1. Introduction
Declarative verbal memory includes the processes of learning new verbal information (
i.e., encoding words, facts, stories), storing the verbal information over time (
i.e., retention) and, later, overtly recalling or recognizing the verbal information (
i.e., retrieval). Research in healthy children and adults has long sought to understand the declarative verbal memory process and its underlying components. Although verbal memory problems are common in a wide variety of clinical pediatric populations (e.g., memory difficulties have been reported in children with Attention-Deficit/Hyperactivity Disorder [ADHD], Autism Spectrum Disorder [ASD], epilepsy, traumatic brain injury [TBI] and cancer), very little information is known regarding the specific verbal memory processes affected in these groups [
1]. Interestingly, the nature of verbal memory problems seems to vary widely, even within specific populations (e.g., epilepsy and TBI) [
2,
3]. The heterogeneous nature of verbal memory problems both within and across pediatric patient populations may be related to differences in the neuroanatomical sites of disruption underlying the involved memory process. Alternatively, these verbal memory problems may be occurring secondary to impairment in other cognitive factor(s), such as poor verbal knowledge or attentional skills [
4].
Research in healthy children and adolescents suggests that some memory processes occur independent from other cognitive abilities (e.g., incidental encoding and implicit recognition); however, research has revealed that the development of and normal variations in
declarative verbal memory abilities are related to several specific cognitive domains [
4,
5,
6]. In contrast to non-declarative memory, declarative verbal memory is considered a more “mature” form of memory, because it requires the additional act of conscious awareness when remembering verbal information. Declarative verbal memory improves with age and brain development; the maturation of the prefrontal cortex and its connections with the temporal lobe and other cortical areas contribute to declarative verbal memory [
7]. Interestingly, these developmental gains in verbal memory ability also coincide with rapid development of verbal knowledge, attention, processing speed, working memory and other executive functions. Furthermore, these cognitive factors are believed to provide critical support for the maturation of declarative verbal memory strategies, which themselves become more strategic, complex and effective with age [
7]. In fact, elaborative verbal encoding strategies and effortful systematic verbal retrieval searches appear to be particularly related to verbal knowledge, attention, processing speed, working memory and executive functioning [
1,
5,
7,
8,
9,
10]. Yet, research has not determined how difficulties in verbal knowledge, attention, processing speed, working memory and other executive functions may be related to the verbal memory problems often seen in pediatric patients with medical or developmental disorders.
Thus, the overall goal of the current study was to determine which cognitive factors contribute to delayed verbal memory performance in a large and heterogeneous sample of clinical pediatric patients. First, a factor model was developed in order to demonstrate how specific neuropsychological measures could be used to identify the discrete cognitive domains of interest in a heterogeneous pediatric sample. It was hypothesized that the cognitive model would be consistent with constructs purported by the test developers, and the model would identify factors representing verbal knowledge, attention, processing speed and working memory/executive functioning. Second, it was hypothesized that each of the cognitive factors of interest would significantly predict overall verbal memory performance. This hypothesis was based on previous literature suggesting that these cognitive domains contribute to verbal memory abilities in healthy, normally developing children. Finally, the relationships between these targeted cognitive factors and specific verbal memory component processes (i.e., encoding, retention and retrieval) were further explored. It was hypothesized that relevant cognitive factors would impact verbal memory performance specifically via influence on encoding and retrieval abilities.
2. Method
2.1. Participants
Data was derived from an Institutional Review Board (IRB)-approved, archival clinical study of pediatric patients who received a neuropsychological assessment at the University of Florida between 2002 and 2012. Patients were those referred for diagnostic clarification and treatment recommendations for a wide variety of childhood conditions (e.g., ASD, ADHD, learning disabilities, communication disorders), as well as cognitive disorders resulting from neurological disease or insult (e.g., TBI, stroke, epilepsy, cancer). Data for the current study was extracted for children between the ages of 5 years 0 months and 16 years 11 months who had completed the verbal memory measures of interest (i.e., core verbal subtests from the Children’s Memory Scale). In order to ensure that the current study results could be generalized to a broad pediatric population, patients were not excluded for any comorbid psychological or medical conditions, and there was no cut-off used to exclude patients of lower intellectual functioning.
2.2. Measures
Verbal memory abilities were assessed using the Children’s Memory Scale (CMS). The CMS is a comprehensive measure designed to assess learning and memory processes in children ages 5 to 16 [
11]. Completion of the core battery of CMS verbal memory tests yields a norm-referenced index score of general verbal memory ability (
i.e., Verbal Delayed Memory Index), as well as a score representing verbal encoding skills (
i.e., Verbal Immediate Memory Index). Using recommendations from the CMS manual and communications with the test author, two additional norm-referenced verbal memory process scores were derived to represent verbal retention and retrieval skills [
11,
12,
13]. Thus, the test scores analyzed for the current study were the CMS Verbal Delayed Memory Index (general verbal memory ability), the CMS Verbal Immediate Memory Index (encoding), a derived percent retention score (retention) and a derived delayed memory contrast score, which compared delayed recall and delayed recognition performances (retrieval).
In addition to the CMS, neuropsychological measures assessing verbal knowledge, sustained attention, working memory, processing speed and working memory/executive functioning were selected. Specifically, the following measures were used as estimates of verbal knowledge, processing speed, attention and working memory/executive functioning: from the Wechsler Intelligence Scale for Children, 4th Edition (WISC-IV), the 5 core subtests comprising the Verbal Comprehension Index (VCI) and the Processing Speed Index (PSI), as well as the Digit Span Backwards subtest [
14] and from the Test of Everyday Attention for Children (TEA-Ch), the Sky Search, Score! and Creature Counting subtests [
15]. Of note, the total score from the TEA-Ch Creature Counting subtest was expected to be a measure of working memory, because this score is dependent on accurate and speeded mental manipulation of numbers [
15]. The other core working memory subtests of the WISC-IV (
i.e., Digit Span Forwards, Letter-Number Sequencing) were not examined in this study in order to minimize the number of variables entered into analyses.
2.3. Analyses
Two multivariate statistical analyses were conducted: an Exploratory Factor Analysis (EFA) and Structural Equation Modeling (SEM). The EFA was used to construct a model where the latent factors represent cognitive domains and the measured indicators are scores from neuropsychological tests. The neuropsychological measures included in the model were the Wechsler Intelligence Scale for Children, 4th Edition (WISC-IV), core verbal comprehension subtests (i.e., Vocabulary, Similarities, Comprehension), the WISC-IV processing speed subtests (i.e., Symbol Search and Coding), WISC-IV Digit Span Backwards and three subtests of the TEA-Ch (i.e., Sky Search, Score!, and Creature Counting). Missing data was excluded using pairwise methodology, and an oblique rotation (Promax) was utilized to determine the factor matrices. The EFA was conducted with SPSS version 18.0.
Next, the cognitive factors identified in the EFA were entered into an SEM that investigated the relationship between the cognitive factors and a measure of general verbal memory performance (
i.e., the CMS Delayed Verbal Memory Index score). The initial specified model was developed based on the results of the EFA. Each latent factor and any measured variables that did not load onto a factor in the EFA were predictors in the SEM. Data was examined and appeared to meet multivariate (e.g., normal distribution, homogeneity of variance, sphericity) and SEM assumptions (
i.e., large sample size) [
16,
17]. All SEM analyses were conducted using the Analysis of Moment Structures (AMOS) software [
18]. A special form of Maximum Likelihood (ML) estimation for incomplete data was used to obtain model fit, as well as parameter estimations, because ML is robust to missing data [
17]. Models were assessed using multiple assessments of good fit (e.g.,
Χ2,
p < 0.01, root mean square error of approximation (RMSEA) < 0.05) [
17]. Significant parameter estimations (
i.e.,
β weights) were identified using a
p < 0.05 probability criterion
In addition to the multivariate analyses, a correlation matrix was used to examine the specific relationships between measures of verbal memory processes (i.e., CMS verbal encoding, retention and retrieval indices) and individual cognitive measures (e.g., WISC-IV Vocabulary, Comprehension and Similarities subtests), as well as overall delayed verbal memory performance. A statistical criterion of p ≤ 0.05, two-tailed, was used to confirm significant correlations between variables.
Finally, a mediation analysis was used to further examine the nature of the relationship between significant cognitive factors identified in the SEM and delayed verbal memory performance. Specifically, Preacher and Hayes’s bootstrapping method was used to investigate whether the relationship was mediated by the indirect effect of cognitive factors on encoding, retention and/or retrieval processes [
19]. The SPSS INDIRECT macro was used to conduct the bootstrapping analysis [
19]. A moderate statistical criterion (
p < 0.05) was used to identify significant effects.
5. Conclusions
The goal of this study was to extend previous research conducted in healthy adults and children to a clinical pediatric sample. Pediatric patients are often referred for neuropsychological evaluation and treatment of verbal “memory problems”; however, previous research has not described the exact nature of these difficulties within a memory process model, nor which cognitive factors might contribute to identified memory problems. This study found that in a large, heterogeneous sample of pediatric patients, verbal knowledge skills are positively associated with performance on verbal memory tasks. No other measured cognitive factors were significantly related to verbal memory performance. This finding was consistent with existing literature that reports that verbal knowledge is related to verbal memory abilities in healthy, normally developing children. The exact causal nature of this relationship remains unclear; however, these current results support the theory that improving verbal knowledge will improve verbal encoding, which, in turn, will positively impact overall verbal memory skills. This hypothesis may have important treatment implications. Specifically, this raises the possibility of improving verbal encoding abilities (and, thus, verbal memory skills) by directing cognitive rehabilitation efforts toward improved verbal knowledge. If the current study findings are replicated, we would recommend future rehabilitation studies that seek to identify methods for improving verbal knowledge in pediatric patients with memory difficulties and investigate whether interventions targeting verbal knowledge skills result in additional verbal memory encoding (and associated verbal memory) improvements.