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. Author manuscript; available in PMC: 2014 Mar 28.
Published in final edited form as: Child Neuropsychol. 2012 Mar 1;19(2):173–189. doi: 10.1080/09297049.2011.648922

Memory Processes in Learning Disability Subtypes of Children Born Preterm

Thomasin E McCoy 1, Amy L Conrad 1, Lynn C Richman 2, Peg C Nopoulos 1,2, Edward F Bell 2
PMCID: PMC3968320  NIHMSID: NIHMS392337  PMID: 22375897

Abstract

The purpose of this study was to evaluate immediate auditory and visual memory processes in learning disability subtypes of 40 children born preterm. Three subgroups of children were examined: (a) primary language disability group (n = 13), (b) perceptual-motor disability group (n = 14), and (c) no learning disability diagnosis group without identified language or perceptual-motor learning disability (n = 13). Between-group comparisons indicate no significant differences in immediate auditory or visual memory performances between language and perceptual-motor learning disability groups. Within-group comparisons revealed that both learning disability groups performed significantly lower on a task of immediate memory when the mode of stimulus presentation and mode of response were visual.

Memory impairments, including working memory, immediate memory, and learning, have been well-documented in preterm children/adolescents compared to full-term (Briscoe, Gathercole, & Marlow, 1998; Hack et al., 1992; Luciana, Lindeke, Georgieff, Mills, & Nelson, 1999; Ross, Lipper, & Auid, 1991; Whitfield et al., 1997). Group differences exist even after controlling for vocabulary and excluding children with neurosensory deficits or IQ < 80 (Taylor, Klein, Minich, & Hack, 2000). Impairments in visual memory span (Rickards, Kitchen, Doyle, Ford, Kelly, & Callanan, 1993), spatial span (Luciana et al., 1999; Saavalainen, Luoma, Bowler, Maatta, Kiviniemi, Laukakanen, et al., 2007), and spatial location learning have been found in former preterm children/adolescents after adjustment for degree of prematurity, race/ethnicity, and gender (Baron, Erickson, Ahronovich, Litman, and Brandt, 2010). Impairments in spatial working memory have been found in toddlers (Baron et al., 2010), preschoolers (Woodward, Edgin, Thompson, & Inder, 2005) and school-aged preterm groups (Bohm, Smelder, & Forssberg, 2004; Luciana et al., 1999). Early working memory impairments have been shown to predict academic problems and learning disabilities at school ages (Wolke & Meyer, 1999). Despite the numerous studies reporting memory deficits of former preterm samples, inconsistencies in memory outcomes are also evident. Some studies, for example, failed to find significant differences between preterm and comparison groups on tests of memory function (Hall, McLeod, Counsell, Thomson, & Mutch, 1995; Herrgard, Luoma, Tuppurainen, Karjalainen, & Martikainen, 1993; Klein, Hack, & Breslau, 1989; Narberhaus, Segarra, Gimenez, Junque, Pueyo, & Botet, 2007; Ross, Lipper, & Auld, 1991).

Differences in memory outcomes within the preterm population may be attributed to additional variables, including degree of prematurity and low birth weight, severity of neonatal insult, and maternal education (Luu, Ment, Allan, Schneider, & Vohr, 2011). A number of studies have demonstrated a gradient effect by which performance on cognitive measures is significantly and positively correlated with birth weight (BW) and gestational age (GA; Bhutta, Cleves, Casey, et al., 2002; Anderson et al., 1990; Taylor, Klein, & Hack, 2000; Taylor et al., 2006; Taylor, Klein, Minich, et al., 2000). Other findings have shown that memory performances may vary depending upon the age range of preterm children assessed in a given study. For example Siegel (1985) assessed three age ranges (5, 6, and 7) and found no differences between preterm and full-term at age 5, though differences were evident in sentence repetition at 7 and expressive language at 6.

The severity and incidence of neurological insult (i.e., periventricular damage) has also been associated with later cognitive performance. For example, in a study of extremely low BW (ELBW; < 1000 grams) infants, Jakobson, et al. (2001) found an association between working memory deficits and mild periventricular damage. In contrast, more severe neurologic insults were associated with receptive vocabulary and naming difficulties.

Learning Disabilities and Memory Functioning

Developmental neuropsychological research with non-preterm groups suggests that performances on measures of verbal short-term and working memory are associated with patterns of neuropsychological functioning. For example, deficits in phonological short-term memory (i.e., nonword repetition) have been found in children with specific language impairments (Bishop, North, Donlan, 1996; Gathercole & Baddeley, 1990; Gilliam, Cowan, & Day, 1996). Visual memory deficits have been found in conjunction with primary deficits in visual-spatial (i.e., nonverbal) reasoning (Tranel, Hall, Olson, & Tranel, 1987; Zimmer, Speiser, & Seidler, 2003) and/or deficiencies in verbal labeling of visual information related to a primary language learning disability (LD; Lindgren, Richman, & Eliason, 1986; Lindgren & Richman, 1984; McCarthy, Richman, & Yarbrough, 1995). Findings from studies of other high-risk cohorts, such as children with orofacial clefts, suggest that cognitive deficits, particularly subtle deficits, may be overlooked or misdiagnosed as primary attention deficits or behavior problems (Richman, Ryan, Wilgenbusch, & Millard, 2004). Thus, the extent to which deficits in language or nonverbal cognitive functioning are associated with visual and verbal memory function is unclear.

Subtyping of preterm children based upon verbal and perceptual-motor deficits or some combination of the two is uncommon in research within the preterm population. At least one study (Grunau, Whitfield, & Davis, 2002) examined patterns of learning disabilities (LD) in former ELBW children without intellectual or neurologic impairment. In this study, 19% (9 of 74) met criteria for a learning disability in all three areas assessed (i.e., reading, arithmetic, and written expression) based upon verbal intelligence quotient (VIQ) and perceptual intelligence quotient (PIQ) discrepancies; 65% (48 of 74) met LD criteria in one or more areas; 35% (26 of 74) did not meet LD criteria in any of the three academic areas assessed. Examination of the prevalence of diagnostic subtypes within the preterm group compared to the full-term group according to the model by Harnadek and Rourke (1994) revealed that 13% of preterm participants met criteria for nonverbal learning disability (NLD); 7% of preterm met criteria for verbal impairment (VI); and 7% were classified as other learning disability. In total, 55% (41 of 74) of the ELBW preterm group met criteria for inclusion in one of the three diagnostic groups (NLD, VI, or other LD) compared to 10% (3 of 30) of full-term participants.

Aims

The current study examined patterns of immediate memory performances in a group of former preterm, very low birth weight (VLBW) children at school ages by classifying participants according to differential patterns of neuropsychological functioning.

Method

Participants

This study was approved by the university's institutional review board. The participants in this study included 40 former premature, VLBW children of at least broad average intelligence who were between the ages 8 and 14 (mean age 11.70, standard deviation [SD] = 1.56). Participants for the current study were selected from a subset of a larger sample of children enrolled in a study on the effects of red blood cell (RBC) transfusion on brain structure and function in children born prematurely (Bell et al., 2005). The original transfusion study and follow-up study on neurocognitive profiles of preterm children randomly assigned to either a liberal or restrictive transfusion strategy are described in detail elsewhere (McCoy et al., 2011). Briefly, participants were eligible for the Bell et al. study if they received neonatal care at the University Hospital between December 1992 and June 1997; had BWs between 500 and 1300 grams; and had one or more RBCs as neonates due to complications associated with preterm birth. None of the participants in the Bell et al. (2005) study had a history of alloimmune hemolytic disease, congenital heart disease, other major birth defects requiring surgery, or a chromosomal abnormality. None of the children participating in the follow-up study (McCoy et al., 2011) had histories of significant hearing loss or history of epilepsy, brain tumor, or head injury resulting in unconsciousness or concussion. A total of 16 of the 56 participants in the McCoy et al. (2011) study were excluded from the present study due to (1) intellectual or developmental disability (i.e., three participants with intellectual disability (defined by prorated Wechsler Intelligence Scale for Children, Fourth Edition [WISC-IV] Verbal Comprehension Index [VCI] < 80 and Perceptual Reasoning Index [PRI] < 80); (2) neurological impairment or sensory deficits that may have interfered with performance on cognitive and academic tasks; and/or (3) incomplete test data (i.e., data for two or more of the measures described in the Instruments section were missing and/or incomplete). The current sample was predominantly male (55%), Caucasian (86.5%; 8.1% African American; 5.4% Multiracial), non-Latino (96.7%), lower-middle-class (mean socioeconomic status [SES] = 2.63, SD = 0.48), and had parental education of at least a high school diploma (mean maternal education = 13.73 years, SD = 2.30; mean paternal education = 13.09 years, SD = 2.29). Mean BW and GA of the sample were 937.03 grams (SD = 193.98) and 27.67 weeks (SD = 2.03), respectively.

Procedure

Participants received neonatal care at the University of Iowa Children's Hospital between December 1992 and June 1997 and had BWs between 500 and 1300 g. None of the participants in the current study had a history of alloimmune hemolytic disease, congenital heart disease, other major birth defects requiring surgery, or a chromosomal abnormality. The Score for Neonatal Acute Physiology (SNAP; Richardson et al., 1993) was recorded on the day of birth and once daily through the first week of life.

At the time of follow-up, guardians were asked to accompany their children to the hospital, and informed consent was obtained in writing from one or both guardians prior to their child's participation. Guardians completed a demographic questionnaire designed for this study that included questions regarding academic performance, SES, and pregnancy/childbirth history. Children completed a battery of cognitive, neurologic, behavioral, and social-emotional tests. All assessments were conducted by a licensed psychologist or a psychology graduate assistant. Guardians of participants were reimbursed for travel, lodging, and meal expenses. Child participants were compensated monetarily.

Instruments

Cognitive Functioning

Cognitive, or intellectual, functioning was assessed using the WISC-IV (Wechsler, 2003a, 2003b). Raw scores for each subtest were converted to scaled scores based upon the test norms for each participant's age at the time of testing. Scaled scores were converted to standard scores for verbal, nonverbal, and processing speed domains and for the General Ability Index (GAI)—a composite of verbal and perceptual domains. The VCI was prorated using scaled scores from Similarities and Vocabulary subtests; the PRI was prorated using Block Design and Matrix Reasoning subtests; and the Processing Speed Index (PSI) using Digit Symbol-Coding and Symbol Search subtests. Internal reliability (r = .79 to .90) and test-retest reliability (r = .76 to .92) for these subtests are excellent (Raiford et al., 2005).

Reading Achievement

The Reading subtest of the Wide Range Achievement Test, Third Edition (WRAT-3) (Wilkinson, 1993) was administered to assess decoding or word recognition abilities. The raw score—or total number of correctly identified words—was converted to an age-based standard score for each participant based upon test norms.

Neuropsychological Functioning

In order to control for age differences, raw scores for the following neuropsychological tests were converted to age-corrected z-scores by comparing each participant's performance with that of same-age (and same-sex, when applicable) peers from the normative test sample. For participants outside the age ranges of the available norms were computed based upon the highest age norms available.

Associative Verbal Fluency

Associative verbal fluency was assessed using a test of Controlled Oral Word Association (COWA) (using the letters “CFL”) from the Multilingual Aphasia Examination (Benton & Hamsher, 1983). Participants were asked to say aloud as many words as possible in one minute for each of three common letters. The score is the total number of words provided for all three letters.

Rapid Automatized Naming

Rapid naming was assessed using the Color Naming subtest of the Rapid Automatized Naming (RAN) test (Denkla & Rudel, 1976). This test requires rapid serial naming of colors that appear multiple times throughout the page. The score is the total time needed to name all colors.

Fine Motor Coordination

Fine motor coordination was assessed by the Grooved Pegboard Test (GPB). This test was developed by Kløve (1963) and is designed to assess fine-motor coordination. It requires participants to quickly place pegs into small holes using their dominant and nondominant hands. Scoring is based upon total time (in seconds) required to place all pegs with each participant's dominant hand.

Visual-Motor Integration

Visual-motor integration was assessed using the Bender Visual-Motor Gestalt Test, Second Edition (Bender-II) (Grannigan & Decker, 2003). For this test, participants were asked to copy increasingly complex geometric designs from cards. Scores for each design are based on the degree of accuracy with which the figure was drawn.

Memory

Immediate memory skills were evaluated using the Color Span Test (Richman & Lindgren, 1978), which assessed retention of color names in increasingly longer sequences. The test consists of three 8 × 11-inch cards, each of which contains the same, regularly-spaced eight color chips (red, blue, green, black, white, brown, yellow, and orange) arranged in different positions on each of the three cards. The cards are constructed so the colors have no common horizontal or vertical alignment, which lessens the possibility that the participant could use verbal or spatial cues to aid memory. The three cards are alternated for each trial to further minimize the effect of hierarchical grouping, which subjects sometime use to remember digits and letters (Chase & Erickson, 1982) or semantic elaborations, which subjects often use to remember lists of words or sequences of pictures (Rohwer, 1980). The use of colors allows assessment of memory span in a manner which is relatively independent of tactile or pictorial associations. It is recognized that the use of colored strips with varying horizontal and vertical alignments together with the use of alternating cards serves merely to minimize the use of visual strategies and promotes use of verbal mediation. Furthermore, by varying stimulus and response combinations, it may be possible to distinguish processing differences between presumably different cognitive groups.

The Color Span Test consists of four subtests which involve different stimulus and response combinations. Standardization with the normative sample indicated no order effects; thus, the subtests are presented in the following fixed order: (1) visual presentation-visual response (pointing), (2) visual presentation-verbal response, (3) verbal presentation-visual response (pointing), and (4) verbal presentation-verbal response. For each presentation, the examiner begins with a two-color sequence and proceeds through two trials at each span until two incorrect responses at a given span occur, analogous to the Digit Span subtest of the WISC-IV (Wechsler, 2003a, 2003b). The fourth trial (verbal presentation-verbal response) is analogous to the Digits Forward portion of the WISC-IV Digit Span subtest (Wechsler, 2003a, 2003b). The examiner must ensure that the child recognizes each color prior to the administration of the first subtest. There are seven spans for each subtest, with span length ranging from two to eight. Each correct response (requiring correct colors and sequence) is given one point, and 14 points is the maximum score possible for each subtest.

Attention/Concentration Functioning

Attention and impulsivity were assessed using a standardized computer test, the Continuous Performance Test, 2nd edition (CPT-II; Lindgren & Lyon, 1983). Participants watch stimuli on a computer screen presented at a variable rate of speed; participants are instructed to press the spacebar when the target appears on the screen and refrain from pressing the spacebar for all non-targets. Raw scores are total omission (inattentive) and commission (impulsive) errors, which are converted to z-scores based upon the sex and grade of each participant. Z-scores were converted so that higher scores reflect better performances.

Learning Disability Subtypes

The 40 participants in this study were assigned to one of three groups based upon their test performances. The following subtype criteria were developed in an a priori manner based upon LD definitions in previous studies of immediate memory functioning in non-preterm, clinical samples (e.g., Lindgren & Richman, 1984; Lindgren, Richman, & Eliason, 1986; Wood & Richman, 1988; Wood, Richman, & Eliason, 1989). The definitions are also based upon Harnadek and Rourke's (1994) analysis of neuropsychological functions--which discriminate NLD from disabilities in reading and spelling—though they have been modified to reflect the test data available for this sample of preterm participants. It is for this reason that additional measures and types of data, such as arithmetic and written language achievement, were not incorporated into the above LD definitions.

Participants were categorized in a hierarchical fashion, such that participants were first considered for Group 1; participants who did not meet criteria for Group 1 were then considered for Group 2. All remaining participants were assigned to Group 3. This method of categorization assured that groups were mutually exclusive and that no participant was included in more than one group. Participants were grouped according to the following patterns of neuropsychological functioning:

  • Group 1: Primary Language Learning Disability

    A total of 13 of 40 participants (32.5%) met criteria for Group 1: Primary language disability. Participants in Group 1 performed below average on at least one measure of expressive language (i.e., z-score ≤ -1.0 on either verbal fluency and/or rapid naming) but average or above on a test of perceptual-motor integration.

  • Group 2: Perceptual-Motor Disability (With or Without Language Disability)

    Fourteen of the remaining participants (or 14 out of the total 40; 35%) who were not classified into Group 1 met criteria for Group 2: Primary perceptual-motor disability. Participants in Group 2 were either below average on a test of perceptual-motor integration or performed lower on measures of nonverbal (perceptual) skill relative to measures of verbal ability (i.e., prorated VCI > PRI by 10 or more standard score points). Though the members of this group could by definition exhibit mixed deficits (i.e., deficits in both language and perceptual-motor functioning), only 2 (14%) of 14 performed below average on measures of verbal fluency and perceptual-motor integration.

  • Group 3: No Learning Disability Diagnosis

    A total of 13 of 40 (32.5%) participants failed to meet criteria for a primary deficit in language (Group 1) or perceptual-motor deficit (Group 2) and were assigned to Group 3.

Statistical Analyses

To evaluate the differences in cognitive, academic, and neuropsychological performances across LD subtype, we conducted the following comparisons using univariate analysis of variance (ANOVA) with subtype as the independent variable. For sets comprised of more than one dependent variable, alpha levels were adjusted with a Bonferroni correction. The following analyses were performed

  1. Demographic and neonatal characteristics: age (at the time of testing), maternal educational attainment (in years), SES, BW, GA, and SNAP. Values of p < .008 are significant;

  2. Cognitive functioning: VCI, PRI, PSI, and composite (GAI). Values of p < .013 are significant;

  3. Reading achievement: WRAT-III reading. Value of p < .05 is significant;

  4. Language functioning (COWA and RAN colors), values of p < .025 are significant;

  5. Perceptual-motor functioning (Bender-II and Grooved Peg), values of p < .025 are significant;

  6. Attention/concentration functioning: CPT-II omission and commission errors. Values of p < .025 are significant.

Because the focus of the current paper was on patterns of memory deficits in preterm children with primary disabilities in either language or nonverbal functioning, only groups (Group 1 and 2) were included in the analyses of memory performance by group and Color Span Trial. To evaluate between-group differences in memory performances, a multivariate analysis of variance (MANOVA), with group (subtype) as the fixed factor and Color Span Trial (1, 2, 3, 4) as the dependent factors, was conducted. In order to examine difference in memory performance across the four Color Span Trials, A repeated measures ANOVA was run for Group 1 and Group 2 with each trail of the Color Span as the within-group variable. Between-group differences of the two LD subtype groups were analyzed using multivariate analysis of variance (MANOVA), with group (subtype) as the fixed factor and Color Span Trial (1, 2, 3, 4) as the dependent factors.

Results

Demographic and neonatal characteristics are reported in Table 1. Means and standard deviations (SDs) of cognitive, neuropsychological, and achievement scores by LD subtype are reported in Table 3. Of note, differences in language and/or perceptual-motor performances were anticipated for those indices and measures utilized in the classification of participants into groups (PRI, Bender-II, COWA, RAN Colors). (1) No group differences were observed for neonatal and demographic characteristics. Age, maternal education, SES, BW, GA, and average SNAP score for first week of life did not differ between the three LD groups. Levine's Test of Equality of Error Variances for heterogeneity of variance for BW between the three groups was non-significant (F (2, 37) = 2.32, p = .112). Please refer to Table 2 for distribution of sex and transfusion strategy by subtype. There were no apparent differences in the distribution of sex and transfusion strategy (liberal vs. restrictive) between Groups 1 and 2. Group 3 (No LD) had fewer participants who had been assigned to a liberal transfusion strategy and fewer female participants than either LD groups (Groups 1 and 2).

Table 1. Demographic and Neonatal Characteristic by LD Subtype: Means, Standard Deviations, Multi-Variate Group Differences.

Language LD Perceptual-Motor LD No LD F p ηp2
Mean (SD) Mean (SD) Mean (SD)
Age 11.67 (1.50) 11.18 (1.57) 12.29 (1.53) 1.75 0.19 0.086
SES 2.79 (0.40) 2.57 (0.48) 2.54 (0.54) 1.01 0.38 0.055
Mom Ed 13.50 (2.20) 14.00 (2.55) 13.67 (2.31) 0.15 0.87 0.009
BW 941.92 (187.58) 894.86 (233.30) 977.54 (155.74) 0.61 0.55 0.032
GA 27.92 (1.50) 27.02 (2.60) 28.12 (1.75) 1.13 0.36 0.057
SNAP0 13.58 (8.79) 18.86 (8.22) 13.46 (7.11) 1.97 0.15 0.099
SNAPW1 9.17 (4.86) 14.00 (8.13) 9.00 (3.85) 3.02 0.06 0.143
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Note. Participant age at time of neurocognitive testing (Age), Socioeconomic Status (SES), ranging from 1 (highest education, income, and social prestige) to 5 (lowest education, income, and social prestige) so that lower numbers reflect higher social class; Mother's Educational Attainment in years (Mom Ed), Birth weight (BW), Gestational Age (GA), Score for Neonatal Acute Physiology Day of Life 0 (SNAP0), Score for Neonatal Acute Physiology Week 1 Average (SNAPW1).

Table 3. Cognitive, Neuropsychological, and Achievement Scores by LD Subtype: Means, Standard Deviations, and Multi-variate Group Differences.

Language LD Perceptual-Motor LD No LD F p ηp2
Mean (SD) Mean (SD) Mean (SD)
Cognitive Tests
 VCI 93.77 (11.27) 104.50 (19.27) 104.38 (15.43) 2.01 .148 0.098
 PRI 96.85 (12.06) 89.07† (12.68) 109.31 (17.44) 6.90 .003* 0.272
 PSI 93.38 (9.36) 87.71 (11.83) 100.46 (12.84) 4.19 .023 0.185
Achievement Tests
 WRAT Reading 96.92 (10.55) 98.43 (14.28) 104.69 (8.85) 1.67 .203 0.083
Neuropsychological Tests
 Language
  COWA -1.51† (0.98) -0.63 (1.24) 0.05 (0.77) 7.32 .002* 0.289
  RAN Colors -0.24† (1.25) -0.03 (1.40) 1.21 (0.85) 5.62 .007* 0.233
 Perceptual-Motor
  Bender-II 107.31 (11.24) 99.21† (12.47) 115.00 (11.91) 5.94 .006* 0.243
  GP Dominant -0.51 (0.87) -2.32† (2.98) 0.03 (0.56) 5.94 .006* 0.243
 Attention/Concentration
  CPT Omission -1.05 (1.86) -1.29 (1.41) -0.72 (1.50) 0.42 .663 0.023
  CPT Commission -1.19 (1.66) -1.07 (1.49) -0.34 (0.81) 1.467 .244 0.075
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Note. Verbal Comprehension Index (VCI); Perceptual Reasoning Index (PRI); Processing Speed Index (PSI); Wide Range Achievement Test (WRAT); Controlled Oral Word Association (COWA); Rapid Automatized Naming (RAN); Grooved Pegboard (GP); Continuous Performance Test (CPT).

*

Denotes significant multivariate differences between groups.

†

Significantly lower than No LD group.

Table 2. Distribution of Sex and Transfusion Strategy by Subtype.

Language LD Perceptual-Motor LD No LD
n = 13 n = 14 n = 13
Male Female Male Female Male Female
Transfusion Strategy
 Liberal 2 8 4 6 3 1
 Restrictive 3 0 1 3 9 0
Total 5 8 5 9 12 1
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  • (2)

    For cognitive functioning, there was a significant difference between the groups for PRI (F (2, 39) = 6.90, p = .003). The PRI for Group 2 was significantly lower than Group 3 (mean difference = -13.26). The PRI did not differ significantly between groups 1 and 2. Means for VCI, PSI, and GAI were not significantly different after Bonferroni correction.

  • (3)

    No significant differences were found for WRAT-III Reading. Although Group 3 (No Diagnosis Group) showed somewhat higher word recognition scores, all three groups scored within the average range.

  • (4)

    Associative verbal fluency (F (2, 38) = 7.32, p = .002) was significantly lower in Group 1 than Group 3 (mean difference = -1.56). Rapid color naming (F (2, 39) = 5.62, p = .007) was also significantly lower in Group 1 compared to Group 3 (mean difference = -1.45). This is consistent with their classification as language impaired.

  • (5)

    Visual-motor integration (mean difference = -15.79; F (2, 39) = 5.94, p = .006) and fine motor speed/dexterity (mean difference = -2.35; F (2, 39) = 5.94, p = .006) scores were lower in Group 2 than Group3. This is consistent with their perceptual-motor LD classification.

  • (6)

    No significant differences between groups were found for omission or commission errors. However, all three groups showed ¾ to 1 ¼ SDs below the mean for inattention, a common feature of prematurity.

Memory Functioning

Mean z-scores and SDs for the four trials of the Color Span Test by group are presented in Table 4. Differences in patterns of memory performance between Group 1 and Group 2 were analyzed using multivariate analysis of variance (MANOVA), with group (subtype) as the fixed factor and Color Span Trial (1, 2, 3, 4) as the dependent factors. Results were non-significant for differences in patterns of immediate memory performance between the Language LD and Perceptual-Motor LD group (F (1, 25) = .075, p = .787).

Table 4. Color Span Means and Standard Deviations by Trial and Subtype.

Trial 1 Trial 2 Trial 3 Trial 4
(Visual-Visual) (Visual-Verbal) (Verbal-Visual) (Verbal-Verbal)
Mean (SD) Mean (SD) Mean (SD) Mean (SD)
Language LD -2.92 (0.44) -1.49 (0.34) -0.82 (0.29) -0.95 (0.31)
Perc-Motor LD -2.97 (0.42) -0.97 (0.33) -0.58 (0.28) -1.18 (0.29)
No LD -1.94 (0.44) -0.69 (0.34) -0.77 (0.29) -1.07 (0.31)
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A repeated measures ANOVA was run for Group 1 and Group 2 with each trail of the Color Span as the within-group variable. Observations of memory performances across Color Span Trial (see Figure 1) revealed similar patterns of memory performance in Group 1 and 2 across all four Color Span Trials. Both groups were lower (> 1.5 SDs) on Trial 1, which is a visual presentation and only requires a pointing response. Group 1 (Language LD) performed significantly lower on Trial 1 than on all other trials: Trial 2 mean difference = -1.71, p = .047, Trial 3 mean difference = -2.25, p = .001, and Trial 4 mean difference = -1.88, p = .005. In other words, memory performances in the Language LD group were significantly lower on the trial involving both visual mode of stimulus presentation and response (Trial 1) compared to trials involving either verbal stimulus presentation or verbal response (Trials 2 and 3), or the trial involving both verbal stimulus presentation and response (Trial 4). Group 2 demonstrated the same pattern of performance in which Trial 1 was significantly lower than Trial 2 (mean difference = 1.71, p < .000), Trial 3 (mean difference = -.53, p = .001), and Trial 4 (mean difference = -.17, p = .003). Interestingly, the premature group that did not fall into one of the LD groups (Group 3) also showed a similar memory pattern, suggesting that this pattern may be more characteristic of prematurity itself rather than to type of LD.

Figure 1.

Figure 1

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Mean Color Span z-scores by trial and learning disability subtype.

Though BW means and variances were not significantly different between groups, BW remains a consistent and robust predictor of later outcomes in studies of prematurity. In order to demonstrate that the differences in memory outcomes between Groups 1 and 2 were not related to group differences in mean BW, we re-ran the above analyses (between-groups differences were analyzes with a MANOVA; within-groups differences were analyzed with repeated measures ANOVA) controlling for BW. The results of these analyses did not change after controlling for BW: in other words, results indicated no significant between-groups differences. Within-groups analyses indicated significantly lower Trial 1 (visual-visual) performances in both Group 1 and Group 2 relative to Trials 2, 3, and 4.

Discussion

We sought to examine whether patterns of neuropsychological functioning (or the presence of a deficit in language and/or perceptual-motor functioning) predicted patterns of memory performance in preterm children who were of broad average intellectual ability and free of neurosensory impairment. The results of the current study support previous findings of immediate memory deficits in preterm children at school ages (Briscoe et al., 1992; Hack et al., 1994). Observations of mean cognitive, achievement, and neuropsychological scores by subtype generally revealed relative deficits in verbal functioning, word reading, associative verbal fluency, and rapid color naming in Group 1 and relative deficits in nonverbal functioning, processing speed, rapid object naming, and visual-motor integration, fine motor speed/dexterity in Group 2. Observations also suggested generally lower test performances in Groups 1 and 2 compared to Group 3. These patterns are consistent with the LD classifications of Groups 1 and 2.

All three preterm groups, regardless of specific pattern of neuropsychological functioning, had significant difficulty on tasks of immediate memory. Moreover, within-group analyses of the LD subtypes indicated the poorest performances, regardless of LD subtype, for the trial involving both visual stimulus presentation and response (i.e., pointing). These findings are consistent with the results of prior studies that have compared immediate memory performance of verbal disorder and perceptual-motor subtypes of reading disabled children of least broad average intellectual ability who were free of neurosensory impairment (in addition to primary emotional/behavioral disorders), but were not born preterm (Wood et al., 1989). As in the current study, no significant differences in immediate memory performance by subtype were found in the Wood et al. (1989) study, which suggests that poor recall alone may characterize samples of preterm and reading disabled children, regardless of associated verbal and/or perceptual-motor deficits (i.e., LD subtype). Interestingly, performances in the Wood et al. (1989) study were also lowest for the visual presentation and visual response combination (Trial 1) in which the participant was not provided verbal labels for visual information (i.e., color names were not stated aloud by either participant or examiner). Failure to consistently activate verbal strategies for encoding and retrieving information, or impaired verbal mediation (often a sign of Dysnomia), may therefore underlie the memory deficits observed in both preterm and reading disabled groups.

Previous research has also suggested that the effect of Attention-Deficit/Hyperactivity Disorder (ADHD) and LD on memory performance is additive, resulting in more significant memory deficits (i.e., lower scores) than attention deficits alone (Johnson, Altmaier, & Richman, 1999). No significant differences in memory performance or computerized ratings of inattention and impulsivity were found among the three groups; however, observations of mean omission and commission z-scores revealed below-normative attention/concentration and impulsivity in both LD subtypes. Thus, it is possible that the combination of learning and attention deficits seen in prematurity results in lower, and potentially more variable, memory performances—though this would not account for the patterns observed in both LD groups in which performances were lowest for the visual presentation, pointing response combination (Trial 1). As with ADHD and reading disability, however, preterm status itself, rather than neuropsychological profile (or LD subtype), predicts memory impairment.

Other studies have found impaired memory performances in children with ADHD (see Douglas & Benezra, 1990). Comorbid ADHD and LD compound in an additive fashion (August & Garfinkel, 1989; Tarnowski, Prinz, & Nay, 1986). Research has generally shown that memory does not consistently differentiate between ADHD and LD groups. It is possible that similar patterns of memory impairment are found in ADHD and LD groups, but for different reasons (Sergeant & Van der Meere, 1990). For example, previous research has demonstrated immediate memory deficits in children with learning disabilities, both in children with developmental language weaknesses (i.e., Dysnomia and Dysphasia) and perceptual-motor deficits—though the hypothesized reasons for the memory deficits observed differ based upon the neurocognitive deficits associated with verbal and nonverbal disabilities, respectively. Children with language learning disabilities, for example, may not consistently utilize verbal strategies for coding or retrieval of visual information; children with perceptual-motor deficits, in contrast, may less efficiently process visual information in the absence of verbal cues due to deficits in perceptual or visual-spatial reasoning. As with ADHD and reading disability, however, preterm status itself, rather than neuropsychological profile (or LD subtype), predicts memory impairment.

It is possible that impairments in immediate memory in preterm samples are related to differences in speed of encoding or processing (Cheatham, Sesma, Bauer, & Georgieff, 2006). Cheatham, Bauer, and Georgieff (2006) found that infants who encoded the details of a stimulus more slowly (i.e., took more time to encode) performed more poorly during an “imitation protocol,” in which the length of time available for coding a sequence of events to be immediately recalled or reproduced is typically standardize across participants regardless of individual differences in encoding (or processing) speed. In another study, de Haan, Bauer, Georgieff, and Nelson (2000) found no group differences in immediate or 10 minute delayed recall, suggesting that preterm and full-term groups perceived and recalled the content of information to be remembered equally. When participants were required to imitate (i.e., recall) both the individual target actions and the order in which the actions were presented (i.e., sequence), however, differences between groups emerged. In other words, deficient recall in the preterm group relative to the full-term emerged as a function of increased cognitive complexity of the task.

The results of these studies suggest that preterm birth is not consistently associated with increased risk for impairments in memory functioning. Preterm birth is consistently associated with impairments in complex cognitive processes, such as those involving ordered recall (temporal sequencing) governed by numerous functional brain systems and necessitating both higher order cognitive processes (i.e., prefrontal cortex, temporal lobe) as well as more basic functions governed by relatively more primitive neural systems/structures (primary visual cortex/occipital lobe, hippocampus). Similar findings have also been observed using a ‘continuous familiarization paradigm’ (see Rose, Feldman, & Jankowski, 2002).

Subtle deficits in neurocognitive functioning have a significant impact on preterm outcomes, enhancing the risk for behavioral, learning/academic, and social-emotional problems—though the long-term outcomes of preterm birth are far from uniform and influenced substantially by both genetic and non-genetic factors occurring before, during, and long after the neonatal period. Patterns of neurocognitive deficit are also frequently obscured by differences in, for example, methodology and/or sample characteristics—as well as by the difficulties inherent in the study of long-term outcomes in any at-risk population. Furthermore, the risk factors for and consequences of preterm birth have implications for both phylogenetically older (e.g., hippocampus) and newer (e.g., prefrontal cortex) regions – regions which develop differently across the human lifespan and govern an enormously diverse range of human functions. The hippocampus and prefrontal regions appear to be particularly vulnerable to insults associated with preterm birth such as cardiopulmonary instability, metabolic changes, inflammation, physiologic stresses, and nutritional deficiencies. Recent research has posited enhanced dorsal stream vulnerability as a potential explanation for the patterns of weakness in spatial reasoning, attention, and executive function which often characterize the very premature and are commonly found in Williams Syndrome and other neurodevelopmental disorders (Atikinson & Braddick, 2011). Since prematurity, like Williams Syndrome, shows multiple cognitive deficits rather than a single, uniform pattern, speculation regarding functional connectivity remains difficult.

Limitations

Small group sizes and power limitations of the current study indicate the need for replication of these findings. Though this study did not specifically address inconsistencies in the literature with regard to visual versus verbal memory in preterm, the results do highlight the importance of considering both mode of presentation and mode of response in examining patterns and degree of memory impairment in preterm children.

Future Directions

Preterm children show deficits in executive functioning (or the process of planning, initiating, and sustaining goal-directed behavior and self-directing behavior and emotion), including attention, working memory, and inhibitory control (Anderson et al., 2004; Aylward, 2005; Bhutta et al., 2002; Harvey et al., 1999; Luciana et al., 1999; Stephens & Vohr, 2009; Taylor et al., 2000), visuo-spatial reasoning, and verbal reasoning and expression (Aylward, 2005; Breslau et al., 2001; Taylor et al., 2004). Recently, computerized memory training programs have been found to improve working memory performance on both trained and non-training memory tasks, improve response inhibition and reasoning, and reduce parent-rated inattentive symptoms of ADHD (Beck, Hanson, Puffenberger, Benninger, & Benninger, 2010; Klingberg, Fernell, Olesen, Johnson, Gustafsson, Dahlström, et al., 2005; Klingberg, Forssberg, & Westerberg, 2002). Functional neuroimaging studies with healthy adult subjects have also shown changes in cortical activity (i.e., increased activity in the middle frontal gyrus and superior and inferior parietal cortices) following working memory training (Olesen, Westerberg, & Klingberg, 2003; Westerberg & Klingberg, 2007).

Computerized verbal and visuo-spatial adaptive working memory training has also been associated with improvements in mathematical ability (Holmes, Gathercole, & Dunning, 2009). The effect of a working memory training program on a group of former extremely low BW (ELBW; <1000 g) adolescent females (n = 16) was recently investigated (Lohaugen, Antonsen, Haberg, Gramstad, Vik, Brubakk, & Skranes, 2010) using the Cogmed RM program developed by Klingberg et al. (2005). This study found significant improvements in memory in the preterm (intervention) group compared to the non-intervention group, though replication of these results with male and female former-preterm samples is warranted.

Conclusion

The current findings suggest that existing subtype criteria can be applied to groups of preterm children, but that a substantial proportion of VLBW preterm children may exhibit mixed patterns of neuropsychological (including memory) functioning that may be unique to prematurity. Future research is necessary to determine whether a priori diagnostic classification of preterm children according to learning disability subtypes could assist in the identification of preferred memory and learning strategies.

Acknowledgments

This publication was made possible by Grant Number UL1RR024979 from the National Center for Research Resources (NCRR), a part of the National Institutes of Health (NIH). Its contents are solely the responsibility of the authors and do not necessarily represent the official views of the CTSA or NIH and our PPG (NIH Program Project Grant P01 HL046925). We would also like to acknowledge the ICTS/CTSA CRU for their assistance with and support of this project.

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