Psychology and Aging 2014, Vol. 29, No. 3, 731-743
© 2014 American Psychological Association 0882-7974/14/$ 12.00 http://dx.doi.org/10.1037/a0037477
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
732
CHAMBON ET AL.
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).
BENEFITS OF MEMORY-ATTENTION TRAINING IN ELDERLY
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,
BENEFITS OF MEMORY-ATTENTION TRAINING IN ELDERLY
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.
References Baddeley, A. D., Emslie, H., & Nimmo-Smith, I. (1994). Doors and people: A test o f visual and verbal recall and recognition. Bury St. Edmunds, England: Thames Valley Test Co. Ball, K., Berch, D. B., Helmers, K. F., Jobe, J. B., Leveck, M. D., Marsiske, M .,. . . Advanced Cognitive Training for Independent and Vital Elderly Study Group. (2002). Effects of cognitive training interventions with older adults: A randomized controlled trial. JAMA: The Journal o f the American Medical Association, 288, 2271-2281. doi:10.1001/jama.288 .18.2271 Belleville, S., Gilbert, B., Fontaine, F., Gagnon, L., Menard, E., & Gau thier, S. (2006). Improvement of episodic memory in persons with mild cognitive impairment and healthy older adults: Evidence from a cogni tive intervention program. Dementia and Geriatric Cognitive Disorders, 22, 486-499. doi:l0.1159/000096316 Bissig, D., & Lustig, C. (2007). Who benefits from memory training? Psy chological Science, 18, 720-726. doi:10.1111/j.l467-9280.2007.01966.x Borella, E., Carretti, B., Riboldi, F., & De Beni, R. (2010). Working memory training in older adults: Evidence of transfer and maintenance effects. Psychology and Aging, 25, 767-778. doi:10.1037/a0020683 Buschkuehl, M., Jaeggi, S. M., Hutchison, S., Perrig-Chiello, P., Dapp, C„ Muller, M .,. . . Perrig, W. J. (2008). Impact of working memory training on memory performance in old-old adults. Psychology and Aging, 23, 743-753. doi:10.1037/a0014342
741
Camp, C. J., & Stevens, A. B. (1990). Spaced-retrieval: A memory inter vention for dementia of the Alzheimer’s type (DAT). Clinical Geron tologist: The Journal o f Aging and Mental Health, 10, 58-61. Cansino, S„ Hemdndez-Ramos, E„ Estrada-Manilla, C., Torres-Trejo, F., Martlnez-Galindo, J. G., Ayala-Hernandez, M., . . . Rodrfguez-Ortiz, M. D. (2013). The decline of verbal and visuospatial working memory across the adult life span. Age (Dordrecht, Netherlands), 35, 2283-2302. doi: 10.1007/s 11357-013-9531-1 Cappell, K. A., Gmeindl, L., & Reuter-Lorenz, P. A. (2010). Age differ ences in prefrontal recruitment during verbal working memory mainte nance depend on memory load. Cortex: A Journal Devoted to the Study o f the Nervous System and Behavior, 46, 462-473. doi:10.1016/j.cortex .2009.11.009 Cavallim, E., Pagnin, A., & Vecchi, T. (2003). Aging and everyday memory: The beneficial effect of memory training. Archives o f Gerontology and Geriatrics, 37, 241-257. doi:10.1016/S0167-4943(03)00063-3 Cheng, Y., Wu, W., Feng, W., Wang, J., Chen, Y., Shen, Y., . . . Li, C. (2012). The effects of multi-domain versus single-domain cognitive training in non-demented older people: A randomized controlled trial. BMC Medicine, 10, 30-42. doi:10.1186/1741-7015-10-30 Cohen, J. (1988). Statistical power analysis fo r the behavioral sciences. San Diego, CA: Academic Press. Craik, F. I. M., & Lockhart, R. S. (1972). Levels of processing: A framework for memory research. Journal o f Verbal Learning & Verbal Behavior, 11, 671-684. doi:10.1016/S0022-5371(72)80001-X Craik, F. I. M., & McDowd, J. M. (1987). Age differences in recall and recognition. Journal o f Experimental Psychology: Learning, Memory, and Cognition, 13, 474-479. doi:10.1037/0278-7393.13.3.474 Craik, F. I. M., Winocur, G., Palmer, H., Binns, M. A., Edwards, M., Bridges, K., . . . Stuss, D. T. (2007). Cognitive rehabilitation in the elderly: Effects on memory. Journal o f the International Neuropsycho logical Society: JINS, 13, 132-142. doi:10.1017/S1355617707070166 Davidson, P. S. R., & Glisky, E. L. (2002). Neuropsychological correlates of recollection and familiarity in normal aging. Cognitive, Affective & Behavioral Neuroscience, 2, 174-186. doi:10.3758/CABN.2.2.174 De Vreese, L. P., Belloi, L., Iacono, S., Finelli, C., & Neri, M. (1998). Memory training programs in memory complainers: Efficacy on objec tive and subjective memory functioning. Archives o f Gerontology and Geriatrics, 26, 141-154. doi:10.1016/S0167-4943(98)80022-8 Fillingham, J. K„ Hodgson, C., Sage, K., & Lambon Ralph, M. A. (2003). The application of errorless learning to aphasic disorders: A review of theory and practice. Neuropsychological Rehabilitation, 13, 337-363. doi: 10.1080/09602010343000020 Floyd, M., & Scogin, F. (1997). Effects of memory training on the subjective memory functioning and mental health of older adults: A meta-analysis. Psychology and Aging, 12, 150-161. doi: 10.1037/08827974.12.1.150 Folstein, M. F., Folstein, S. E., & McHugh, P. R. (1975). “Mini-mental state”: A practical method for grading the cognitive state of patients for the clinician. Journal o f Psychiatric Research, 12, 189-198. doi:10.1016/00223956(75)90026-6 Friedman, D., Nessler, D., & Johnson, R„ Jr. (2007). Memory encoding and retrieval in the aging brain. Clinical EEG and Neuroscience, 38, 2-7. doi:10.1177/155005940703800105 Gardiner, J. M„ & Java, R. I. (1990). Recollective experience in word and nonword recognition. Memory & Cognition, 18, 23-30. doi:10.3758/ BF03202642 Gazzaley, A., Cooney, J. W„ Rissman, J., & D ’Esposito, M. (2005). Top-down suppression deficit underlies working memory impairment in normal aging. Nature Neuroscience, 8, 1298-1300. doi:10.1038/nnl543 Gilewski, M. J., Zelinski, E. M„ & Schaie, K. W. (1990). The Memory Functioning Questionnaire for assessment of memory complaints in adulthood and old age. Psychology and Aging, 5, 482-490. doi: 10.1037/ 0882-7974.5.4.482
742
CHAMBON ET AL.
Golby, A. J.. Poldrack, R. A., Brewer, J, B„ Spencer, D., Desmond, J. E., Aron, A. P., & Gabrieli, J. D. (2001). Material-specific lateralization in the medial temporal lobe and prefrontal cortex during memory encoding. Brain: A Journal o f Neurology, 124, 1841-1854. doi:10.1093/brain/124 .9.1841 Guelfi, J. D. (1996). Devaluation clinique standardisee en psychiatrie: Tome II (Gdriatrie, pediatrie, psychoses, effets secondaires, divers). [The standardized clinical assessment in psychiatry: Volume II (Geriatrics, pediatrics, psychoses, side effects, divers)]. Boulogne, France: Editions Medicales Pierre Fabre. Gutchess, A. H., Hebrank, A., Sutton, B. P., Leshikar, E., Chee, M. W. L., Tan, J. C .,. . . Park, D. C. (2007). Contextual interference in recognition memory with age. Neuroimage, 35, 1338-1347. doi:10.1016/j.neuroimage.2007.01 .043 Henke. K.. Buck, A., Weber, B„ & Wieser, H. G. (1997). Human hip pocampus establishes associations in memory. Hippocampus, 7, 2 4 9 256. doi: 10.1002/(SICI) 1098-1063(1997)7:3 3.0 .CO;2-G Herrera, C., Chambon, C., Michel, B. F., Paban, V., & Alescio-Lautier, B. (2012). Positive effects of computer-based cognitive training in adults with mild cognitive impairment. Neuropsychologia, 50, 1871-1881. doi: 10.1016/j .neuropsychologia.2012.04.012 Hertel, P. T., Benbow, A. A., & Geraerts, E. (2012). Brooding deficits in memory: Focusing attention improves subsequent recall. Cognition and Emotion, 26, 1516-1525. doi:10.1080/02699931.2012.668852 Howard, M. W., Bessette-Symons, B., Zhang, Y., & Hoyer, W. J. (2006). Aging selectively impairs recollection in recognition memory for pic tures: Evidence from modeling and receiver operating characteristic curves. Psychology and Aging, 21, 96-106. doi: 10.1037/0882-7974.21 .1.96 Hughes, C. P., Berg, L„ Danziger, W. L., Coben, L. A., & Martin, R. L. (1982). A new clinical scale for the staging of dementia. The British Journal o f Psychiatry, 140, 566-572. doi: 10.1192/bjp. 140.6.566 Jennings, J. M., & Jacoby, L. L. (1993). Automatic versus intentional uses of memory: Aging, attention, and control. Psychology and Aging, 8, 283-293. doi: 10.1037/0882-7974.8.2.283 Johnston, W. A., Dark, V. J., & Jacoby, L. L. (1985). Perceptual fluency and recognition judgements. Journal o f Experimental Psychology, 11, 3-11. Kelley, W. M., Miezin, F. M., McDermott, K. B., Buckner, R. L., Raichle, M. E., Cohen, N. J........Petersen, S. E. (1998). Hemispheric specialization in human dorsal frontal cortex and medial temporal lobe for verbal and nonverbal memory encoding. Neuron, 20, 927-936. doi:10.1016/S08966273(00)80474-2 Kirchhoff, B. A., Anderson, B. A., Barch, D. M„ & Jacoby, L. L. (2012). Cognitive and neural effects of semantic encoding strategy training in older adults. Cerebral Cortex, 22, 788-799. doi:10.1093/cercor/bhrl29 Landauer, T. K., & Bjork, R. A. (1978). Optimum rehearsal patterns and name learning. In M. M. Gruneberg, P. E. Morris, & R. N. Sykes (Eds.), Practical aspects o f memory (pp. 625-632). New York, NY: Academic Press. Lawton, M. P., & Brody, E. M. (1969). Assessment of older people: Self-maintaining and instrumental activities of daily living. The Geron tologist, 9, 179-186. doi: 10.1093/geront/9.3_Part_l. 179 Levine, B., Stuss, D. T., Winocur, G., Binns, M. A., Fahy, L., Mandic, M., . . . Robertson, I. H. (2007). Cognitive rehabilitation in the elderly: Effects on strategic behavior in relation to goal management. Journal of the International Neuropsychological Society: JINS, 13, 143—152. doi: 10.1017/S1355617707070178 Li, S.-C., Schmiedek, F., Huxhold, O., Rocke, C., Smith, J., & Lindenberger, U. (2008). Working memory plasticity in old age: Practice gain, transfer, and maintenance. Psychology and Aging, 23, 731-742. doi: 10.1037/a0014343
Marklund, P., Fransson, P., Cabeza, R„ Petersson, K. M., Ingvar, M., & Nyberg, L. (2007). Sustained and transient neural modulations in pre frontal cortex related to declarative long-term memory, working mem ory, and attention. Cortex: A Journal Devoted to the Study o f the Nervous System and Behavior, 43, 22-37. McKhann, G., Drachman, D., Folstein, M., Katzman, R., Price, D., & Stadlan, E. M. (1984). Clinical diagnosis of Alzheimer’s disease: Report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer’s Disease. Neurology, 34, 939-944. doi:10.1212AVNL.34.7.939 Nee, D. E., & Jonides, J. (2011). Dissociable contributions of prefrontal cortex and the hippocampus to short-term memory: Evidence for a 3-state model of memory. Neuroimage, 54, 1540-1548. doi:10.1016/j .neuroimage.2010.09.002 Neely, A. S., & Backman, L. (1993). Long-term maintenance of gains from memory training in older adults: Two 3 1/2-year follow-up studies. Journal o f Gerontology, 48, P233-P237. doi:10.1093/geronj/48.5.P233 Neely, A. S., & Backman, L. (1995). Effects of multifactorial memory training in old age: Generalizability across tasks and individuals. The Journals o f Gerontology Series B; Psychological Sciences and Social Sciences, 50, P134-P140. doi:10.1093/geronb/50B.3.P134 Noice, H., & Noice, T. (2009). An arts intervention for older adults living in subsidized retirement homes. Neuropsychology, Development, and Cognition Section B. Aging, Neuropsychology and Cognition, 16, 5 6 79. doi: 10.1080/13825580802233400 Optale, G., Urgesi, C., Busato, V., Marin, S., Piron, L., Priftis, K .,. . . Bordin, A. (2010). Controlling memory impairment in elderly adults using virtual reality memory training: A randomized controlled pilot study. Neurorehabilitation and Neural Repair, 24, 348-357. doi: 10.1177/1545968309353328 Petersen, R. C., Smith, G. E„ Waring, S. C„ Ivnik, R. J., Tangalos, E. G„ & Kokmen, E. (1999). Mild cognitive impairment: Clinical character ization and outcome. Archives o f Neurology, 56, 303-308. doi: 10.1001/ archneur.56.3.303 Rankin, J. L., Karol, R., & Tuten, C. (1984). Strategy use, recall, and recall organization in young, middle-aged, and elderly adults. Experimental Aging Research, 10, 193-196. doi:10.1080/03610738408258463 Rasmusson, D. X., Rebok, G. W., Bylsma, F. W., & Brandt, J. (1999). Effects of three types of memory training in normal elderly. Aging, Neuropsychology, and Cognition, 6, 56-66. doi: 10.1076/anec.6.1.56 .790 Rebok, G. W., & Balcerak, L. J. (1989). Memory self-efficacy and per formance differences in young and old adults: Effects of mnemonic training. Developmental Psychology, 25, 714-721. doi: 10.1037/00121649.25.5.714 Reuter-Lorenz, P. A., & Capped, K. (2008). Neurocognitive aging and the compensation hypothesis. Current Directions in Psychological Science, 17, 177-182. doi: 10. I l l 1/j. 1467-8721.2008.00570.x Rosenberg, M. (1965). Society and the adolescent self-image. Princeton, NJ: Princeton University Press. Salthouse, T. A. (1996). The processing-speed theory of adult age differ ences in cognition. Psychological Review, 103, 403-428. doi: 10.1037/ 0033-295X. 103.3.403 Schacter, D. L., Rich, S. A., & Stampp, M. S. (1985). Remediation of memory disorders: Experimental evaluation of the spaced-retrieval tech nique. Journal o f Clinical and Experimental Neuropsychology, 7, 7 9 96. doi: 10.1080/01688638508401243 Schmiedek, F., Lovden, M., & Lindenberger, U. (2010). Hundred days of cognitive training enhance broad cognitive abilities in adulthood: Find ings from the COGITO Study. Frontiers in Aging Neuroscience, 2, 1-10. doi: 10.3389/fnagi.2010.00027 Signoret, J. L. (1991). Batterie d ’efficience mnesique BEM 144. Paris, France: Editions Scientifiques Elsevier.
BENEFITS OF MEMORY-ATTENTION TRAINING IN ELDERLY Stigsdotter, A., & Backman, L. (1989). Multifactorial memory training with older adults: How to foster maintenance of improved performance. Gerontology, 35, 260-267. doi:10.1159/000213035 Stigsdotter Neely, A. (2000). Multifactorial memory training in normal aging: In search of memory improvement beyond the ordinary. In D. R. Hill, L. Backman, & A. Stigsdotter-Neely (Eds.), Cognitive rehabilita tion in old age (pp. 63-80). New York, NY: Oxford University Press. Stigsdotter Neely, A. S., & Backman, L. (1993). Maintenance of gains fol lowing multifactorial and unifactorial memory training in adulthood. Edu cational Gerontology, 19, 105-117. doi:10.1080/0360127930190202 Sturm, W., Willmes, K., Orgass, B., & Hartje, W. (1997). Do specific attention deficits need specific training? Neuropsychological Rehabili tation, 7, 81-103. doi: 10.1080/713755526 Tranter, L. J., & Koutstaal, W. (2008). Age and flexible thinking: An exper imental demonstration of the beneficial effects of increased cognitively stimulating activity on fluid intelligence in healthy older adults. Neuropsy chology, Development, and Cognition Section B, Aging, Neuropsychology and Cognition, 15, 184-207. doi:10.1080/13825580701322163 Valentijn, S. A. M., Hill, R. D., Van Hooren, S. A. H., Bosma, H., Van Boxtel, M. P. J., Jolles, J„ & Ponds, R. W. H. M. (2006). Memory self-efficacy predicts memory performance: Results from a 6-year follow-up study. Psychology and Aging, 21, 165-172. doi:10.1037/ 0882-7974.21.2.165 Valentijn, S. A. M., van Hooren, S. A. H., Bosma, H., Touw, D. M., Jolles, J., van Boxtel, M. P. J., & Ponds, R. W. H. M. (2005). The effect of two types of memory training on subjective and objective memory perfor mance in healthy individuals aged 55 years and older: A randomized controlled trial. Patient Education and Counseling, 57, 106-114. doi: 10.1016/j.pec.2004.05.002
743
Van der Linden, M., Coyette, F., Poitrenaud, J., Kalafat, M., Calacis, F., Wyns, C., & Adam, S. (2004). The 16-items free recall/cued recall test (RL/RI 16). In M. Van der Linden, S. Adam, A. Agniel, C. BaissetMouly, F. Bardet, F. Coyette, . . . C. Thomas-Anterion (Eds.), L'evaluation des troubles de la memoire: Presentation de quatre tests de memoire episodique (avec leur etalonnage). Marseille, France: Solal. van Zomeren, A. H., & Brouwer, W. H. (1994). Clinical neuropsychology o f attention. New York, NY: Oxford University Press. Verhaeghen, P., & Marcoen, A. (1996). On the mechanisms of plasticity in young and older adults after instruction in the method of loci: Evidence for an amplification model. Psychology and Aging, 11, 164-178. doi: 10.1037/0882-7974.11.1.164 Yesavage, J. A., Brink, T. L., Rose, T. L., Lum, O., Huang, V., Adey, M., & Leirer, V. O. (1982-1983). Development and validation of a geriatric depression screening scale: A preliminary report. Journal o f Psychiatric Research, 17, 37-49. doi:10.1016/0022-3956(82)90033-4 Yesavage, J. A., & Rose, T. L. (1984a). Semantic elaboration and the method of loci: A new trip for older learners. Experimental Aging Research, 10, 155-159. doi: 10.1080/03610738408258560 Yesavage, J. A., & Rose, T. L. (1984b). The effects of a face-name mnemonic in young, middle-aged, and elderly adults. Experimental Aging Research, 10, 55-57. doi:10.1080/03610738408258543 Yonelinas, A. P. (2002). The nature of recollection and familiarity: A review of 30 years of research. Journal o f Memory and Language, 46, 441-517. doi: 10.1006/jmla.2002.2864
Received December 2, 2013 Revision received May 28, 2014 Accepted June 5, 2014 ■
Copyright of Psychology & Aging is the property of American Psychological Association and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.
© 2014 American Psychological Association 0882-7974/14/$ 12.00 http://dx.doi.org/10.1037/a0037477
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
732
CHAMBON ET AL.
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).
BENEFITS OF MEMORY-ATTENTION TRAINING IN ELDERLY
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,
BENEFITS OF MEMORY-ATTENTION TRAINING IN ELDERLY
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.
References Baddeley, A. D., Emslie, H., & Nimmo-Smith, I. (1994). Doors and people: A test o f visual and verbal recall and recognition. Bury St. Edmunds, England: Thames Valley Test Co. Ball, K., Berch, D. B., Helmers, K. F., Jobe, J. B., Leveck, M. D., Marsiske, M .,. . . Advanced Cognitive Training for Independent and Vital Elderly Study Group. (2002). Effects of cognitive training interventions with older adults: A randomized controlled trial. JAMA: The Journal o f the American Medical Association, 288, 2271-2281. doi:10.1001/jama.288 .18.2271 Belleville, S., Gilbert, B., Fontaine, F., Gagnon, L., Menard, E., & Gau thier, S. (2006). Improvement of episodic memory in persons with mild cognitive impairment and healthy older adults: Evidence from a cogni tive intervention program. Dementia and Geriatric Cognitive Disorders, 22, 486-499. doi:l0.1159/000096316 Bissig, D., & Lustig, C. (2007). Who benefits from memory training? Psy chological Science, 18, 720-726. doi:10.1111/j.l467-9280.2007.01966.x Borella, E., Carretti, B., Riboldi, F., & De Beni, R. (2010). Working memory training in older adults: Evidence of transfer and maintenance effects. Psychology and Aging, 25, 767-778. doi:10.1037/a0020683 Buschkuehl, M., Jaeggi, S. M., Hutchison, S., Perrig-Chiello, P., Dapp, C„ Muller, M .,. . . Perrig, W. J. (2008). Impact of working memory training on memory performance in old-old adults. Psychology and Aging, 23, 743-753. doi:10.1037/a0014342
741
Camp, C. J., & Stevens, A. B. (1990). Spaced-retrieval: A memory inter vention for dementia of the Alzheimer’s type (DAT). Clinical Geron tologist: The Journal o f Aging and Mental Health, 10, 58-61. Cansino, S„ Hemdndez-Ramos, E„ Estrada-Manilla, C., Torres-Trejo, F., Martlnez-Galindo, J. G., Ayala-Hernandez, M., . . . Rodrfguez-Ortiz, M. D. (2013). The decline of verbal and visuospatial working memory across the adult life span. Age (Dordrecht, Netherlands), 35, 2283-2302. doi: 10.1007/s 11357-013-9531-1 Cappell, K. A., Gmeindl, L., & Reuter-Lorenz, P. A. (2010). Age differ ences in prefrontal recruitment during verbal working memory mainte nance depend on memory load. Cortex: A Journal Devoted to the Study o f the Nervous System and Behavior, 46, 462-473. doi:10.1016/j.cortex .2009.11.009 Cavallim, E., Pagnin, A., & Vecchi, T. (2003). Aging and everyday memory: The beneficial effect of memory training. Archives o f Gerontology and Geriatrics, 37, 241-257. doi:10.1016/S0167-4943(03)00063-3 Cheng, Y., Wu, W., Feng, W., Wang, J., Chen, Y., Shen, Y., . . . Li, C. (2012). The effects of multi-domain versus single-domain cognitive training in non-demented older people: A randomized controlled trial. BMC Medicine, 10, 30-42. doi:10.1186/1741-7015-10-30 Cohen, J. (1988). Statistical power analysis fo r the behavioral sciences. San Diego, CA: Academic Press. Craik, F. I. M., & Lockhart, R. S. (1972). Levels of processing: A framework for memory research. Journal o f Verbal Learning & Verbal Behavior, 11, 671-684. doi:10.1016/S0022-5371(72)80001-X Craik, F. I. M., & McDowd, J. M. (1987). Age differences in recall and recognition. Journal o f Experimental Psychology: Learning, Memory, and Cognition, 13, 474-479. doi:10.1037/0278-7393.13.3.474 Craik, F. I. M., Winocur, G., Palmer, H., Binns, M. A., Edwards, M., Bridges, K., . . . Stuss, D. T. (2007). Cognitive rehabilitation in the elderly: Effects on memory. Journal o f the International Neuropsycho logical Society: JINS, 13, 132-142. doi:10.1017/S1355617707070166 Davidson, P. S. R., & Glisky, E. L. (2002). Neuropsychological correlates of recollection and familiarity in normal aging. Cognitive, Affective & Behavioral Neuroscience, 2, 174-186. doi:10.3758/CABN.2.2.174 De Vreese, L. P., Belloi, L., Iacono, S., Finelli, C., & Neri, M. (1998). Memory training programs in memory complainers: Efficacy on objec tive and subjective memory functioning. Archives o f Gerontology and Geriatrics, 26, 141-154. doi:10.1016/S0167-4943(98)80022-8 Fillingham, J. K„ Hodgson, C., Sage, K., & Lambon Ralph, M. A. (2003). The application of errorless learning to aphasic disorders: A review of theory and practice. Neuropsychological Rehabilitation, 13, 337-363. doi: 10.1080/09602010343000020 Floyd, M., & Scogin, F. (1997). Effects of memory training on the subjective memory functioning and mental health of older adults: A meta-analysis. Psychology and Aging, 12, 150-161. doi: 10.1037/08827974.12.1.150 Folstein, M. F., Folstein, S. E., & McHugh, P. R. (1975). “Mini-mental state”: A practical method for grading the cognitive state of patients for the clinician. Journal o f Psychiatric Research, 12, 189-198. doi:10.1016/00223956(75)90026-6 Friedman, D., Nessler, D., & Johnson, R„ Jr. (2007). Memory encoding and retrieval in the aging brain. Clinical EEG and Neuroscience, 38, 2-7. doi:10.1177/155005940703800105 Gardiner, J. M„ & Java, R. I. (1990). Recollective experience in word and nonword recognition. Memory & Cognition, 18, 23-30. doi:10.3758/ BF03202642 Gazzaley, A., Cooney, J. W„ Rissman, J., & D ’Esposito, M. (2005). Top-down suppression deficit underlies working memory impairment in normal aging. Nature Neuroscience, 8, 1298-1300. doi:10.1038/nnl543 Gilewski, M. J., Zelinski, E. M„ & Schaie, K. W. (1990). The Memory Functioning Questionnaire for assessment of memory complaints in adulthood and old age. Psychology and Aging, 5, 482-490. doi: 10.1037/ 0882-7974.5.4.482
742
CHAMBON ET AL.
Golby, A. J.. Poldrack, R. A., Brewer, J, B„ Spencer, D., Desmond, J. E., Aron, A. P., & Gabrieli, J. D. (2001). Material-specific lateralization in the medial temporal lobe and prefrontal cortex during memory encoding. Brain: A Journal o f Neurology, 124, 1841-1854. doi:10.1093/brain/124 .9.1841 Guelfi, J. D. (1996). Devaluation clinique standardisee en psychiatrie: Tome II (Gdriatrie, pediatrie, psychoses, effets secondaires, divers). [The standardized clinical assessment in psychiatry: Volume II (Geriatrics, pediatrics, psychoses, side effects, divers)]. Boulogne, France: Editions Medicales Pierre Fabre. Gutchess, A. H., Hebrank, A., Sutton, B. P., Leshikar, E., Chee, M. W. L., Tan, J. C .,. . . Park, D. C. (2007). Contextual interference in recognition memory with age. Neuroimage, 35, 1338-1347. doi:10.1016/j.neuroimage.2007.01 .043 Henke. K.. Buck, A., Weber, B„ & Wieser, H. G. (1997). Human hip pocampus establishes associations in memory. Hippocampus, 7, 2 4 9 256. doi: 10.1002/(SICI) 1098-1063(1997)7:3 3.0 .CO;2-G Herrera, C., Chambon, C., Michel, B. F., Paban, V., & Alescio-Lautier, B. (2012). Positive effects of computer-based cognitive training in adults with mild cognitive impairment. Neuropsychologia, 50, 1871-1881. doi: 10.1016/j .neuropsychologia.2012.04.012 Hertel, P. T., Benbow, A. A., & Geraerts, E. (2012). Brooding deficits in memory: Focusing attention improves subsequent recall. Cognition and Emotion, 26, 1516-1525. doi:10.1080/02699931.2012.668852 Howard, M. W., Bessette-Symons, B., Zhang, Y., & Hoyer, W. J. (2006). Aging selectively impairs recollection in recognition memory for pic tures: Evidence from modeling and receiver operating characteristic curves. Psychology and Aging, 21, 96-106. doi: 10.1037/0882-7974.21 .1.96 Hughes, C. P., Berg, L„ Danziger, W. L., Coben, L. A., & Martin, R. L. (1982). A new clinical scale for the staging of dementia. The British Journal o f Psychiatry, 140, 566-572. doi: 10.1192/bjp. 140.6.566 Jennings, J. M., & Jacoby, L. L. (1993). Automatic versus intentional uses of memory: Aging, attention, and control. Psychology and Aging, 8, 283-293. doi: 10.1037/0882-7974.8.2.283 Johnston, W. A., Dark, V. J., & Jacoby, L. L. (1985). Perceptual fluency and recognition judgements. Journal o f Experimental Psychology, 11, 3-11. Kelley, W. M., Miezin, F. M., McDermott, K. B., Buckner, R. L., Raichle, M. E., Cohen, N. J........Petersen, S. E. (1998). Hemispheric specialization in human dorsal frontal cortex and medial temporal lobe for verbal and nonverbal memory encoding. Neuron, 20, 927-936. doi:10.1016/S08966273(00)80474-2 Kirchhoff, B. A., Anderson, B. A., Barch, D. M„ & Jacoby, L. L. (2012). Cognitive and neural effects of semantic encoding strategy training in older adults. Cerebral Cortex, 22, 788-799. doi:10.1093/cercor/bhrl29 Landauer, T. K., & Bjork, R. A. (1978). Optimum rehearsal patterns and name learning. In M. M. Gruneberg, P. E. Morris, & R. N. Sykes (Eds.), Practical aspects o f memory (pp. 625-632). New York, NY: Academic Press. Lawton, M. P., & Brody, E. M. (1969). Assessment of older people: Self-maintaining and instrumental activities of daily living. The Geron tologist, 9, 179-186. doi: 10.1093/geront/9.3_Part_l. 179 Levine, B., Stuss, D. T., Winocur, G., Binns, M. A., Fahy, L., Mandic, M., . . . Robertson, I. H. (2007). Cognitive rehabilitation in the elderly: Effects on strategic behavior in relation to goal management. Journal of the International Neuropsychological Society: JINS, 13, 143—152. doi: 10.1017/S1355617707070178 Li, S.-C., Schmiedek, F., Huxhold, O., Rocke, C., Smith, J., & Lindenberger, U. (2008). Working memory plasticity in old age: Practice gain, transfer, and maintenance. Psychology and Aging, 23, 731-742. doi: 10.1037/a0014343
Marklund, P., Fransson, P., Cabeza, R„ Petersson, K. M., Ingvar, M., & Nyberg, L. (2007). Sustained and transient neural modulations in pre frontal cortex related to declarative long-term memory, working mem ory, and attention. Cortex: A Journal Devoted to the Study o f the Nervous System and Behavior, 43, 22-37. McKhann, G., Drachman, D., Folstein, M., Katzman, R., Price, D., & Stadlan, E. M. (1984). Clinical diagnosis of Alzheimer’s disease: Report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer’s Disease. Neurology, 34, 939-944. doi:10.1212AVNL.34.7.939 Nee, D. E., & Jonides, J. (2011). Dissociable contributions of prefrontal cortex and the hippocampus to short-term memory: Evidence for a 3-state model of memory. Neuroimage, 54, 1540-1548. doi:10.1016/j .neuroimage.2010.09.002 Neely, A. S., & Backman, L. (1993). Long-term maintenance of gains from memory training in older adults: Two 3 1/2-year follow-up studies. Journal o f Gerontology, 48, P233-P237. doi:10.1093/geronj/48.5.P233 Neely, A. S., & Backman, L. (1995). Effects of multifactorial memory training in old age: Generalizability across tasks and individuals. The Journals o f Gerontology Series B; Psychological Sciences and Social Sciences, 50, P134-P140. doi:10.1093/geronb/50B.3.P134 Noice, H., & Noice, T. (2009). An arts intervention for older adults living in subsidized retirement homes. Neuropsychology, Development, and Cognition Section B. Aging, Neuropsychology and Cognition, 16, 5 6 79. doi: 10.1080/13825580802233400 Optale, G., Urgesi, C., Busato, V., Marin, S., Piron, L., Priftis, K .,. . . Bordin, A. (2010). Controlling memory impairment in elderly adults using virtual reality memory training: A randomized controlled pilot study. Neurorehabilitation and Neural Repair, 24, 348-357. doi: 10.1177/1545968309353328 Petersen, R. C., Smith, G. E„ Waring, S. C„ Ivnik, R. J., Tangalos, E. G„ & Kokmen, E. (1999). Mild cognitive impairment: Clinical character ization and outcome. Archives o f Neurology, 56, 303-308. doi: 10.1001/ archneur.56.3.303 Rankin, J. L., Karol, R., & Tuten, C. (1984). Strategy use, recall, and recall organization in young, middle-aged, and elderly adults. Experimental Aging Research, 10, 193-196. doi:10.1080/03610738408258463 Rasmusson, D. X., Rebok, G. W., Bylsma, F. W., & Brandt, J. (1999). Effects of three types of memory training in normal elderly. Aging, Neuropsychology, and Cognition, 6, 56-66. doi: 10.1076/anec.6.1.56 .790 Rebok, G. W., & Balcerak, L. J. (1989). Memory self-efficacy and per formance differences in young and old adults: Effects of mnemonic training. Developmental Psychology, 25, 714-721. doi: 10.1037/00121649.25.5.714 Reuter-Lorenz, P. A., & Capped, K. (2008). Neurocognitive aging and the compensation hypothesis. Current Directions in Psychological Science, 17, 177-182. doi: 10. I l l 1/j. 1467-8721.2008.00570.x Rosenberg, M. (1965). Society and the adolescent self-image. Princeton, NJ: Princeton University Press. Salthouse, T. A. (1996). The processing-speed theory of adult age differ ences in cognition. Psychological Review, 103, 403-428. doi: 10.1037/ 0033-295X. 103.3.403 Schacter, D. L., Rich, S. A., & Stampp, M. S. (1985). Remediation of memory disorders: Experimental evaluation of the spaced-retrieval tech nique. Journal o f Clinical and Experimental Neuropsychology, 7, 7 9 96. doi: 10.1080/01688638508401243 Schmiedek, F., Lovden, M., & Lindenberger, U. (2010). Hundred days of cognitive training enhance broad cognitive abilities in adulthood: Find ings from the COGITO Study. Frontiers in Aging Neuroscience, 2, 1-10. doi: 10.3389/fnagi.2010.00027 Signoret, J. L. (1991). Batterie d ’efficience mnesique BEM 144. Paris, France: Editions Scientifiques Elsevier.
BENEFITS OF MEMORY-ATTENTION TRAINING IN ELDERLY Stigsdotter, A., & Backman, L. (1989). Multifactorial memory training with older adults: How to foster maintenance of improved performance. Gerontology, 35, 260-267. doi:10.1159/000213035 Stigsdotter Neely, A. (2000). Multifactorial memory training in normal aging: In search of memory improvement beyond the ordinary. In D. R. Hill, L. Backman, & A. Stigsdotter-Neely (Eds.), Cognitive rehabilita tion in old age (pp. 63-80). New York, NY: Oxford University Press. Stigsdotter Neely, A. S., & Backman, L. (1993). Maintenance of gains fol lowing multifactorial and unifactorial memory training in adulthood. Edu cational Gerontology, 19, 105-117. doi:10.1080/0360127930190202 Sturm, W., Willmes, K., Orgass, B., & Hartje, W. (1997). Do specific attention deficits need specific training? Neuropsychological Rehabili tation, 7, 81-103. doi: 10.1080/713755526 Tranter, L. J., & Koutstaal, W. (2008). Age and flexible thinking: An exper imental demonstration of the beneficial effects of increased cognitively stimulating activity on fluid intelligence in healthy older adults. Neuropsy chology, Development, and Cognition Section B, Aging, Neuropsychology and Cognition, 15, 184-207. doi:10.1080/13825580701322163 Valentijn, S. A. M., Hill, R. D., Van Hooren, S. A. H., Bosma, H., Van Boxtel, M. P. J., Jolles, J„ & Ponds, R. W. H. M. (2006). Memory self-efficacy predicts memory performance: Results from a 6-year follow-up study. Psychology and Aging, 21, 165-172. doi:10.1037/ 0882-7974.21.2.165 Valentijn, S. A. M., van Hooren, S. A. H., Bosma, H., Touw, D. M., Jolles, J., van Boxtel, M. P. J., & Ponds, R. W. H. M. (2005). The effect of two types of memory training on subjective and objective memory perfor mance in healthy individuals aged 55 years and older: A randomized controlled trial. Patient Education and Counseling, 57, 106-114. doi: 10.1016/j.pec.2004.05.002
743
Van der Linden, M., Coyette, F., Poitrenaud, J., Kalafat, M., Calacis, F., Wyns, C., & Adam, S. (2004). The 16-items free recall/cued recall test (RL/RI 16). In M. Van der Linden, S. Adam, A. Agniel, C. BaissetMouly, F. Bardet, F. Coyette, . . . C. Thomas-Anterion (Eds.), L'evaluation des troubles de la memoire: Presentation de quatre tests de memoire episodique (avec leur etalonnage). Marseille, France: Solal. van Zomeren, A. H., & Brouwer, W. H. (1994). Clinical neuropsychology o f attention. New York, NY: Oxford University Press. Verhaeghen, P., & Marcoen, A. (1996). On the mechanisms of plasticity in young and older adults after instruction in the method of loci: Evidence for an amplification model. Psychology and Aging, 11, 164-178. doi: 10.1037/0882-7974.11.1.164 Yesavage, J. A., Brink, T. L., Rose, T. L., Lum, O., Huang, V., Adey, M., & Leirer, V. O. (1982-1983). Development and validation of a geriatric depression screening scale: A preliminary report. Journal o f Psychiatric Research, 17, 37-49. doi:10.1016/0022-3956(82)90033-4 Yesavage, J. A., & Rose, T. L. (1984a). Semantic elaboration and the method of loci: A new trip for older learners. Experimental Aging Research, 10, 155-159. doi: 10.1080/03610738408258560 Yesavage, J. A., & Rose, T. L. (1984b). The effects of a face-name mnemonic in young, middle-aged, and elderly adults. Experimental Aging Research, 10, 55-57. doi:10.1080/03610738408258543 Yonelinas, A. P. (2002). The nature of recollection and familiarity: A review of 30 years of research. Journal o f Memory and Language, 46, 441-517. doi: 10.1006/jmla.2002.2864
Received December 2, 2013 Revision received May 28, 2014 Accepted June 5, 2014 ■
Copyright of Psychology & Aging is the property of American Psychological Association and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.
