Psychology and Aging 2014, Vol. 29, No. 3, 731-743

© 2014 American Psychological Association 0882-7974/14/$ 12.00

Benefits of Computer-Based Memory and Attention Training in Healthy Older Adults Caroline Chambon, Cathy Herrera, Patricia Romaiguere, Veronique Paban, and Beatrice Alescio-Lautier Aix-Marseille Universite Multifactorial cognitive training programs have a positive effect on cognition in healthy older adults. Among the age-sensitive cognitive domains, episodic memory is the most affected. In the present study, we evaluated the benefits on episodic memory of a computer-based memory and attention training. We targeted consciously controlled processes at encoding and minimizing processing at retrieval, by using more familiarity than recollection during recognition. Such an approach emphasizes processing at encoding and prevents subjects from reinforcing their own errors. Results showed that the training improved recognition performances and induced near transfer to recall. The largest benefits, however, were for tasks with high mental load. Improvement in free recall depended on the modality to recall; semantic recall was improved but not spatial recall. In addition, a far transfer was also observed with better memory self-perception and self-esteem of the participants. Finally, at 6-month follow up, maintenance of benefits was observed only for semantic free recall. The challenge now is to corroborate far transfer by objective measures of everyday life executive functioning. Keywords: older adults, cognitive training program, memory, attention, recognition, recall

Data in healthy older adults suggest that cognitively stimulating activities have a positive effect on cognition (Noice & Noice, 2009; Tranter & Koutstaal, 2008). Memory training programs are classified into two categories. The first one consists of training older participants on a specific mnemonic strategy; for example, the method of loci or the name-face association method (Cavallini, Pagnin, & Vecchi, 2003; Rebok & Balcerak, 1989; Verhaeghen & Marcoen, 1996; Yesavage & Rose, 1984a, 1984b), or on a variety of mnemonic strategies such as mental imagery and organization (Ball et al., 2002; Rankin, Karol, & Tuten, 1984; Rasmusson, Rebok, Bylsma, & Brandt, 1999). Both result in large benefits for the trained task but show limited transfer to other functions. The second category of memory training programs consists of a com­ plex memory task or a set of memory tasks. For instance, working memory training yielded benefits for the practiced tasks and a transfer to untrained memory tasks (Borella, Carretti, Riboldi, & De Beni, 2010; Buschkuehl et al., 2008; Li, Schmiedek, Huxhold, Rocke, Smith, & Lindberger, 2008). Multifactorial cognitive training programs have also been de­ veloped to train memory and other functions, such as attention in older adults. Some data showed that memory performances could be further improved with no transfer to other cognitive tasks (Belleville et al., 2006; Craik et al., 2007; Neely & Backman, 1995; Stigsdotter & Backman, 1989; Stigsdotter Neely, 2000;

Stigsdotter Neely & Backman, 1993), whereas other data showed a transfer to other cognitive abilities such as language (Levine et al., 2007) and enhanced unspecific broad cognitive abilities (Schmiedek, Lovden, & Lindenberger, 2010). Altogether, these findings indicate that, in older adults, all types of training pro­ grams can provide benefits, but the multifactorial approach best promotes transfer to untrained cognitive processes. In a recent study (Herrera, Chambon, Michel, Paban, & AlescioLautier, 2012), we evaluated the benefits of a computer-based multifactorial training focusing on memory and attention, in am­ nesic mild cognitive impairment (aMCI). This training improved recognition performances and induced benefits to episodic free recall. Moreover, benefits remained stable at 6-month follow-up. Based on the positive results obtained on recall in the aMCI population, we now focused on the healthy elderly population. Indeed, free recall is a component of remembering that involves consciously controlled memory retrieval processes, which are af­ fected in aging. It is the core cognitive impairment in patients with aMCI. It would be of interest if such cognitive training could be adapted to the elderly, so as to serve as preventive tool promoting successful aging. Because Craik and Lockhart (1972) showed that controlled processing at encoding provides good support for later retrieval and Bissig and Lustig (2007) showed that processes engaged at encoding could be a highly effective target for memory training, we thus adapted the training evaluated in the aMCI population to target consciously controlled processes to improve episodic recall in elderly. The modifications concern different aspects of the training. One additional task served to work on encoding strategies leading to deeper processing, thus allowing better encoding. Other tasks were used at higher complexity levels. A complex task, that is, a working memory task, was introduced earlier in the training. Finally, after each training exercise, the

Caroline Chambon, Cathy Herrera, Patricia Romaiguere, Veronique Paban, and Beatrice Alescio-Lautier, UMR 7260 CNRS Aix-Marseille University, Neurosciences Integratives and Adaptatives. Correspondence concerning this article should be addressed to Caroline Chambon, UMR 7260 CNRS Aix-Marseille University, Neurosciences Integratives and Adaptatives, 13 331 Marseille, Cedex 03, France. E-mail: [email protected] 731



feedback information was more detailed to allow the subject to consciously act on the more relevant processes for the task. In our training, moreover, we introduced the use of memory strategies and complex memory and attention tasks. We de­ signed the training program based on the notion that memory and attention are highly interactive and interdependent pro­ cesses, because of their functional association and shared cir­ cuitries. Attention is composed of hierarchical subcomponents, and memory is a multidimensional construct. High in the tax­ onomy are complex cognitive abilities such as working mem­ ory, divided attention, and the ability to shift attention between different tasks (Sturm, Willmes, Orgass, & Hartje, 1997). To enhance memory and attention performances throughout train­ ing and to allow subjects to handle the mental and attentional load increase, we systematically trained memory and attention within the same session. We hierarchically ordered training tasks, being attentive to the association established within each domain (memory or attention) and between the two domains. The arrangement of memory and attention tasks during training is described in the Method section. Because the engagement of additional executive resources is limited in the elderly (Capped, Gmeindl, & Reuter-Lorenz, 2010; Reuter-Lorenz & Capped, 2008) and based on the notion that aging spares automatic processing but not effortful processing (Jennings & Jacoby, 1993), the hierarchical order of the training tasks promoted acquisition of automatisms that promote release of attentional resources that could be engaged in a more complex task. Concerning memory training, we acted on several mecha­ nisms. (a) To improve encoding, we cautiously worked with subjects on mnemonic strategies. Indeed, Craik et al. (2007) reported promising results for the rehabilitation of memory functioning in older adults using a variety of strategies and techniques improving organization and memory skids, (b) To improve information maintenance, impaired in aging, in some memory tasks we used the spaced retrieval method (Landauer & Bjork, 1978) in which the subject is taught to retrieve informa­ tion with increasing time intervals after initial presentation. This method was reported efficient in numerous pathologies (Camp & Stevens, 1990; Schacter, Rich, & Stampp, 1985) and helped patients to learn new information, (c) During item rec­ ognition, the elderly are more vulnerable than young adults to interference from distractors appearing in the retention interval (Gazzaley, Cooney, Rissman, & D’Esposito, 2005). To strengthen resistance to interference, in some training exercises we introduced distractors in the interval between the initial presentation and the recognition test, (d) We used recognition as mode of remembering. Recognition relies on two processes used to access encoded information, that is, familiarity de­ scribed as an automatic process, which is preserved in aging (Jennings & Jacoby, 1993), and recollection described as a conscious retrieval process (for review, see Yonelinas, 2002), which displays age-related deficits (Craik & McDowd, 1987; Gutchess et al., 2007). We used recognition tasks built to solicit more familiarity than recollection, thus minimizing processing at retrieval. Minimizing the effort during recovery made the subjects experience reward for the effort they provided during encoding. Moreover, because training is better if subjects are prevented from reinforcing their own errors, it is of interest to use familiarity, rather than recollection, because it leads to

much less retrieval failures. This endorses the definition of “error reduction” proposed by Fillingham, Hodgson, Sage, and Lambon Ralph (2003). Regarding attention training, we repeatedly administered several focused and divided attention tasks in a hierarchy based on the model of Van Zomeren and Brouwer (1994), which highlights areas of strength and selectivity of attention. For each hierarchical step of the selectivity axis, hierarchical steps of the intensity axis were embedded. Such hierarchies have been successfully used by Sturm et al. (1997) in training of attention only. Because numerous studies demonstrated a prominent role of processing speed in age-related cognitive decline (Salthouse, 1996), we also focused on increasing processing speed through­ out training. We used a guided procedure that was repeated until the subjects had acquired the automatisms to properly perform the task, and then asked them to increase their execu­ tion speed. In addition, computer-based training allows greater complexity in task design and provides greater accuracy for individualized parameter adaptation. These features allow control of ceiling and floor effects, which are both important for successful cognitive exercise, because individuals are continually cognitively chal­ lenged. This computer-based training program differs from other pro­ grams for older adults in several points, (a) We embedded exec­ utive mechanisms such as inhibition and flexibility in both atten­ tion and memory tasks, (b) Mnemonic and executive strategies were implemented progressively throughout training according to the difficulties encountered by the subject. Among the proposed strategies, the subjects could choose the one they believed to be best for them, which favored metacognition, (c) Based on perfor­ mances from the pretraining session and the beginning of training, we proposed easy tasks at the beginning of training and more complex ones at later sessions; the difficulty of the tasks was dynamically adapted to each subject’s progression. In other words, we adjusted the level of exigency and complexity of the training according to the skills of the persons and to their progress during training, (d) We emphasized controlled processing at encoding but minimized it at retrieval to allow the subjects to cope with the increasing mental and attentional load throughout training but maintain good performances. To evaluate the benefits of this personalized training on episodic recall, many measures were taken. First, we assessed near transfer to the untrained memory retrieval component; that is, episodic free recall, by using the 16-item free reminding test (RL/RI-16 test; Van der Linden et al., 2004) and the 12-word recall test from the memory efficiency battery (BEM-144) (Signoret, 1991) for semantic material, and by a computerbased letter-location association recall task developed in our laboratory for visuospatial material. We also measured effects of training on recognition using the visual recognition subtest from the Doors and People test (Baddeley, Emslie, & NimmoSmith, 1994), which has the same material and retrieval process as the practiced tasks. Then, far transfer was evaluated by the Memory Functioning Questionnaire (MFQ; Gilewski, Zelinski, & Schaie, 1990) to assess the participant’s self-perception of everyday memory functioning after training, and by the Rosen­ berg Self-Esteem Scale (RSE; Rosenberg, 1965).


Method Participants and Screening for Eligibility Participants were volunteering elderly with good cognitive sta­ tus, living independently in the community. They were recruited mainly through flyers distributed by general practitioners, physio­ therapists, associations for senior citizens, and social clubs and by personal contacts. In the screening for eligibility, 51 volunteers were interviewed at home by a neuropsychologist during a 120-min session. During this session, the study plan and the research procedure were clearly explained. All included subjects expressed their will to participate in the study and answered a questionnaire estimating their health status, medications, and educational level. Cognitive screening was performed to characterize the participants and exclude depres­ sion, mild cognitive impairment (MCI), or dementia. Volunteers were evaluated with Mini-Mental State Examination (MMSE; Folstein, Folstein, & McHugh, 1975), the Clinical Dementia Rat­ ing scale (CDR; Hughes, Berg, Danzinger, Coben, & Martin, 1982), the Instrumental Activities of Daily Living scale (IADL; Lawton & Brody, 1969), and the 30-item version of the Geriatric Depression Scale (GDS; Yesavage et ah, 1982-1983). Exclusion criteria for the study were (a) a MMSE score 33) after training. This could be explained by conscious awareness on the part of subjects about

what they were able to do and even to succeed in tasks they were not used to doing before training. This reasoning can be applied for the leisure-type training, as well as for the memory and attention one but the larger increase observed for the Training group, that is, 5 points, relative to the Leisure group; that is, 2 points, indicates a larger effect on self-esteem for people trained with our memory and attention training even though there was no significant differ­ ence between the two groups. While healthy elderly persons tend to gradually depreciate the inner representation of their memory because they underestimate their effective memory abilities and systematically exaggerate their memory difficulties, our computer-based memory and atten­ tion training may have positively influenced their self-esteem by showing them that they were able to perform correctly in memory tasks. Moreover, the use of a media such as a computer may also partially explain the greater benefits observed in self-esteem for the Training group compared with the Leisure one.

Benefits Maintenance Note that although our training used recognition as retrieval process, benefits on visual recognition were not present anymore at 6-month follow up, even if there was a tendency to maintain in part A of the task (Figure 1). Such data indicate that if the age-sensitive recognition memory can be improved by training, the process needs to be regularly trained to maintain benefits in particular in challenging conditions; that is, part B of the Doors and People test. At 6-month follow up, benefits maintenance was also observed for the immediate and delayed free recall of semantic material assessed in the 12-word recall test (Figure 3). During training, subjects used encoding strategies that made information process­ ing deeper. It is thus likely that they actively used these strategies to improve their memory and better recall words in the 12-word recall test. The RL/RI-16 test uses the same semantic material as the 12-word recall test but is easier because of forced encoding. It was thus surprising to observe a weaker benefit in the RL/RI-16, and this was all the more prominent on the delayed free recall at T3 where the benefit observed at T2 was lost. An explanation could be that, because of the forced encoding, subjects passively memorized words and thus the information was superficially processed, which weakened the recall. Benefits of training on the free recall of a letter-location asso­ ciation were stable at 6-month follow up (Figure 4). Because this condition involves a large attentional demand and a high memory load, such results are in favor of the hypothesis that the deeper the information processing during training, the longer and better the recall. Such a long-lasting effect of a multidomain training on untrained immediate and delayed recall has been reported (Cheng et al., 2012), indicating that this memory process does not need a permanent cognitive training to display maintenance of good per­ formances.

Conclusion In the present study, we highlighted that a personalized computer-based memory and attention training that emphasizes highly controlled processes during encoding, and familiarity dur­ ing retrieval, improves performances of both recognition and re­ call. The larger benefits observed on recall relative to recognition,


although training used recognition as retrieval process, may be explained by our using only the familiarity aspect of recognition at retrieval but also our targeting controlled processes at encoding. Moreover, we showed that free recall of semantic material was improved whereas free recall of spatial material was not, indicating that the free recall improvements observed depend on the material to recall, that is, manipulation of spatial information being more age-sensitive than that of semantic information. Such results high­ light that, to improve manipulation of spatial information in the elderly, training should be incremented with additional pure spatial tasks. The present results also underline that the larger training benefits are for tasks with the higher mental load such as part B of the doors recognition subtest, the 12-word recall test, and the free recall of a letter-location association task. Interestingly, our results highlight benefits on participants’ self-perception of memory and self-esteem, reflecting a far transfer to untrained abilities induced by our personalized computer-based memory and attention train­ ing. In addition, we think that using a media such as a computer during training partially explains the difference in benefits be­ tween both trainings, computer-based and paper-and-pencil. Fi­ nally, at 6-month follow up, maintenance of benefits was observed only for semantic free recall, indicating that to maintain all benefits and thus to fight age-related cognitive decline sustainably, such cognitive training has to be regularly practiced. The next challenge would be to propose a preventive training method for healthy older adults that would protect them against age-related cognitive decline. Further studies will be necessary (a) to evaluate how the training should be practiced to highlight a stabilization of cognitive performances, and in particular longitu­ dinal studies to validate effects preventing age-related cognitive decline but also (b) to evaluate whether such training may induce additional far transfer, as the participant’s memory self-perception and self-esteem were better after training, everyday life executive functioning should be objectively measured.

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Received December 2, 2013 Revision received May 28, 2014 Accepted June 5, 2014 ■

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Benefits of computer-based memory and attention training in healthy older adults.

Multifactorial cognitive training programs have a positive effect on cognition in healthy older adults. Among the age-sensitive cognitive domains, epi...
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