The authors have declared that no competing interests exist.
Conceived and designed the experiments: MH MU MJ. Performed the experiments: MH. Analyzed the data: MH JP PA. Wrote the paper: MH JP MU.
Developmental dyslexia (DD) has previously been associated with a number of cognitive deficits. Little attention has been directed to cognitive functions that remain intact in the disorder, though the investigation and identification of such strengths might be useful for developing new, and improving current, therapeutical interventions. In this study, an old/new recognition memory paradigm was used to examine previously untested aspects of declarative memory in children with DD and typically developing control children. The DD group was not only not impaired at the task, but actually showed superior recognition memory, as compared to the control children. These findings complement previous reports of enhanced cognition in other domains (e.g., visuo-spatial processing) in DD. Possible underlying mechanisms for the observed DD advantage in declarative memory, and the possibility of compensation by this system for reading deficits in dyslexia, are discussed.
Developmental dyslexia (DD) is characterized by unexpected difficulties with reading, in the context of typical educational opportunities and intact intellectual and sensory abilities
Although much attention has been given to cognitive deficits associated with DD, it is evidently not the case that all cognitive functions are impaired in the disorder. Knowledge about what is well-functioning may be as important for increasing our understanding of the disorder as knowledge about what is impaired. The investigation and identification of cognitive strengths associated with DD could be used for developing new, and improving current, therapeutical interventions. In this study, we examine a previously untested aspect of declarative memory in children with DD, namely recognition memory after incidental encoding.
Declarative memory encompasses memory for factual knowledge (semantic memory) and personally experienced events (episodic memory)
Few studies have directly tested declarative memory functions in DD, and those that have done so have yielded inconsistent findings. Whereas some studies have reported that declarative memory is normal in the disorder
Another factor that appears to affect the performance of dyslexic participants in tasks probing declarative memory is the extent to which test performance depends on the use of intentional encoding strategies. In line with previous evidence suggesting problems with executive functions in DD
Declarative memory is a complex phenomenon that depends on the integrity of several underlying functions. Accordingly, a research program aimed at elucidating the status of declarative memory in DD may benefit from a systematic investigation of these underlying functions. One aspect of declarative memory that still remains untested in DD is recognition memory after incidental encoding. Crucially, in this paradigm, subjects are unaware of the subsequent memory test, and incidental encoding is promoted by, for example, a semantic categorization task. Thus, potential group differences in intentional encoding strategies should not be a confounding factor in this task. Moreover, this paradigm does not rely on free recall of information but rather on the identification of a specific item as “old/seen before” or “new/not seen before”. These characteristics may make this paradigm particularly suitable for revealing aspects of declarative memory that might function well in DD. Despite these advantages, this paradigm has not yet been used in DD. The present study was designed to fill this gap in the literature.
The study was approved by the ethical review board in the city of Uppsala. All parents or guardians provided informed written consent; children provided informed written assent and received a cinema ticket for their participation.
Twelve children with developmental dyslexia (DD) and 17 typically developing (TD) control children participated in the study. The two groups did not differ in sex, age and handedness (see
Demographics | DD | TD | ||
N | 11 | 17 | – | – |
Age in years | 11.0 (0.71) | 11.0 (0.49) | 0.28 | .78 |
Sex (f/m) | 5/6 | 5/12 | .39 | |
Handedness | 85.1 (16.4) | 92.2 (10.2) | 1.4 | .17 |
Cognitive scores | ||||
PIQ | 87.3 (12.5) | 97.1 (15.0) | 1.8 | .085 |
Phonological decoding | 1.82 (0.87) | 5.24 (1.15) | 8.4 | <.0001 |
Orthographic reading | 2.0 (1.18) | 5.76 (1.15) | 8.4 | <.0001 |
Nonword repetition | 106 (5.3) | 111 (5.4) | 2.4 | .026 |
TROG | 17.9 (1.20) | 18.9 (0.70) | 2.7 | .012 |
PPVT | 150 (15.9) | 160 (13.5) | 1.8 | .089 |
DD = Children with developmental dyslexia, TD = Typically developing control children, PIQ = Performance IQ; TROG = Test for reception of grammar; PPVT = Peabody picture vocabulary test. Standard deviations are shown in parentheses.
Children with DD were recruited via speech-language pathology clinics in the cities of Stockholm, Uppsala, Gävle and Västerås, in Sweden. All children with DD had been independently tested and diagnosed with dyslexia by a certified speech-language pathologist within 1.5 years prior to participation in the study. The TD group consisted of a subset of children who were recruited from schools in and around the cities of Stockholm and Uppsala as part of a larger study on memory and language in typically developing children. All children in the study were reported by their parents to be monolingual Swedish-speaking, to have normal (or corrected to normal) vision and hearing, and to have no known cognitive or motor impairment, apart from reading problems in the DD group.
In order to confirm reading problems in the DD group, and the lack thereof in the TD group, two reading tests, assessing phonological decoding and orthographic reading, respectively, were administered on the same day as the declarative memory task. These tests were paper and pencil Swedish adaptations
All TD children had stanine scores ≥4 out of 9 on both reading tests (corresponding to performance at or above –0.75
In addition to these reading tests, all children were also tested on nonword repetition
Performance IQ (PIQ), which was assessed by Raven’s Standard Progressive Matrices Plus
One child in the DD group was excluded from statistical analyses because he was an outlier on the recognition memory test, with a mean d’ score of 0.19, which was equal to − 3
Declarative memory was tested with an object recognition memory task developed by the Brain and Language Lab at Georgetown University. Similar tasks have previously been shown to engage the network of brain structures underlying declarative memory, including medial temporal lobe and frontal structures, for both non-verbal and verbal stimuli
The object recognition task consists of three phases; i) incidental encoding, ii) recognition 10 minutes after encoding and iii) recognition 24 hours after encoding. The stimuli were black-and-white line drawings of real objects and made-up objects (
There were three different sets of objects used in this task: i) those presented in the encoding phase (as well as in subsequent phases), ii) those used as foils in the 10 minute recognition phase and iii) those used as foils in the 24 hour recognition phase. Each of these three sets of objects consisted of 32 real objects and 32 made-up objects.
Testing took place in a quiet room under normal classroom lighting conditions. The stimuli were presented on an LCD screen of a portable PC computer running Windows, using E-Prime version 1.2. (Psychology Software Tools). The physical size of the images was 13.7×10.3 centimeters, and the viewing distance was approximately 50 centimeters. Participants were instructed to place their left and right index fingers on the designated buttons on a serial response box (E-prime SRBox) that was placed in front of them, and to make a response by pressing one of these buttons. Preceding each stimulus, a crosshair appeared in the center of the screen for 1000 milliseconds (ms), followed by the item for 500 ms, also in the center of the screen. In cases where the participant responded before 500 ms, the item remained onscreen until the 500 ms finished, to equalize presentation duration across stimuli and subjects. After the item presentation, the crosshair reappeared on the screen until the subject responded, or up to 4500 ms. As soon as the subject made a response through the SRBox, a 200 ms advance tone sounded, followed by 800 ms of fixation. If instead the subject made no response within the 4500 ms response period, a 400 ms time-out tone sounded, followed by 600 ms of fixation. After this the 200 ms advance tone sounded followed by 800 ms of fixation. The next item then began with 1000 ms of fixation.
In the incidental
The incidental encoding phase was followed by a 10 minute break during which subjects were encouraged to stretch their legs or have a snack. Just before the subsequent
Responses were captured using E-prime version 1.2. Two versions (A and B) of the task, for which the response buttons for “real”/“made-up” and “yes”/“no” were reversed, were assigned to consecutive participants in each group. Testing took place in a quiet room in the child’s school or home over the two consecutive days. Each test session took about 70–90 minutes, including the administration of reading, language and performance IQ tests.
Reaction times (RTs) were calculated for correct responses only, and filtered by excluding responses faster than 300 milliseconds (ms) or greater than 4500 ms. Median RTs were used in order to avoid undue influence from outlier RTs. D-prime (d’ =
Potential group differences (DD vs. TD) in the incidental encoding task were tested with one-way ANCOVAs (with PIQ as a covariate), with either categorization accuracy (percent correct) for real vs. made-up, or reaction times of correct responses (RTs), as the dependent variable. The DD and TD groups did not differ significantly in accuracy, though the DD group showed somewhat better performance, a pattern that approached significance (DD
Potential group differences in recognition memory accuracy across the two recognition sessions (10 minutes and 24 hours) were examined with a 2 (group: DD vs TD)×2 (session: 10 minutes vs 24 hours) ANCOVA with d’ scores as the dependent variable. Because the DD group’s trend of better performance at distinguishing real and made-up objects in the incidental encoding task could potentially confound performance at recognition, semantic categorization performance during encoding was included along with PIQ as a covariate.
Analyses revealed that the DD group had better recognition memory, as compared to the TD group, across both recognition sessions (
Reaction times, by contrast, did not differ significantly between the two groups (mean RTs across both recognition sessions: DD
In order to rule out alternative explanations to the observed DD recognition memory advantage, a set of control analyses was performed, with the aim of investigating potentially confounding factors.
First, we asked if group differences in speed-accuracy tradeoff during the recognition memory task could explain the present findings. This question was addressed by partial correlation analyses (controlling for PIQ and encoding accuracy) of RT against d’ scores within each recognition session separately. These analyses revealed no evidence of speed-accuracy tradeoffs in either of the two sessions, across all children or within either of the two groups (10 minute recognition session: all children:
Second, because the two groups were somewhat unbalanced with respect to sex (
Third, the effects of PIQ were more carefully examined. First, we performed a correlation analysis between PIQ and semantic categorization performance (which was the second covariate in the main ANCOVA). This analysis revealed that there was no correlation between PIQ and semantic categorization, across groups or within groups (all
Finally, we followed up on these analyses by creating new DD and TD groups that were matched one-to-one on PIQ. These groups were created by including all DD children for which there was a TD child with an identical PIQ standard score. If there were more than one TD option for a particular DD child (this was the case for one DD child in our data set), we selected the one that would also balance the groups with respect to sex. There were 5 children (3 boys and 2 girls) in each group. All DD children had mean stanine reading scores ≤2 and all TD children had mean stanine reading scores ≥4. The PIQ range was 85–115. These groups were then compared with Mann-Whitney U tests on recognition memory d’ scores and reaction times. The results confirmed the pattern observed in the main analysis with a significant DD advantage at recognition memory accuracy (main effect of group across both sessions:
Next, the relationships between reading performance and recognition memory within the two groups were examined. We performed partial correlation analyses (controlling for PIQ and encoding accuracy) between the mean d’ score across both sessions and the combined standardized raw scores from the phonological decoding and orthographic reading tests. These analyses revealed a marginally significant association between recognition memory and reading performance in the DD group
Finally, to examine whether the two groups differed with respect to potential effects of object-type, we performed 2 (object-type: real vs made-up)×2 (group: DD vs TD) ANCOVAs (controlling for PIQ and encoding accuracy) for each of the two recognition sessions. The ANCOVA for the 10 minute session produced a marginally significant main effect of group (
In the 24 hour session, there was again a marginally significant main effect of group (
The aim of the present study was to investigate a previously untested aspect of declarative memory in children with DD, namely recognition memory after incidental encoding. Based on previous evidence indicating that declarative memory impairments in DD may be related to less efficient encoding strategies
Developmental dyslexia has previously been associated with a number of linguistic and non-linguistic deficits (see introduction). The present findings indicate that this condition may also entail an enhancement of certain cognitive functions. These findings complement previous reports suggesting enhancements in other aspects of cognition in DD, namely visuo-spatial processing
One explanation that has been proposed to account for enhanced visuo-spatial processing in DD
Alternatively, it may be the case that the superior performance in the DD group was not a result of an enhancement in this group, but rather the result of relatively impaired performance in the TD group. According to the neuronal recycling hypothesis
A third possible explanation for the present findings is that they reflect intricate interactions between the procedural and declarative memory systems. Converging evidence from human and animal studies suggest that the procedural and declarative memory systems rely on at least partly dissociable neural substrates and support different cognitive functions
A possible enhancement of aspects of declarative memory is particularly intriguing since evidence suggests that declarative memory may play an important compensatory role for the reading deficits in dyslexia. This phenomenon may reflect the cooperative aspect of the procedural-declarative relationship
If declarative memory indeed plays a compensatory role for reading in the present study, we would expect to find a correlation between performance at the recognition memory test and reading scores in the DD group, but not in the TD group. This prediction did not seem to be strictly supported, as the correlation between recognition memory d’ scores (across both sessions) and the combined standardized raw scores from the two reading tests did not reach significance. However, the lack of such an effect in the DD group may reflect a lack of power due to the small sample size. Indeed, the correlation approached significance in the DD group (
The present study has various limitations that may be addressed by future studies. First, samples sizes were relatively small. Thus, the present findings need to be replicated with larger samples in order to ensure their generalizability. In addition, the present study tests only one aspect of declarative memory, and leaves many other aspects unexplored. Future studies would benefit from contrasting the recognition memory paradigm used in the present study with paradigms assessing encoding strategies and recall. Such a within-subjects design would allow for a powerful examination of different aspects of declarative memory, and their status in DD.
Keeping these limitations in mind, the results of the present study are encouraging, as they point to possible cognitive strengths associated with an otherwise difficult and persisting condition. Crucially, knowledge about which aspects of cognition are intact, or even enhanced, in DD, should be of theoretical as well as of clinical and pedagogical interest.
We gratefully acknowledge the help of the many schools and families who participated in this study. We also wish to thank Åke Olofsson for helpful comments and advice.