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Talk;memory

Thursday stream 3 Session 14.00 - 15.40 Length 25 minutes

Patterns of long-term memory deficit in a learning disorders clinic cohort

Wayne Levick

John Hunter Children's Hospital, NSW, 2310, Australia pswrl@alinga.newcastle.edu.au

Abstract

A deficit in the ability to store new verbal and/or non-verbal information in long-term memory (LTM) is the main feature of the amnesic syndrome described in adults and children with medial temporal and diencephalic dysfunction. In recent years a number of cases have been reported suggesting that children and adults of average IQ and without apparent acquired brain damage can display varying degrees of deficit in the ability to store new information in LTM. The deficit typically shows up on testing as poor initial learning and/or delayed recall. This study examined the incidence of various patterns of LTM deficit and the relationship of these deficits to literacy skill development in a group of 260 children referred for assessment of specific learning difficulties. Each child was administered a selection of subtests of the WRAML in addition to IQ, reading, spelling and other measures. Performance on the learning trials and at delayed recall on the WRAML Verbal and Visual Learning subtests was examined. Several patterns of long-term memory deficit emerged. Significant patterns included a global deficit, a verbal-specific deficit, and a verbal retrieval deficit. The contribution of a range of potentially related variables including IQ, immediate memory, phonological processing and confrontation naming is addressed. Theoretical and clinical implications of these findings are considered.

INTRODUCTION

The process of learning to read at the word recognition level is essentially an associative learning task in which verbal labels are associated with symbols and meaning according to various rules, a process which could be presumed to involve long-term memory (LTM). Models of reading tend to focus on the process of reading rather than the establishment of the process and generally have little to say about the role of LTM. The dual route cascaded model, for example, readily accounts for acquired deficits in reading in individuals who have a well-established reading process but, as Coltheart, Rastle, Perry, & Langdon (2001) concede, "it has nothing to say about the actual process of learning to read".

The reading system architecture includes various modules in which reside knowledge such as a grapheme-phoneme rule system, word meanings, words recognised as whole units, and phonological representations of words (Coltheart et al, 2001). It seems reasonable to suppose that the contents of these modules accumulate through a combination of explicit and implicit learning processes. It is the involvement of explicit memory, specifically the episodic/declarative aspect of explicit memory, that this paper aims to explore. It may be that some aspects of reading are initially acquired via episodic learning and that as this material is rehearsed and applied in reading it gradually loses it episodic characteristics and is established in semantic memory (Patterson & Hodges, 1995). Alternatively, there may be a dissociation in declarative memory such that new semantic memory can be stored independently of episodic memory (Vargha-Khadem, Gadian, Watkins, Connelly, Van Paesschen, & Mishkin, 1997).

It is well established that short-term memory, specifically phonological working memory, is intimately involved in the development of and the process of phonological decoding. Typically developmental phonological dyslexics have inordinate difficulty with auditory-verbal serial recall tasks such as digit span. There is evidence from relatively small group studies to suggest that children with specific learning disorders (SLD) such as dyslexia have problems at the encoding stage of LTM but that once material is entered into memory it tends not to be lost abnormally rapidly (Lorsbach, 1982; Kramer, Knee, & Delis, 1999).

The reading process, once established, is quite resilient in the face of circumscribed, severe impairment of long-term memory in the form of the amnesic syndrome. The effect of LTM impairment in childhood when the reading process is in development is less clear. Cases have been reported in which the onset of LTM impairment in the form of an amnesic syndrome is presumed to have been at birth (Vargha-Khadem et al, 1997; (Gadian, Aicardi, Watkins, Porter, Mishkin, & Vargha-Khadem, 2000), in the pre-school years (Vargha-Khadem et al, 1997) or at an age when the reading process has undergone significant development (Ostergaard, 1987; Wood, Brown & Felton, 1989; Vargha-Khadem et al, 1997; Broman, Rose, Hotson, & Casey, 1997; Benedict, Shapiro, Duffner & Jaeger, 1998). Evidence from these relatively few cases suggests that reading may continue to develop following the onset of an amnesic syndrome in childhood though the level of learning may be affected. There does not appear to be a relationship between age of onset and the extent to which reading develops though the number of cases is too small to be considered conclusive. Furthermore, the incidence of brain damage in addition to that in memory centres complicates the picture.

This paper examines the status of long-term memory in a large, clinic-referred cohort of children with SLD including the nature and incidence of subtypes of long-term memory deficit and the relationship of these deficits to the development of reading.

METHOD

Data for analysis was derived from the records of 300 children (242 males; 58 females) seen for assessment in a health service based learning disorders clinic. To be eligible for referral children must have a Verbal or Performance IQ of at least 85 and evidence of a specific difficulty in development of literacy and/or numeracy skills. See Table 1 for demographic information relating to the Cohort.

Table 1. Cohort Demographics

Results on the Verbal Learning and Visual Learning subtests of the Wide Range Assessment of Memory and Learning (WRAML) (Sheslow & Adams, 1990) were examined. Results included the subtest scaled scores, based on the number of words recalled over 4 learning trials, delayed recall savings scores (percentage of the 4th learning trial recalled after a delay), and a verbal learning recognition trial (percentage of targets correctly recognised following delayed recall). These tasks are typical of those used in clinical settings to detect deficits in LTM, specifically in episodic declarative memory. Reading (word recognition) was assessed on the Wide Range Achievement Test - Revised (WRAT-R).

The WRAML Sound Symbol Learning subtest results were also examined to control for the effect of a phonological processing deficit on the other memory tasks and the WRAML Number Letter subtest results to control for memory span.

Subtypes were determined based on possible patterns of long-term memory deficit. Cut-off points were based on standardisation data for the tests used and the statistical characteristics of the SLD cohort memory variables.

RESULTS

Exploratory analysis revealed a number of outliers, particularly for Visual Learning Delayed Recall. Outliers were omitted before statistical analysis.

All statistical analyses were carried out using SPSS version 10 for Windows.

Single sample t tests (see Table 2) were carried out to compare memory test results with the standardisation groups of the tests used. The LD cohort did not differ significantly from the test standardisation group on Verbal Learning (t=-.674; df=299; ns) or Visual Learning (t=.315; df=293; ns). The LD cohort differed significantly from the standardisation group on Sound Symbol Learning (t=-15.85; df=201; p<0.01) and Number Letter Memory (t=-29.64; df=294; p<0.01). There were significant differences for all delayed recall results: Verbal Learning Delayed Recall (t=-6.16; df=296; p<0.01), Visual Learning Delayed Recall (t=-3.22; df=286; p<0.01), Sound Symbol Delayed Recall (t=-4.92; df=170; p<0.01). There was no significant difference for Verbal Learning Recognition (t=-1.44; df=230; ns)

Table 2. Cohort Results on Memory Tests Compared with Test Standardisation Means (Predicted Mean)

The following mutually exclusive memory deficit subgroups were formed:-

1. Abnormal forgetting of verbal material (Verbal Learning Delayed Recall Savings Score less than 70). (n=14; 4.7% of the Cohort)
2. Verbal encoding deficit (Verbal Learning scaled score less than 7 and delayed recall greater than 70). (n=22; 7.4%)
3. Verbal retrieval deficit (Verbal Learning delayed recall less than 70 and recognition greater than 73). (n=49; 16.6%)
4. Abnormal forgetting of visuo-spatial material (Visual Learning delayed recall less than 75). (n=17; 5.8%)
5. Visuo-Spatial encoding deficit (Visual Learning scaled score less than 7 and Visual Learning delayed recall less than 74). (n=15; 5.1%)
6. Global memory deficit (Verbal Delayed Recall less than 70 and Visual Delayed Recall less than 75). (n=10; 3.4%)
7. Normal memory results. (n=168; 57%)

Cases with missing data for either Verbal or Visual Learning were omitted. The seven category subgrouping was examined statistically using the Kruskal Wallis Test. The subgrouping proved to be statistically robust (see Table 3).

Table 3. Memory Deficit Subgroups: Kruskal Wallis Test Results

No significant differences were found between the memory deficit subgroups on age, VIQ, PIQ, verbal memory span, or word recognition.

Verbal and Visual Learning Delayed Recall results were assigned to 8 subgroups based on the level of delayed recall. There was no significant difference in the reading levels of these 8 Verbal subgroups. There was a significant difference between the groups in Visual Learning Delayed Recall. However, post hoc analysis indicated that the difference was not related to severity of the delayed recall deficit.

A stepwise multiple regression analysis was carried out with reading as the dependent variable and the LTM variables and VIQ as independent variables. Only Sound Symbol Learning and VIQ emerged as significant predictors of reading explaining approximately 19% and 28% respectively of the variability in reading.

Verbal Learning Recognition, unlike the delayed recall measures, was significantly correlated with age with recognition increasing with age. Verbal Learning Recognition was a significant predictor of reading but when age was included in the analysis as a covariate the Recognition-Reading relationship was no longer significant.

DISCUSSION

A range of specific LTM deficit subtypes was evident in this LD Clinic cohort. In contrast to previous studies which have found normal rates of forgetting in groups of children with SLD, nearly 14% of this cohort displayed abnormal forgetting of verbal and/or visuo-spatial material. This loss of information after a delay has been associated with medial temporal brain pathology in children (Gadian et al, 2000) and appears to be the most distinctly abnormal feature of performance in this LD cohort. Approximately 12% displayed deficient encoding of verbal or visuo-spatial material but in this subgroup once information was encoded it was not forgotten. While this is a less distinct feature it could also be linked to deficiencies in the key memory centres in the brain.

The identification of these deficits in this cohort can be partly attributed to the large group of subjects examined. The low incidence (e.g. around 8% displaying abnormal forgetting of verbal material) of these LTM deficits may account for the fact that they have not emerged in other studies which have examined LTM.

There was also a significant verbal retrieval deficit group (about 16% of the cohort). Retrieval deficits may be related to problems in encoding and retrieval strategies and have been linked to white matter dysfunction in children with myelomeningocele (Yeates, Enrile, Loss, & Blumenstein, 1995). The frontal lobes of the brain have also been implicated in retrieval. The recognition procedure used to infer a retrieval deficit raises a further issue in that it has been suggested that such procedures involve a significant element of implicit memory. This appears to be a potentially fruitful area for further research with a recent report suggesting a link between deficient visual implicit learning and developmental surface dyslexia (Samuelsson, Bogges, & Karlsson, 2000). Furthermore, there has been one case report of successful training of reading of pseudo-words in a 19 year old amnesic, AC, who was 10 years old at the onset of the amnesic syndrome (Benedict et al, 1998). AC's episodic and semantic memory was severely impaired but she performed normally on tests of implicit and procedural memory suggesting that these non-declarative memory processes were significant in her successful learning.

As a group the Cohort performed normally in encoding verbal material which did not involve a significant novel, phonological processing element. Where a phonological processing element was involved the Cohort demonstrated a significant encoding deficit. This encoding deficit did not appear to impact on delayed recall as delayed recall of the relatively phonological processing-free verbal material did not differ from delayed recall of material involving a phonological processing element.

Although some aspect of LTM was an area of weakness for a significant proportion of the Cohort, there was no evidence of a relationship between LTM variables and reading levels apart from where the LTM variable involved a novel phonological processing element. Even the most globally memory impaired subgroup, those with deficient verbal and visual delayed recall, did not differ from the unimpaired LTM subgroup on reading. There was also no difference between the LTM subgroups in VIQ and although VIQ was significantly lower than the standardisation sample mean it was nonetheless still well within the average range.

Given the significant element of semantic knowledge involved in VIQ it would appear that as a group this LD cohort has relatively intact semantic memory. Even in the cases of the most severely impaired episodic memory, VIQ did not differ from those with unimpaired episodic memory. This dissociation lends weight to the contention of Mishkin et al (1998) that episodic and semantic memory are dissociable although it does not rule out the possibility that pre-semantic implicit learning processes might play a major role in reading development.

These results support the considerable evidence that a deficit in phonological processing is the most significant factor underlying developmental disorders of reading acquisition. Episodic memory, on the other hand, does not appear to play a significant role in the accumulation of associations and rules involved in the reading development process.

It would appear that only a small percentage (around 3%, in fact) of children with SLD fall at the more severe end of the episodic memory deficit scale and exhibit a global, non-material specific deficit which has been termed developmental dysmnesia. This very small subgroup is unlikely to be detected in small group studies of children with SLD. There was a larger group of children (around 11%) with a deficit in delayed recall of either verbal or visuo-spatial material.

The significance of these memory deficits in children with SLD requires further research. Although these episodic memory deficits may not have a significant impact on reading development their possible significance in activities of daily living remain to be explored given the difficulties reported by Gadian et al (2000) in their five cases of developmental amnesia. It would seem that relatively large groups of children with SLD would need to be examined to detect the small proportion displaying significant episodic memory impairment. From a clinical point-of-view word-list learning tasks such as the WRAML Verbal Learning subtest represent a relatively quick and efficient means of screening for episodic memory deficits in children with SLD. Where episodic memory deficits do emerge clinicians must be cautious about suggesting a causal link between the episodic memory deficit and the SLD.

There may be implications for reading instruction where delayed recall deficits exist. Evidence suggests that errorless learning approaches may be more productive in establishing some learning in adults with acquired amnesia (Ylvisaker & Feeney, 1998). Such an approach, which is a component of the Direct Instruction approach to reading, may promote some acceleration in reading development in SLD children with episodic memory deficits.

REFERENCES

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Broman, M., Rose, A L., Hotson, G., & Casey, C M. (1997). Severe anterograde amnesia with onset in childhood as a result of anoxic encephalopathy. Brain, 120, 417-433.

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Yeates, K.O., Enrile, B.G., Loss, N., & Blumenstein, E. (1995). Verbal learning and memory in children with myelomeningocele. Journal of Pediatric Psychology, 20, 801-815.

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