Research in Developmental Disabilities 35 (2014) 1384–1392

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Research in Developmental Disabilities

Differential outcomes training improves face recognition memory in children and in adults with Down syndrome Laura Esteban a, Victoria Plaza b, Ginesa Lo´pez-Crespo c, Ana B. Vivas d, Angeles F. Este´vez a,* a

Universidad de Almerı´a, Spain Universidad Auto´noma de Chile, Chile Universidad de Zaragoza, Spain d Psychology Department, The University of Sheffield International Faculty, City College, Thessaloniki, Greece b c

A R T I C L E I N F O

A B S T R A C T

Article history: Received 12 December 2013 Received in revised form 14 March 2014 Accepted 14 March 2014 Available online 10 April 2014

Previous studies have demonstrated that the differential outcomes procedure (DOP), which involves paring a unique reward with a specific stimulus, enhances discriminative learning and memory performance in several populations. The present study aimed to further investigate whether this procedure would improve face recognition memory in 5and 7-year-old children (Experiment 1) and adults with Down syndrome (Experiment 2). In a delayed matching-to-sample task, participants had to select the previously shown face (sample stimulus) among six alternatives faces (comparison stimuli) in four different delays (1, 5, 10, or 15 s). Participants were tested in two conditions: differential, where each sample stimulus was paired with a specific outcome; and non-differential outcomes, where reinforcers were administered randomly. The results showed a significantly better face recognition in the differential outcomes condition relative to the non-differential in both experiments. Implications for memory training programs and future research are discussed. ß 2014 Elsevier Ltd. All rights reserved.

Keywords: Differential outcomes effect Facial recognition memory Children Down syndrome

The differential outcomes procedure (DOP) refers to the increase in performance and terminal accuracy seen in conditional discrimination tasks when each of the stimuli-response associations to be learned is followed by a unique outcome. The DOP was first described by Trapold (1970) using rats as experimental subjects. Trapold showed that rats were able to learn faster to discriminate between a tone and a click when each correct stimulus-response association was followed by a specific outcome (e.g., tone-right lever-sucrose vs. click-left lever-food pellets), as compared with a condition where the same reinforcer was administered for both S-R associations. Since this first demonstration, the ubiquity of the phenomenon has been demonstrated in a variety of species and procedures (see Goeters, Blakely, & Poling, 1992; Urcuioli, 2005, for a review). Some of the key findings with humans participants are enhanced learning of symbolic relations in children (e.g., Este´vez & Fuentes, 2003; Este´vez, Fuentes, Marı´-Beffa, Gonza´lez, & A´lvarez, 2001; Maki, Overmier, Delos, & Gutman, 1995), adults (Este´vez et al., 2007; Miller, Waugh, & Chambers, 2002; Mok & Overmier, 2007), adults with Prader–Willi syndrome (Joseph, Overmier, & Thompson, 1997) and children and adults with Down syndrome (Este´vez, Overmier, Fuentes, & Gonza´lez, 2003).

* Corresponding author at: Departamento de Psicologı´a, Universidad de Almerı´a, 04120 Almerı´a, Spain. Tel.: +34 950 21 46 26; fax: +34 950 21 43 83. E-mail address: [email protected] (A.F. Este´vez). http://dx.doi.org/10.1016/j.ridd.2014.03.031 0891-4222/ß 2014 Elsevier Ltd. All rights reserved.

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In addition to the benefits of the DOP observed with conditional discrimination learning, there is an increasing amount of evidence suggesting positive effects with memory tasks as well (see Lo´pez-Crespo & Este´vez, 2013, for a review). For instance, studies conducted on animals showed the potential of the DOP to alleviate short-term memory problems associated with aging or brain-damage. Concretely, the DOP has been found to improve memory performance of aged rats (Savage, Pitkin, & Careri, 1999) and pyrithiamine treated rats–an animal model of Wernicke–Korsakoff syndrome (Savage & Langlais, 1995). Similar results have been reported with humans. Hochhalter, Sweeney, Bakke, Holub, and Overmier (2000) employed a face Delayed Matching to Sample (DMTS) task in people with alcohol dementia. They reported improved memory performance in the differential outcomes condition, relative to the non-differential, in three of the participants. This finding has been replicated in larger samples of older adults (Lo´pez-Crespo, Plaza, Fuentes, & Este´vez, 2009), and people with Alzheimer’s disease (Plaza, Lo´pez-Crespo, Antu´nez, Fuentes, & Este´vez, 2012). Finally, two other studies have extended the finding of better performance in a delayed face recognition task with the DOP to a sample of young adults (Plaza, Este´vez, Lo´pez-Crespo, & Fuentes, 2011) and sleep-deprived adults with transient memory deficits (Martella, Plaza, Este´vez, Castillo, & Fuentes, 2012). All together, the results obtained in the aforementioned studies support the potential of the DOP to improve memory for faces in a variety of conditions. However, more research with other relevant populations, such as Down syndrome (DS), is needed before this technique may be implemented as an intervention/education tool in school and health care settings. DS results from anormalities of chromosome 21 (in particular Trisomy 21), and it is considered the most common genetic form of intellectual disability (McGrother & Marshall, 1990; Sherman, Allen, Bean, & Freeman, 2007). Among these intellectual disabilities, the study of the working memory capacities in DS has received an important amount of attention. Although, initially it was thought that visuospatial working memory was relatively spared in DS (e.g., Jarrold & Baddeley, 1997, 2001; Lanfranchi, Cornoldi, & Vianello, 2004; Laws, 2002; Marcell & Weeks, 1988; Wang & Bellugi, 1994), more recent studies suggest deficits in several aspects of visuospatial working memory in this population (e.g., Carreti, Lanfranchi, & Mammarella, 2013; Lanfranchi, Carretti, Spano`, & Cornoldi, 2009; Visu-Petra, Benga, Tincas, & Miclea, 2007). Specifically, task complexity seems to be a crucial factor. Thus, when participants with DS were shown a complex visual pattern in a DMTS (as part of the Cambridge Neuropsychological Test Automated Battery, CANTB), they performed worse than the control group matched on mental age (Visu-Petra et al., 2007). The evidence with face processing is also relatively scarce, and studies have mostly focused on emotional face processing. Studies have reported impaired recognition of neutral expressions (e.g., Hippolyte, Barisnikov, Van der Linden, & Detraux, 2009), anger, surprise and fear (e.g., Kasari, Freeman, & Hughes, 2001; Porter, Coltheart, & Langdon, 2007; Williams, Wishart, Pitcairn, & Willis, 2005; Wishart & Pitcairn, 2000). Overall, people with DS seem to show tendency toward positive evaluation of facial expressions (Kasari et al., 2001). Few researchers have investigated facial identity recognition in DS, and the results are not consistent. While some studies reported no significant differences between DS adults and control participants on a simultaneous face identity-matching task (e.g., Hippolyte, Barisnikov, & Van der Linden, 2008; Hippolyte et al., 2009); a more recent study (Ferna´ndez-Alcaraz, Rueda, Garcı´a-Andre´s, & Carvajal, 2010) showed worse performance on a face discrimination task in adults with DS as compared to a control group. In the present study we aimed at testing the efficacy of the DOP to improve delayed recognition of faces in typically developing children, and in a sample of adults with DS. Based on the findings of impaired delayed recognition of complex visual patterns (Visu-Petra et al., 2007) and impaired recognition of identities (e.g., Ferna´ndez-Alcaraz et al., 2010) or facial expressions (e.g., Hippolyte et al., 2009; Kasari et al., 2001; Porter et al., 2007; Williams et al., 2005), we hypothesized that people with DS would show worse performance in a face DMTS as compared to a mental-age matched control group. We also expected that the overall performance of both groups, children and DS, would be improved in the differential outcomes condition relative to the non-differential outcomes condition. 1. Experiment 1: DOP in typically developing children 1.1. Method 1.1.1. Participants Forty-six typically developing children (23 girls and 23 boys), ranging in age from 4 years and 2 months to 8 years and 11 months participated in the present study. They were assigned to two groups according to age: younger children (from 4 years and 2 months to 5 years and 11 months; N = 15, Meanage = 5.2 years, SD = 0.50) and older children (from 6 years and 3 months to 7 years and 11 months; N = 31, Meanage = 6.8 years, SD = 0.49). All of them were Hispanic, recruited from a public school (C.E.I.P. Lope de Vega) in Almerı´a (Spain), had Spanish as their mother-tongue and normal or corrected-to-normal vision. The study was approved by the University of Almeria’s Ethics Committee, and we obtained written informed consent from the parents and oral consent to participate from the children. 1.1.2. Stimuli and materials Each participant sat next to the experimenter in a quiet room. The stimuli consisted of 18 photographs of neutral male faces taken from a front perspective presented on a white background on a touch screen (12,100 TFT LCD WXGA monitor) located on a child-size table. Photographs were selected from Kristen Kennedy’ Normed Faces available at: http:// agingmind.utdallas.edu/facedb/view/normed-faces-by-kristen-kennedy (Kennedy, Hope, & Raz, 2009). They were grouped

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in two sets of nine photographs each that served as the sample and the comparison stimuli for the two versions of the recognition task. The photographs measured 5.5 cm  6.5 cm and were displayed either individually in the center of screen (sample stimulus), or grouped in a 3  2 grid (comparison stimuli) equidistant from the borders. The position of the photographs on the grid was randomly arranged. The E-prime program (Schneider, Eschman, & Zuccolotto, 2002) controlled the presentation of the stimuli as well as data collection. Children sat approximately 40 cm away from the computer screen so that they were close enough to make touch-screen responses. Primary and secondary reinforces served as outcomes. Three photographs of the primary reinforces (lollipops, candies and sweets) served as immediate secondary reinforces. They measured approximately 10 cm  13 cm and were presented individually, after a correct choice, at the center of the screen. Both, younger and older children rated all primary reinforcers as highly desirable. At the end of their participation all the children regardless of their performance received at least two hedonic outcomes along with verbal appraisal. The Spanish versions of the Peabody Picture Vocabulary Test-III (PPVT-III, Dunn & Dunn, 1997) and the Automated Working Memory Assessment (AWMA, Alloway, 2007) were administered to all participants prior to the experimental session. The PPVT-III is a test of receptive vocabulary that provides an estimate of children’ verbal intelligence; total score can be converted to a percentile rank, mental age or a standard deviation IQ score. The AWMA is a computerized battery to assess different aspect of working memory and has been standardized for use with typically developing children. We used the short form consisting of four tests (digit recall, dot matrix, listening recall, and spatial recall) that assesses verbal-short term memory, visuospatial short-term memory, verbal working memory, and visuospatial working memory, respectively. 1.2. Procedure 1.2.1. Pilot studies Because a within-subject designed was used in the study, two versions of a facial recognition memory task were designed by using two different sets of stimuli. To explore whether these two sets of faces had the same difficulty level and were equally discriminated, 10 children from the school C.E.I.P. Lope de Vega (Almerı´a, Spain; Meanage = 4.7 years, SD = 0.60) participated in this pilot study. Children were asked to perform a delayed face recognition task within a single experimental session that consisted of two blocks of 12 trials each. Each block included faces from one of the two stimuli set (young adults – version A- vs. older adults – version B-). Half of the children had to respond first to the young set of faces – version A- and then to the old set – version B-; the other half did the opposite. Correct responses were not followed by any outcome. The analysis showed no significant difference between the two blocks when percentage of correct responses were analyzed (87% vs. 72%; Fs < 1). However, the overall results with the accuracy data suggested that the task was too easy for this population, and previous studies have shown no improvement in performance with the DOP when overall accuracy approaches ceiling effects (e.g., Este´vez et al., 2001, 2007; Plaza et al., 2011). Consequently, we increased the difficulty of the task by presenting six comparison face stimuli instead of four. A further pilot study with eight naı¨ve children from the same school (Meanage = 5.2 years, SD = 1.75) showed that this manipulation was effective in increasing task difficulty. Also, there were no differences between the two stimuli sets (45% vs. 38%; Fs < 1).

Table 1 Demographic variables and mean scores obtained on the Peabody Picture Vocabulary Test (PPVT-III) and the Automated Working Memory Assessment (AWMA) by participants in both experiments (standard deviations in parenthesis). Results of the comparison between the groups (Student’s t) for Experiment 2 are also presented. Experiment 1

n Sex (F/M) Age (years) PPVT-III Mental age Raw score AWMAa STM_V WM_V_R WM_V_P STM_VS WM_VS_R WM_VS_P

Experiment 2

Younger children

Older children

DS group

TD group

t

p

15 9/6 5.2 (0.50)

31 14/17 7.1 (0.46)

7 3/4 40.9 (4.16)

7 4/3 5.5 (1.14)

21.71

0.00

7.5 (1.33) 59.3 (11.82)

9.7 (1.77) 72.8 (11.06)

5.2 (1.32) 41.3 (11.2)

5.5 (1.38) 43(11.98)

0.38 0.28

0.71 0.79

91.87 (10.62) 127.33 (9.48) 117.73 (10.19) 113.07 (13.43) 122.46 (20.05) 123.6 (22.44)

86.03 (11.09) 112.19 (16.76) 99.84 (12.76) 103.19 (11.59) 104.35 (14.15) 101.61 (14.12)

10.87 (3.85) 0.43 (0.79) 2.86 (1.07) 9.43 (4.54) 3.86 (2.91) 4.29 (3.64)

14.57 (4.58) 11 (4.12) 13.14 (4.22) 15.57 (4.72) 6.86 (5.24) 11.86 (11.99)

1.64 6.66 6.25 2.48 1.32 1.60

0.13 0.00 0.00 0.03 0.21 0.14

Note. STM_V, Short Term Memory-Verbal (digit recall test); WM_V_R, Working Memory-Verbal Recall (listening recall test); WM_V_P, Working MemoryVerbal Processing (listening recall test); STM_VS, Short Term Memory-Visuospatial (dot matrix test); WM_VS_R, Working Memory-Visuospatial Recall (spatial recall test); WM_VS_P, Working Memory-Visuospatial Processing (spatial recall test); DS, Down syndrome; TD, typically developing. a Raw scores are presented for Experiment 2.

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Fig. 1. Stimuli sequence (from left to right) used in Experiments 1 and 2.

1.2.2. Experimental study Participants were tested individually in a quiet room free from distraction at their school. In the first session, the PPVT-III and the AWMA was administered in order to determine children’s mental age and working memory skills. As it can be observed in Table 1, all participants had AWMA standard scores within the average to high range as well as a mental age equal to, or higher than, their chronological age. Two experimental sessions (DO and NDO) of approximately 20 min each, followed this assessment phase. The order of the outcome session was counterbalanced across participants. We also orthogonally combined the two stimuli sets with the two outcomes conditions to avoid any potential bias. To avoid fatigue effect there was a week interval between the two experimental sessions. The task began with a practice block of three practice trials to ensure that participants fully understood the instructions. The trial sequence (see Fig. 1) started with a central fixation point (a cross) presented for 1000 ms. The cross was replaced by a blank screen for 500 ms and then a photograph of a face (the sample stimulus) appeared on the center of the screen for 1000 ms. After a delay of 1, 5, 10 or 15 s, a set of six faces was presented (the comparison stimuli). Children had to touch on the screen the previously presented face. Correct responses were followed by a secondary reinforce for 2500 ms. When the response was incorrect, there was a blank screen for 2500 ms. Seventy-two facial recognition-training trials grouped into three blocks of 24 trials each, followed the practice phase. Each of the three target faces was presented 24 times as a sample stimulus and 54 times as a comparison stimulus. There were six faces that were presented only as distractors. In all trials, two target faces (one presented also as the sample stimulus) and four distractors served as the choice or comparison stimuli. In the differential outcomes condition, each sample stimulus was always associated with a specific outcome. Finally, in the non-differential condition, the three outcomes were randomly presented after correct responses. 1.2.3. Statistical analyses Normality of data, using Kolmogorov–Smirnov tests, and homogeneity of variance, using Leven’s tests were tested. Results indicated that normality values were in acceptable ranges and all variables have homogeneity of variance. Mauchly’s test of sphericity indicated also that the assumption of sphericity was not violated. The assumptions to perform ANOVAs were thus satisfied. Percentages of correct responses were submitted to a 2  2  4 mixed ANOVA with Age (young and older children) as the between-subject factor, and Outcomes (differential vs. non-differential) and Delay (1, 5, 10 and 15 s) as the within-subject factors. Bonferroni post hoc test was used for post hoc comparisons when appropriate. The significance level was set at p  .05.

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% Correct Responses

5 year-old-group

7 year-old-group

90 80 70 60

DIF NODIF

50 40 1

5

10

15

1

5

10

15

Delay (s) Fig. 2. Mean percentage of correct responses as a function of group (younger vs. older), delay (1, 5, 10, and 15 s), and outcomes (differential and nondifferential) in Experiment 1. Error bars represent the standard error of the mean.

1.3. Results The analysis conducted on percent of correct responses showed significant main effects of Age [F(1, 44) = 15.95, p < .001,

h2p ¼ :266], and Delay [F(3, 132) = 9.39, p < .001, h2p ¼ :176]. Older children performed the task better than younger children (79% vs. 65% accuracy, respectively) and accuracy decreased as the delay interval increased (see Fig. 2). That is, participants overall were less good at recognizing the previously presented face with increasing delays. Pair-wise comparisons showed significant differences between the 15 (68%) and the 1 (76%) and 10 (73%) delays conditions, p < .05. Results also revealed a significant main effect of Outcomes [F(1, 44) = 13.46, p < .01, h2p ¼ :234] indicating that children showed a better delayed face recognition when differential outcomes were arranged (75% vs. 70% accuracy for the differential and non-differential outcomes conditions, respectively). No other effects, nor their interaction, reached statistical significance (p > .05). 1.4. Discussion This first experiment was designed to explore the potential of the DOP to improve delayed face recognition memory in 5and 7-year-old typically developing children. To the best of our knowledge, this is the first study to report better face recognition performance in children who received differential outcomes after their correct responses relative to a nondifferential outcomes condition. The present findings add to those obtained in patients with alcohol-related amnesia (Hochhalter et al., 2000), people with Alzheimer’s disease (Plaza et al., 2012) and senior and young adults (Lo´pez-Crespo et al., 2009; Martella et al., 2012; Plaza et al., 2011).

2. Experiment 2. The DOP in people with DS 2.1. Method 2.1.1. Participants Seven adults with DS (from 36 years and 4 months to 46 years; Meanage = 40.9 years, SD = 4.16) and seven typically developing children (TD) who were matched in mental age to the DS group (from 4 years and 6 months to 7 years and 4 months; Meanage = 5.5 years, SD = 1.14) participated in this study. DS participants were recruited from the Non Governmental Organization San Jose´ (Granada, Spain). The TD participants were contacted in the C.E.I.P. Lope de Vega, a local school in Almerı´a (Spain). Demographic characteristics, cognitive functioning scores and statistical differences between the two groups are presented in Table 1. All participants in the TD and DS groups were matched on one to one basis for their verbal mental age estimated with a task of receptive vocabulary (PPVT-III). A child was included in the TD control group when his raw score on the PPVT-III lied within (in either direction) 4 points of the score of the corresponding DS child. Exclusion criteria were sensory, psychiatric, or physical disabilities, and clinical symptoms of dementia. The participants’ native language was Spanish, and they all were Hispanic and had normal or corrected-to-normal vision. The study was approved by ethics committee of the University of Almerı´a, and written informed consent was obtained from the parents or caregivers. In addition, participants gave their oral consent to take part in the study, and were free to withdraw from the procedure at any time. 2.1.2. Procedure The stimuli, materials and procedure were the same as those of Experiment 1 except that the delayed face recognition task was shortened. Thus, 48 facial recognition-training trials instead of 72 were used. Trials were grouped into two blocks of 24 trials each.

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% Correct Responses

DS group

1389

TD group

90

DIF NODIF

80 70 60 50 40 0

1

5

10

15

1

5

10

15

Delay (s) Fig. 3. Mean percentage of correct responses as a function of group (younger vs. older), delay (1, 5, 10, and 15 s), and outcomes (differential and nondifferential) in Experiment 2. Error bars represent the standard error of the mean.

2.2. Results The PPVT-III and the AWMA scores are presented in Table 1. Participants in the control group showed a mental age equal to, or higher than, their chronological age. As expected, DS participants had a mental age below their chronological age. Raw scores were used in order to compare AWMA results of both groups. There were statistically significant differences between the DS and the TD groups in the visuospatial short-term memory and verbal working memory tests (see Table 1). Face recognition accuracy data (see Fig. 3) were submitted to a mixed ANOVA with Outcomes and Delay as the withinsubject factors and Group as the between-subject factor. As in the previous experiment, results showed a significant main effect of Outcomes [F(1, 12) = 24.94, p < .001, h2p ¼ :675] and Delay [F(3, 36) = 9.64, p < .001, h2p ¼ :445]. Participants were more accurate in the 1 s delay than in the other three delays (80%, 67%, 69% and 61% accuracy in 1, 5, 10 and 15 s) as well as when specific outcomes were arranged (75% vs. 63% accuracy for the differential and non-differential outcomes conditions, respectively). No other effects, nor their interaction, reached statistical significance (Fs < 1). To explore whether the effect of using differential outcomes would be modulated by memory processes, Pearson’s correlations with differential outcomes scores (% accuracy differential outcomes condition minus % accuracy nondifferential outcomes) and the six AWMA scores (calculated from the digit recall, the listening recall, the dot matrix and the spatial recall tests) were performed. Due to the multiple correlations we adopted a stricter level of significance, p < .008 (Bonferroni corrected). We found a significant negative correlation between the differential outcomes scores and the visuospatial short-term memory (from the dot matrix test; r = .739, p = .003). 2.3. Discussion The results obtained in the present experiment are the first to demonstrate that the delayed face recognition memory of people with DS is improved when differential outcomes are arranged, as compared to non-differential outcomes. As in Experiment 1, this effect was also observed in 5-year-old children (the control group). Furthermore, the DS group showed worse performance, than the control group, in the visuospatial short-term memory and verbal working memory tests from the AWMA. This result fits well with the deficit in verbal working memory reported previously in people with DS (e.g., Jarrold & Baddeley, 1997, 2001; Lanfranchi et al., 2004; Laws, 2002) and suggests, in addition, deficits in visuospatial short-term memory. Finally, there was a significant negative correlation between the magnitude of the differential outcomes effect and performance in the visuospatial short-term memory test. That is, the lower the performance in the visuospatial short-term memory test the greater the magnitude of the DOE. This result suggests that people with deficits in short-term memory may benefit more from the DOP.

3. General discussion The effectiveness of the DOP to improve working memory has received considerable support from basic research with animals (e.g., Demarse & Urcuioli, 1994; Savage et al., 1999). However, there is limited evidence with humans. Studies so far have shown better delayed face recognition memory with the DOP in people with alcohol-related amnesia and Alzheimer’s disease, sleep-deprived adults, and older adults (Hochhalter et al., 2000; Lo´pez-Crespo et al., 2009; Martella et al., 2012; Plaza et al., 2011). The present study extended these findings to typically developing children (Experiment 1) and people with DS (Experiment 2). Although the overall performance in the delayed recognition task did not significantly differ between the DS and control groups, the DS group scored significantly lower, than the control group, on the visuospatial short-term memory test. The stronger spatial component in visuospatial short-term test relative to the face delayed recognition task, may account for this

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disagreement. That is, in the former participants had to remember the order sequence of a dot in 4  4 matrix. This points out to a specific deficit in spatial processing in DS, although further research is needed to clarify under what circumstances we may observe deficits in visuosaptial short-term memory in people with DS. Regardless of this, the DOP was effective in improving the overall performance of both groups. In addition, the significant negative correlation between performance on the visuospatial short-term memory test and the magnitude of the DOE supports that the poorer the visuospatial short-term memory capabilities, the higher the benefit of using specific outcomes. Our results suggest that the DOP may be an effective tool in the school context. There is now substantial evidence supporting the crucial role of short-term/working memory in the development of language and in the overall capacity of children to learn (Alloway, Gathercole, Willis, & Adams, 2004; Dollaghan, Campbell, Needleman, & Dunlosky, 1997; Weismer et al., 2000). Actually, working memory capacity seem to be a strong predictor of children’s academic achievements (e.g., Alloway, Gathercole, Adams, Willis, Eaglen, & Lamont, 2005; Alloway, Banner, & Smith, 2010; Gathercole & Pickering, 2000; Gathercole, Pickering, Knight, & Stegmann, 2004; Jarvis & Gathercole, 2003). The DOP could be an easy-to-implement-inclass technique to improve short-term/working memory of children, in particular of children with developmental disabilities such as DS. There are a few studies showing a positive effect of memory training interventions in children with DS. For instance, Bennett, Holmes, and Buckley (2013) reported improved performance on trained and non-trained visuospatial short-term memory tasks in a group of children with DS, after training with a computerized visuospatial memory program. The results were maintained when children were tested four months later. Similarly, Conners, Rosenquist, Arnett, Moore, and Hume (2008) reported an improvement in the auditory verbal memory span of children with DS after rehearsal training. We propose that the DOP could be used in combination with other training techniques, or in isolation, in school settings to improve memory in children. Further research is needed to answer some outstanding questions: Are there spill over effects to other memory processes (e.g., verbal short-term memory) or everyday tasks with DOP training? How much training is needed to observe sustained positive effects over a long period of time? Another outstanding question is what is the mechanism underlying the effect of using specific outcomes on discriminative learning and memory. The two-memory systems model has received the most empirical support (e.g., Overmier, Savage, & Sweeney, 1999; Ramirez, Buzzetti, & Savage, 2005; Savage, 2001; Savage & Parsons, 1997). According to this theory, unique reward expectancies are produced with the DOP via classical conditioning; that is, an association between the to-be-remembered stimulus and the specific outcome is formed. They also propose that the prospective memory of the upcoming reward would guide the retrieval or/and response selection mechanisms via the implicit memory system. Under the non-differential condition, there is no prospective information to guide the retrieval/response processes, which are guided only by the retrospective memory of the sample stimulus via the explicit memory system. This dissociation is supported by activation of distinct brain regions under differential and non-differential conditions (for a review on animal literature, see Savage & Ramos, 2009; see also Mok, Thomas, Lungu, & Overmier, 2009 for a fMRI study with humans). Thus, the DOP may be particularly effective in populations with deficit on explicit memory, since learning with the DOP would utilize the intact implicit memory system. This hypothesis has been further supported by studies with elderly people and with people suffering from Alzheimer’s Disease, which are characterized by a deficit in explicit memory (Lo´pez-Crespo et al., 2009; Plaza et al., 2012). We believe that the same hypothesis can be put forward to explain the improved performance in the DMTS found with the DS group in our study. That is, studies have consistently reported a pattern of impaired explicit memory but spared implicit memory in people with DS (Carlesimo, Marotta, & Vicari, 1997; Jarrold, Baddeley, & Phillips, 2007; Vicari, 2001; Vicari, Bellucci, & Carlesimo, 2000). In sum, the present results demonstrate that face recognition memory of both typically developing children and adults with DS is improved by a non-invasive technique, which associate specific outcomes to each memory stimulus. This finding has important implications for educators and health professionals, since the DOP could be an easy-to-implement tool to enhance short-term/working memory in typically developing children and people with memory impairments or learning disabilities such as people with DS. Conflicts of interest The authors report no conflicts of interest. Acknowledgements This research was supported by grants PSI2009-09261 and PSI2012-39228 from Spanish Ministerio de Ciencia e Innovacio´n and from Spanish Ministerio de Economı´a y Competitividad, respectively. We thank the staff of the C.E.I.P. Lope de Vega and the Non Governmental Organization San Jose´ for their contribution and help throughout the course of this study. We also thank the parents of children and the caregiver of the participants with Down syndrome that kindly accepted them to participate in the study. References Alloway, T. P. (2007). Automated Working Memory Assessment. London, UK: Harcourt Assessment. Alloway, T. P., Gathercole, S. E., Willis, C. S., & Adams, A. M. (2004). A structural analysis of working memory and related cognitive skills in young children. Journal of Experimental Child Psychology, 87, 85–170.

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