidence that suggests that part of the initial impairment lies in attentional control (see Balota & Faust, 2001, and Perry & Hodges, 1999, for reviews). Impairments in attentional control can lead to impairments in encoding and maintaining relevant information in working memory (Hasher & Zacks, 1988), inhibitory control (Amieva, Phillips, Della Sella, & Henry, 2004), as well as retrieval and response control (Castel, Balota, Hutchison, Yap, & Logan, 2007). The present study examines how the ability to selectively attend to information that differs in value is influenced by aging and Alzheimer’s disease. This approach not only allows one to examine attentional control and memory capacity, but also the efficient use memory in the context of paying attention to, and encoding, high value information. There is considerable evidence that healthy older adults show various degrees of impairment on a wide range of cognitive tasks (Balota, Dolan, & Duchek, 2000). Specifically, tasks that involve executive processes, working memory, and frontal lobe function are thought to be especially impaired, leading to other attentional and memory deficits (West, 1996). This has lead to various theories that attempt to describe and account for the changes in cognitive function in old age, centering on reductions in available processing resources (Craik, 1982, 2002), general slowing of processing (Myerson, Hale, Wagstaff, Poon, & Smith, 1990; Salthouse, 1996), declines in working Memory Efficiency & Alzheimer’s Disease 4 memory capacity (McCabe, Smith, & Parks, 2007; Park et al., 1996) and reductions in inhibitory control (Hasher & Zacks, 1988; Rabbitt, 1965). The notion that there are breakdowns in the ability to control partially activated, but incorrect, information has also been quite useful in terms of accounting for some of the cognitive deficits that are associated with AD (e.g. Balota & Ferraro, 1993, 1996; Spieler, Balota, & Faust, 1996; Perry & Hodges, 1999). Although Alzheimer’s disease is often characterized by impairments in memory performance, tests that examine the impairments in the control of attention, and the development of behavioral measures that can detect early changes and declines in these areas, may also serve as useful measures for the early diagnosis and treatment of AD. The role of attention in memory performance has been a central theme in many lines of research, with the main finding being that distraction or divided attention lead to reductions in overall memory (e.g., Craik, Govoni, Naveh-Benjamin & Anderson, 1996). However, one method of reducing memory deficits that result from a lack of available attentional resources is to use some form of strategic control to focus attention on the necessary “to be remembered” information, and thereby encourage selectivity about which information is processed (Logan, Sanders, Snyder, Morris, & Buckner, 2002; Perfect & Dasgupta, 1997). This process of strategic control likely relies on a form of attentional control that has been examined using many techniques, and has often shown robust individual differences (e.g., Engle & Kane, 2004). Furthermore, control of attention and working memory has also revealed somewhat striking differences between individuals and various groups and populations in terms of age differences and AD (e.g. Balota & Faust, 2001; Faust & Balota, 2007). However, in many of these studies, the Memory Efficiency & Alzheimer’s Disease 5 critical measure is overall memory quantity, whereas very few studies have examined memory efficiency, which may be related to frontal lobe function and executive control. The present study seeks to examine how attentional control can lead to efficient encoding of high value information, by comparing measures of both memory quantity (number of items recalled) and memory efficiency (the average value of recalled items). Of primary interest is whether memory quantity and efficiency were both selectivity impaired in AD relative to healthy younger and older adults. The link between attentional control and memory performance in AD, and how attentional control can influence memory performance, is the central theme in the current investigation. In order to examine how one can selectively encode information using strategic control, different values (e.g., points) can be assigned to to-be-remembered information, thereby allowing one to examine the extent to which people use this value based information to guide the efficient use of memory (by recalling the high point value items). The selectivity paradigm has been used to this end, and involves presenting items paired with point values, with the point value indicating how important it is to remember each item (see Castel, Benjamin, Craik & Watkins, 2002; Castel, Farb, & Craik, 2007; Hanten, Li, Chapman, Swank, Gamino, Roberson, & Levin, 2007; Watkins & Bloom, 1999). In the selectivity paradigm, participants are presented with lists of words, with each word in the list having a distinct value ranging from 1 point to 12 points. Participants are told to remember as many words as they can, and that their goal is to maximize their score, which is the sum of the point values of each recalled word. After recall, participants are told their score, and then are given a new list, with instructions to Memory Efficiency & Alzheimer’s Disease 6 try to achieve as high a score as possible. In addition to simply measuring the overall total point score achieved, a selectivity index (SI) can be calculated, which is the participant’s score relative to an ideal score based on the number of words recalled. For example, if you were a participant and you recalled three words (the 8, 10, and 12 point words), your score would be 8+10+12 = 30 points. An ideal score (if you recalled 3 words) would be 10+11+12 = 33 points (i.e., recalling the top three value words). Your efficiency index would be your actual score divided by the ideal score, actual/ideal = 30/33 = .91 (see Castel et al., 2002, for more details about the selectivity index). Thus, the SI provides a selectivity, or efficiency, index based on one’s actual score, relative to an idea score, taking into account the number of words recalled. In previous work, although healthy older adults recalled few words than younger adults, their selectivity index was similar to the younger adults. The similarity in SI index occurred because the older adults focused on the high value words to maximize their score, whereas the younger adults recalled high value words and some additional low value words. Thus, the selectivity index provides a useful measure of memory efficiency, one that goes beyond simply measuring the overall quantity of recalled items. The selectivity task can also afford a measure of learning which items to attend to across lists. Specifically, participants are presented with several lists or trials, and after each list they are given feedback about their score, which is the sum of the point values of the words that they recalled. The number of items presented in each list (12) is greater than the typical memory span of an individual, so participants soon realize they cannot remember all of the items. Participants typically learn to modulate which items to attend to, as reflected by the finding that the selectivity index begins to increase across Memory Efficiency & Alzheimer’s Disease 7 successive lists. Thus, in order to achieve an optimal score (i.e., efficient use of memory), participants need to focus or attend to the high value items, and recall them on the immediate memory test. This ability (a form of strategic control over memory) has been examined with children and begins to emerge as early as the age of six (Hanten et al., 2007), and is impaired in children with traumatic brain injury. In addition, Castel (2007) has shown that healthy older adults being to develop a strategy (after several lists) of focusing on the higher value items, in order to maximize their score, despite recalling fewer items relative to younger adults. Thus, although healthy older adults recall fewer words than younger adults, they are efficient in terms of focusing on high value words in order to maximize their overall score. Given that previous research has established that healthy older adults were able to strategically allocate attention to higher value items (see Castel, 2007, for a review), we attempted to extend this work to address whether older adults with very mild and mild AD would display impairments in this type of task. Thus, we were interested in measuring memory capacity (or quantity) as well as the ability to selectivity encode and retrieve information according to value, a form of memory efficiency. Specific impairments in selectivity in AD would suggest that memory impairments in AD are not simply a global memory deficit. The ability to selectively encode information that is of high importance, and distinguish between low and high value information in order to maximize memory efficiency, is crucial to effective use of memory. To examine this issue of memory selectivity, healthy younger and older adults, and individuals with very mild to mild AD, participated in a modified form of the selectivity/selective learning task (e.g., Castel et al., 2002; Hanten et al., 2007). Memory Efficiency & Alzheimer’s Disease 8 In addition to examining how selective encoding is affected by AD, we were also interested in examining how age-related and AD-related changes in executive control measures, as reflected by reading and operation span, might influence selective encoding. According to many models of working memory, attention is allocated to task demands in working memory by a limited capacity central executive (Baddeley, 2000; Engle, Tuholski, Laughlin, & Conway, 1999). Individual differences in the efficiency of the central executive, or working memory capacity, have been shown to predict many higherlevel cognition tasks (see Engle & Kane, 2004 for a review) and have typically been measured using complex span tasks. Because selective encoding in the selectivity task involves strategically allocating limited attention resources to ongoing processing, we were interested in examining whether individual differences in working memory capacity would be related to efficient selection (as measured by the selectivity index). Because age and AD have both been found to reduce the efficiency of the working memory system (Logie, Cocchini, Della Sala, & Baddeley, 2004; McCabe, Robertson & Smith, 2005), we hypothesized that age and AD related changes in working memory capacity would mediate, to some degree, any changes seen in selective encoding. Thus, selectively encoding high value information in the selectivity task requires allocation of attention to high value items while concurrently ignoring or inhibiting low value items, and it was hypothesized that working memory capacity should be related to selective encoding of high value items.