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Developmental changes in performance on tests of purported frontal lobe functioning a

b

Harvey S. Levin , Kathleen A. Culhane , Joel b

b

Hartmann , Karen Evankovich , Audrey J. b

c

Mattson , Harriet Harward , George Ringholz e

, Linda Ewing‐Cobbs & Jack M. Fletcher

d

e

a

Division of Neurosurgery , The University of Texas Medical Branch , D‐73, Galveston, TX, 77550 b

Division of Neurosurgery , The University of Texas Medical Branch , c

The Greenery Rehabilitation Center ,

d

Transitional Learning Community ,

e

Department of Pediatrics , The University of Texas Medical School , Published online: 04 Nov 2009.

To cite this article: Harvey S. Levin , Kathleen A. Culhane , Joel Hartmann , Karen Evankovich , Audrey J. Mattson , Harriet Harward , George Ringholz , Linda Ewing‐Cobbs & Jack M. Fletcher (1991) Developmental changes in performance on tests of purported frontal lobe functioning, Developmental Neuropsychology, 7:3, 377-395, DOI: 10.1080/87565649109540499 To link to this article: http://dx.doi.org/10.1080/87565649109540499

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DEVELOPMENTAL NEUROPSYCHOLOGY, 1991, 7(3), 377-395 Copyright © 1991, Lawrence Erlbaum Associates, Inc.

Developmental Changes in Performance on Tests of Purported Frontal Lobe Functioning


Harvey S. Levin, Kathleen A. Culhane, Joel Hartmann, Karen Evankovich, and Audrey J. Mattson Division of Neurosurgery The University of Texas Medical Branch

Harriet Harward The Greenery Rehabilitation Center

George Ringholz Transitional Learning Community

Linda Ewing-Cobbs and Jack M. Fletcher Department of Pediatrics The University of Texas Medical School

To investigate developmental changes in performance on cognitive and memory tests purported to reflect frontal lobe functioning, 52 normal children and adolescents were studied including 17 children in the 7- to 8-year-old group, 17 children in the 9- to 12-year-old age range, and 18 adolescents who ranged from 13 to IS years. The tests included the Wisconsin Card Sorting Test, California Verbal Learning Test-Children's Version, Word Fluency, Animal Naming and Design Fluency, the Twenty Questions task, the Go-No Go task, the Tower of London, and Delayed Alternation. With the exception of Delayed Alternation, developmental changes were confirmed on all of the tests. Major gains were found primarily between the 7- to 8- and 9- to 12-yearold groups on Wisconsin Card Sorting measures and false-positive errors on the Go-No Go Task. However, further advances in performance in the 13- to 15-year-old age range were confirmed on the California Verbal Learning Test, Twenty Questions, and Tower of London. A principal components analysis revealed a three-factor solution, including a semantic association/concept formation factor, a freedom from perseveration factor, and a planning/strategy factor. Our findings encourage the application of these tests to children with frontal lobe lesions. Requests for reprints should be sent to Harvey S. Levin, Division of Neurosurgery D-73, The University of Texas Medical Branch, Calveston, TX 77550.


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The burgeoning interest in development of cognitive skills that are dependent on frontal lobe functioning can be traced to three areas of research. First, experiments involving dorsolateral frontal lesions in infant, juvenile, and adult monkeys have implicated a developmental progression in the functional commitment of this region to specific cognitive abilities (Goldman & Rosvold, 1970; Goldman-Rakic, 1987). Second, cognitive tasks of purported frontal lobe functioning have been derived from Luria's clinical reports and theoretical work (Luria, 1966) and administered to normal children in developmental studies (Passler, Issac, & Hynd, 1985). The developmental research by Passler et al. employed verbal and nonverbal tasks designed to produce proactive and retroactive interference. Third, recent findings concerning delayed response performance in normal human infants have closely paralleled the results obtained in adult monkeys with dorsolateral frontal lesions (Diamond & Goldman-Rakic, 1989). In this connection, Diamond and Goldman-Rakic (1989) showed that human infants-in the 7.5- to 9-month age range and dorsolateral-lesioned adult monkeys were able to remove the cover from one of two possible locations that was concealing a toy provided that no delay was imposed. However, as human infants matured and reached 12 months, they were able to perform the task with successively longer delays (e.g., as long as 10 sec at 12 months). In contrast, delayed response performance remained impaired in the adult monkeys with dorsolateral lesions. Cognitive tasks employed in previous studies of frontal lobe functioning in children can be generally classified as (a) downward extensions of measures originally designed to study adults and (b) tasks that were derived from developmental theory (Welsh & Pennington, 1988). Chelune and Baer (1986) argued that elucidation of growth curves prior to applying cognitive tasks to brain-injured children is perhaps more important than whether the measure was originally used with adults or conceptualized from a developmental perspective. We have collected developmental data in normal children on a series of tasks that include downward extensions of tests used to assess frontal lobe dysfunction in adults (Benton & Hamsher, 1976; Grant & Berg, 1948), measures derived from the developmental cognition literature (Denny & Denny, 1973), and that which are adaptations (Drewe, 1975) of techniques used by Luria (1966). The study reported here is in preparation for an investigation of children sustaining frontal lesions as a result of head injury. METHODS Subjects

The 52 children studied were chosen from a pool of families responding to an advertisement in a local newspaper. Children with learning difficulties

FRONTAL LOBE FUNCTIONS

379

TABLE 1 Summary of Demographic Characteristics and WISC-R Subtest Scores

Age (years)

M SD

Gender Race Parental education


Parental occupation

M SD M SD

7 to 8 Years'

9 to 12 rears*

13 to 15 Years*

7.47

11.06 1.07 53% female 47% male 71% White 29% Black 5.23 1.03 3.00 1.69

14.34

.60 53% female 47% male 76% White 24% Black 5.24 1.15 3.00 1.66

Similarities Picture Completion Block Design

'

P _

.88 56% female 44% male 89% White 11% Black 5.11 1.37 3.22 1.59

WISC-R Subtest Vocabulary

tf

M SD M SD

10.82 3.47 9.94 3.96

9.53 3.14 11.53 2.98

9.76 2.73 11.88 3.66

M SD M SD

11.29 2.76 10.17 3.83

11.59 2.67 10.70 2.97

12.06 4.76 10.94 2.92

.11

.95

1.65

.44

2.83

.95

11.33

.66

F value

P

.83

.44

1.44

.23

.20

.82

.24

.78

Note. Parental education was rated using a 7-point coding system ranging from preschool only (1) to postgraduate education (7). Parental occupation was rated using the Hollingshead Occupation Scale (1958). This scale ranges from executive/major professional (1) to unskilled manual/unemployment (7). •n = 17. *n = 18.

were excluded, as were those who had a history of neurological problems. Table 1 gives the demographic characteristics for each of the three age groups studied (7- to 8-year-olds, 9- to 12-year-olds, and 13- to 15-yearolds). As indicated, the groups did not differ in terms of distribution of gender, race, or levels of parental education and occupation. Parental occupational level was derived using the Hollingshead and Redlich (1958) occupation scale which rates occupations on a 7-point scale (Table 1). Parental education was also categorized using a 7-point scale. In addition, table 1 shows that the groups did not differ significantly in terms of their scaled scores on four subtests of the Wechsler Intelligence Scale for ChildrenRevised (WISC-R; Wechsler, 1974). Procedures Neuropsychological tests of problem-solving, memory, and conceptual ability were administered in a single 2- to 2%-hi session. This report focuses on data for the following tasks: delayed alternation (Freedman & Oscar-

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LEVIN ET AL.


Berman, 1986), verbal fluency (Benton & Hamsher, 1976), and design fluency (Jones-Gotman & Milner, 1977), California Verbal Learning Test-Children's Version (Delis, Kramer, Kaplan, & Ober, 1986), the Tower of London test (Shallice, 1982), the Go-No Go task (Drewe, 1975), Wisconsin Card Sorting Test (Grant & Berg, 1948), and the Twenty Questions test (Denny & Denny, 1973). The majority of administrations followed this standardized order, although there were a few exceptions due to equipment availability. Four subtests (Similarities, Vocabulary, Picture Completion, Block Design) of the WISC-R were administered after the specific cognitive and memory tests. Verbal and design fluency. Verbal fluency was assessed via the Controlled Oral Word Association test from the Multilingual Aphasia Examination (Benton & Hamsher, 1976). In addition, an animal naming task (1-min time limit) was administered to assess verbal fluency under semantic constraint. Similarly, the subject's ability to create abstract designs was assessed using the design fluency task of Jones-Gotman and Milner (1977). In the free condition of this task, the subject is asked to create as many different nonsense designs as he or she can; in the fixed condition, there is one additional constraint in that the subject's drawings must consist of four lines. The subject is allowed 3 min per condition. The examiner corrected the first error made by the child in each condition. The total number of correct drawings, as well as the number of perseverative and nonperseverative errors committed, are scored. Memory. The California Verbal Learning Test-Children's Version (Delis et al., 1986) was employed to assess the use of memory strategies and efficiency of memory. Five recall trials of a 15-word list including items belonging to three semantic categories (i.e., fruit, clothing, and toys) are administered. The test differs from the adult version, which involves recall of a 16-item list divided into four semantic categories (i.e., fruit, clothing, tools, and spices). Variables included in this analysis are the sum of words recalled over five trials, the percentage of responses that are clustered according to semantic category (e.g., recalling two or more items of clothing in a row), the percentage of perseverative responses, and the percentage of intrusion responses (i.e., words that were not on the examiner's list). Problem solving and concept formation. The Wisconsin Card Sorting Test (Grant & Berg, 1948) was administered on a microcomputer with an examiner present to assist in explaining the task. The instructions and test administration were given in a standard manner (see Heaton, 1981, for details). The measures analyzed in this study include the number of categories completed (0 to 6), the conceptual level of responses (i.e., all correct responses in the test that occurred consecutively in runs of three or more),


381

Initial Position Given to Patient


0

B

V FIGURE 1 Tower of London, modified after Shallice (1982), consists of colored beads (one blue, one green, one red) presented on three pegs of varying length. Beginning with a standard initial position, the child is asked to transfer the beads using the minimum number of moves necessary to reach the goal position displayed in the accompanying model.

perseverative errors (i.e., a response that would have been correct in an earlier stage of the test and that is considered an error according to the manual), and failure to maintain set (i.e., number of times in a task that the patient makes 5 correct responses in a row but fails to attain the 10 that are required to complete the category). The total number of conceptual level responses and the total number of perseverative errors were each divided by the total number of trials and expressed as a percentage. The Tower of London task (Shallice, 1982) makes use of three colored beads which can be placed on pegs of three different heights (see Figure 1). The subject is required to match the examiner's three-bead pattern in a prescribed number of moves. The problems are graded in difficulty, with the simplest problems requiring two moves and the most difficult requiring five moves. The subject must solve each problem within three trials or that problem is discontinued. The number of trials to solution and the latency to the first move, or initial planning time, is recorded for each problem. The initial planning time is summed over the 12 problems. Additional variables include the number of problems solved on the first trial and the average number of trials to solution.


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LEVIN ET AL.

FIGURE 2

Apparatus used for delayed alternation task.

The Twenty Questions procedure (Denny & Denny, 1973) follows the parlor game of the same name. The target stimuli are 42 hand-drawn color pictures presented on a large sheet of poster board. The pictures can be grouped into various categories (e.g., animals, tools, etc.). The subject is instructed to determine which item the examiner has chosen by asking as few yes-no questions as possible. The test is terminated when the subject has not guessed the target item on the 20th question. The subject's questions are categorized as constraint seeking, pseudoconstraint seeking, hypothesis seeking, redundant, or nonscorable. Constraint-seeking questions are those that refer to two or more pictures and eliminate several alternatives (e.g., Is it a living thing?), whereas hypothesis-seeking questions simply name one particular picture (e.g., Is it the hammer?). A pseudoconstraint-seeking question is similar to a hypothesis-seeking question in that it refers to only one picture, yet it is phrased like a constraint question (e.g., Does it bark?). The data were analyzed in terms of the percentage of each type of question used. The delayed alternation task (Freedman & Oscar-Berman, 1986) is a simple problem-solving task requiring an apparatus that consists of two drawers and a curtain that hangs between the subject and examiner to hide the drawers from the subject's view (see Figure 2). On each trial the subject must choose the drawer in which he or she believes a coin is hidden. If the choice is correct, the examiner moves the coin to the opposite drawer on the


383


next trial; if the choice is incorrect, the coin remains on the same side on subsequent trials until the subject makes the correct choice. Criterion is reached when the subject correctly identifies 12 alternations of the coin. Number of trials to criterion and number of errors are scored. Response modulation. The Go-No Go task (Drewe, 1975) is a computerized test of problem solving and inhibitory control. The test consists of a motor and a verbal condition. The verbal condition, which involves adding verbal responses to motor responses that have been established during the prior motor condition, is not considered in this analysis. The child must determine a rule for responding to 5 x 5 cm colored squares that appear on the screen (i.e., response to red squares, no response to blue squares). Each square is presented for 3 sec and response time is recorded for each trial on which a response is made. A minimum of 10 trials (including 4 red squares and 6 blue squares) is presented. A maximum of 40 trials is presented (including 18 red squares and 22 blue squares) before the task is discontinued. The order of presentation of stimuli was the same for all subjects, regardless of the number of errors made. Number of hits (correct responses to a red square) and false positive errors (incorrect responses to a blue square) are scored. A ratio of false positive errors (as described next) was also calculated. RESULTS Analysis of Developmental Changes

To assess the primary effects of age on performance, an analysis of variance (ANOVA) was conducted on each dependent measure separately, with age (three levels) serving as the between groups variable. A post hoc analysis using the Tukey's Studentized Range Test was computed for each measure to compare means between age group pairs. Table 2 summarizes the results of the ANOVA and Tukey's test procedures, indicating the means and standard deviations for each dependent measure across the three age groups, as well as the level of significance of between group differences. Problem Solving and Concept Formation

Wisconsin Card Sorting Test (WCST). Figure 3 plots the number of categories obtained (expressed in percentages), the percentage of conceptual level responses and perseverative errors as a function of age. A pattern is seen in which concept formation (i.e., number of categories obtained) and problem-solving efficiency (i.e., percentage of conceptual level responses) increases, whereas the percentage of perseverative errors diminishes with age. The largest developmental shift on these measures appears between the 7- to 8- and 9- to 12-year-old groups ANOVAs (Table 2) re-

TABLE 2 Means and Standard Deviations for Selected Frontal Lobe Measures 7 to 8 Years'


M Wisconsin Card Sorting Test 3.1 Categories obtained Percentage conceptual level responses 41.6 Percentage perseverative errors 18.2 Failure to maintain set 1.4 California Verbal Learning Test 46.1 Total recall trials 1-5 Percentage clustered responses 23.6 Percentage perseverations 19.2 Percentage intrusions 5.0 Fluency Measures (number of correct) Word fluency 15.9 Animal naming 14.4 Design fluency-free 8.4 Design fluency-fixed 7.7 Twenty Questions Task .Percentage constraintseeking questions 25.2 Percentage hypothesisseeking questions 62.9 Percentage pseudoconstraint-seeking questions 10.7 Go-No Co Task (motor condition) 14.2 Hits Correct rejections 10.9 . False alarms 12.0 5.2 Misses False-positive ratio .48 Tower of London Percentage solved on trial 1 52.9 Average initial Planning time 5.0 Average trials to solution 1.8 Delayed Alternation 23.7 Trials to criterion 22.0 Errors

9 to 12 Years'

13 to IS Yearf

SD

M

SD

M

SD

F(2, 46)

P

1.5'-1"

4.9

1.2'

5.4

1.3d

14.91