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Global — local processing in childrenprenatally exposed to alcoholSarah N. Mattson a , Laura Gramling a , Edward P. Riley a , Dean C.Delis b & Kenneth Lyons Jones ca Center for Behavioral Teratology , San Diego State University ,b Department of Psychiatry , University of California San DiegoSchool of Medicine and Psychology Service , San Diego, DVA MedicalCenterc Division of Dysmorphology and Teratology, Departaient ofPediatrics , UCSD Medical Center ,Published online: 24 Oct 2007.

To cite this article: Sarah N. Mattson , Laura Gramling , Edward P. Riley , Dean C. Delis & KennethLyons Jones (1996) Global — local processing in children prenatally exposed to alcohol, ChildNeuropsychology: A Journal on Normal and Abnormal Development in Childhood and Adolescence,2:3, 165-175, DOI: 10.1080/09297049608402249

To link to this article: http://dx.doi.org/10.1080/09297049608402249

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Child Neuropsychology 1996, Vol. 2, No. 3, pp. 165-175

0929-7049/96/0203- 165$12.00 0 Swets & Zeitlinger

Global - Local Processing in Children Prenatally Exposed to Alcohol*

Sarah N. Mattson', Laura Gramling', Dean C . Delis2, Kenneth Lyons Jones3, and Edward P. Riley' 'Center for Behavioral Teratology, San Diego State University, *Department of Psychiatry, University of Cal- ifornia, San Diego School of Medicine and Psychology Service, San Diego DVA Medical Center, 3Division of

Dysmorphology and Teratology, Department of Pediatrics, UCSD Medical Center

ABSTRACT

Fetal alcohol syndrome (FAS) is associated with a wide variety of cognitive deficits and behavioral prob- lems. Little is known, however, about the effects of prenatal alcohol exposure on visuospatial processing. Alcohol-exposed and normal control children were presented with visual hierarchical stimuli consisting of large (global) letters or shapes constructed from the arrangement of numerous smaller (local) letters or shapes. The children were asked first to recall the global-local stimuli and different single-level stimuli from memory and then to copy them. Alcohol-exposed children were impaired in recalling local features relative to global features. When the alcohol-exposed children attempted to copy the same stimuli, there was also a selective deficit in local but not global reproduction. A control condition indicated that the selective deficit in local processing was not due to a size effect per se. These results suggest that prenatal alcohol exposure does not result in a unitary visual-spatial impairment, but rather, is manifested as a selec- tive deficit in the visual processing of local (detail) features.

Fetal Alcohol Syndrome (FAS) results from ma- ternal alcohol abuse during pregnancy and is estimated to affect a t least 1200 children in the United States each year (Abel & Sokol, 1991). It i s characterized by a recognized pattern of facial anomalies, growth deficiency, and central ner- vous system (CNS) dysfunction (Jones, Smith, Ulleland, & Streissguth, 1973). This C N S dys- function may manifest itself as mental retarda- tion and/or other behavioral problems such as hyperactivity, attentional deficits, poor adaptive behaviors, and a range of cognitive deficits (Streissguth, 1986). Although over 20 years have passed since the recognition of FAS, the question still remains whether this disorder rep- resents a unitary decline in intelligence or whether there is a pattern of selective strengths

and weaknesses. S o m e studies (LaDue, Streiss- guth, & Randels, 1992; Streissguth e t al., 1991) but not all (Aronson, Kyllerman, Sabel, Sandin, & Olegiird, 1985; Janzen, Nanson, & Block, 1995; Mattson, Riley, Gramling, Delis, &Jones, 1996a) report that VIQ is typically lower than PIQ in children with FAS.

In the two decades since FAS was identified, most research has focused on general intellec- tual functioning and only recently have more specific neuropsychological results been re- ported. Overall I Q measures for this population have revealed FSIQ scores between 20-120, with average performance at around 70 (Abel, 1990). We recently compared children with doc- umented histories of heavy prenatal exposure with or without the typical facial features of

* This paper was supported in part by National Institute on Alcohol Abuse and Alcoholism grants AA10417 and AA03249 to EPR. The authors would like to acknowledge the assistance of Rachel Braithwaite, Kathleen John- son, and Larry Baum. Address correspondence to: Sarah N. Mattson, Ph.D., Center for Behavioral Teratology, 6363 Alvarado Court, Suite 209, San Diego, CA 92120, USA. Accepted for publication: May 27, 1996.

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166 SARAH N. MATTSON ET AL

FAS (Mattson, Riley, Grambling et al., 1996a). The mean FSIQ scores for these two groups were 74.4 and 83.6, respectively. The ranges of scores for these two groups were 40-103 and 64-1 12, thus attesting to the broad range of in- tellectual functioning in children with prenatal alcohol exposure.

Although most previous research focused on global abilities, several recent studies have doc- umented more specific cognitive disabilities. Neuropsychological studies have revealed defi- cits in language, visuospatial, and fine-motor skills in preschoolers (Janzen et al., 1995) and children (Conry, 1990; Mattson, Riley, Gram- ling, Delis, & Jones, 1996b) with FAS. Atten- tional deficits are also widely reported in these children (Coles, Raskind-Hood, Brown, & Silverstein, 1994; Nanson & Hiscock, 1990) and prospective studies have revealed that deficits in attention and short-term memory also occur fol- lowing exposure to lower levels of alcohol (Streissguth et a]., 1994a; Streissguth et a]., 1994b).

We recently assessed verbal learning and me- mory in 20 children with FAS (Mattson, Riley, Delis, Stem, & Jones, 1996a). When compared with controls matched for age, sex, and ethnic- ity, the children with FAS demonstrated deficits in both learning and recalling a 15-word list. However, given their reduced levels of learning, their retention was surprisingly intact. Specifi- cally, their pattern of recall suggested deficits in encoding verbal information and an impairment in response inhibition capabilities. A similar finding was reported in adults with FAS (Don, Kerns, Mateer, & Streissguth, 1993). Other stud- ies have noted deficits in the recall of stories, designs, and faces (Streissguth, Bookstein, Sampson, & Barr, 1989), and in working mem- ory (Kodituwakku, Handmaker, Cutler, Weathersby, & Handmaker, 1995). However, it is still unclear whether memory represents a specific deficit following prenatal alcohol expo- sure or is secondary to overall intellectual defi- cits.

Although rats exposed to alcohol prenatally are known to have deficits on tasks involving spatial abilities (Gianoulakis, 1990; Kelly, Goodlett, Hulsether, & West, 1988; Reyes,

Wolfe, & Savage, 1989), little is known about this cognitive domain in children with FAS. Streissguth and colleagues have reported deficits in spatial learning on the Stepping Stone Maze in 14-year-old children (Streissguth et al., 1994b). Additionally, at 7 1/2 years of age, a visuoconstructional task was one of the most sensitive measures of alcohol’s teratogenesis (Streissguth et al., 1989). Recently, Uecker and Nadel ( I 996) reported that children with FAS or fetal alcohol effects (FAE) were significantly impaired in delayed but not immediate recall of information involving spatial location. In an- other task, these children had difficulty with location but not object recall. That is, they were able to recall the items but not the spatial loca- tions of the items.

The task used in the current study, the Global-Local Test (Bihrle, Bellugi, Delis, & Marks, 1989), assesses visual hierarchical pro- cessing by requiring the subject to recall draw- ings consisting of large letters or shapes (the global form) made up of smaller letters or shapes (the local form). Using this test, investi- gators have documented that certain patient groups have selective deficits in recalling global (configural) visual information, whereas other patient groups show a selective deficit in recall- ing local (detail) visual information. For exam- ple, patients with focal brain damage in the left hemisphere tend to be impaired in recalling local features of hierarchical stimuli, whereas patients with damage to the right hemisphere are primar- ily impaired in recalling global information (Delis, Kiefner, & Fridlund, 1988). A similar dissociation has been documented in mentally retarded children who do not have focal brain damage. Children with Down syndrome were more impaired in local than global analysis, whereas children with Williams syndrome dis- played the opposite pattern. It appears that this difference in global-local processing is related to verbal and nonverbal abilities; children with Down syndrome are often more impaired in the verbal domain whereas children with Williams syndrome show greater impairment in spatial abilities (Bihrle et al., 1989).

In presenting the Global-Local Test, we were interested in whether the hierarchical nature of

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PRENATAL ALCOHOL AND GLOBAL-LOCAL PROCESSING 167

the stimuli would present a unique difficulty to the alcohol-exposed subjects as compared to the normal controls. Additionally, portions of this task allow for an assessment of whether deficits in hierarchical processing are more likely to oc- cur on a memory or perceptual level. Finally, while some studies may suggest otherwise, chil- dren with FAS, like children with Down syn- drome, may show greater deficits in verbal than nonverbal abilities and have higher Performance than Verbal IQ scores (LaDue et al., 1992). Based on the findings for children with Williams and Down syndromes, we hypothesized that children with prenatal alcohol exposure would show greater deficits in local than in global pro- cessing.

METHOD

Subjects Twenty-eight children participated in this project, 14 with verifiable histories of prenatal exposure to high doses of alcohol and 14 normal control chil- dren. The alcohol-exposed children were recruited through the California Teratogen Information Ser- vice at UCSD Medical School. Prior to behavioral testing, these children underwent complete dys- morphology examinations, at which time a diagno- sis was made. All alcohol-exposed children in- cluded in this study were diagnosed as having FAS (n = 12) or Prenatal Exposure to Alcohol (PEA; n = 2). The children with FAS clearly met all of the criteria established by the Medical-Scientific Forum of the American Medical Society on Alco- holism and the Research Society on Alcoholism (Rosett, 1980). The PEA cases did not meet the standard criteria for an FAS diagnosis, although they had verifiable alcohol exposure histories. Be- cause of the retrospective nature of the diagnoses in most of these cases, the exact amounts of alco- hol consumed by the mothers of these children is not known. However, it was well documented that the mothers were chronic alcoholics and were con- suming large amounts of alcohol during their preg- nancies. In addition, because of the lack of pro- spective data on these alcohol-exposed subjects, little is known about other substances to which they may have been exposed. In five (35.7%) of the alcohol-exposed children, other exposures were suspected. In two cases, the mothers smoked ciga- rettes (approximately I pack per day); in three cases, intravenous drug use was suspected.

The alcohol-exposed and control groups were matched for age (range = 9-16; mean = 12.6 years) and sex (6 females, 8 males in each group). Chil- dren were not matched for socioeconomic status because this information was only available for 71.4% of them. However. an analysis of these data indicated that although there was a trend for the control group to be of a higher socioeconomic level, the difference did not reach statistical sig- nificance (p > .05). The control subjects were screened for prenatal exposure to teratogenic or potentially teratogenic substances. Generally, mothers of the control subjects reported little if any alcohol consumption during pregnancy.

The Global-Local Test (Bihrle et al., 1989) was administered as part of a larger battery of neuro- psychological tests that also included the Wechsler Intelligence Scale for Children-Revised (WISC-R; Wechsler, 1974). Full Scale IQ scores for each child were obtained within a maximum of 1 month of administration of the Global-Local Test. The Full Scale IQ scores for the alcohol-exposed chil- dren ranged from 41-91 (mean = 70.9, SD = 16.08), and for the normal control children scores ranged from 88-1 33 (mean = 1 12.5, SD = 12.45).

The Global-Local Test

Stimuli There were 10 hierarchical stimuli, each of which consisted of a large “global” symbol made up of smaller ‘‘local’’ symbols (see Figure 1) presented on standard white paper (8.5 in. x 11 in.). In addi- tion, 8 single-level stimuli were used which con- sisted of only one small or one large figure similar in size to those used in the hierarchical stimuli. This condition was included in the study to deter- mine if selective deficits in global or local analysis were related to size effects per se. All figures con- sisted of letters or shapes and were easily identifi- able by all of the children.

Procedure The test consisted of three conditions: recall of hierarchical stimuli, recall of single-level stimuli, and copy of hierarchical stimuli. In the first condi- tion, 10 hierarchical stimuli were presented indi- vidually for 5-s duration. Five seconds after each stimulus was removed, the subject was asked to draw it from memory. The second condition was similar except that the stimuli consisted of 8 single-level figures. Finally, the subject was asked to copy 2 of the original hierarchical stimuli. Dur- ing this phase, the stimuli were placed on the table in front of the child.

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168 SARAH N. MATTSON ET AL.

Scoring Global and local figures in each stimulus were scored independently based on criteria described in Delis et al. (1988). Briefly, each figure received 3 points for recognizability and 2 points for accu- racy, for a maximum total (Global + Local) of 10 points. A figure was considered recognizable if three quarters of the figure resembled the original global or local stimulus. Accuracy was defined as: (1) few omitted or extra features; (2) relatively accurate proportions; and (3) orientation within 45" with no extreme distortion. Scoring did not reflect artistic ability or talent. For example, in the case where the global stimulus was drawn correct- ly, but contained no local elements and was simply a solid line or connected lines, it was given a total score of 5 (3 points for recognizability of the global feature, 2 points for accuracy of the global feature, and 0 points for the local stimuli). Two judges scored all tests independently. There was little difference between the two independent rat- ers of the drawings, and a Pearson's product-mo- ment correlation for data from the two raters was highly significant ( r = .99, p < .0001).

Analyses Results of the hierarchical and single-level recall and copy conditions were analyzed separately by 2 x 2 analyses of variance (ANOVA) with group (alcohol-exposed or controls) as a between-sub- jects factor and level (global or local ) as the within-subjects factor.

RESULTS

Examples of the Hierarchical Stimuli Prototypical examples of the drawings of chil- dren with FAS are shown in Figure l and illus- trate their difficulty in drawing local figures. In fact, when the subjects prenatally exposed to alcohol were asked to recall hierarchical forms, the local figures were frequently omitted from their drawings or were inaccurate andlor unrec- ognizable.

Recall of Hierarchical Stimuli The group of children with alcohol exposure histories had difficulty recalling the hierarchical stimuli, and this difficulty appeared to be due to a deficit in processing the local but not the glo- bal stimuli (see Figure 2). This was supported by

a significant interaction between group and hier- archical level (F (1,26) = 5.89, p < .05). Follow- up Newman-Keuls tests indicated that the alco- hol-exposed group differed from the controls at the local (p < .05) but not the global level. The analysis also indicated significant main effects of group (F( 1,26) = 1 6 . 9 5 , ~ < .001) and hierar- chical level (F( 1,26) = 9.59, p < .01). Interest- ingly, one element that appeared to interfere with the accurate processing of local features was a tendency for the alcohol-exposed children to be perseverative when they did draw local figures. This perseverative tendency did not, however, interfere with their reproduction of the global features, nor was it present in the draw- ings of the normal controls (for an example, see Figure lc).

Recall of Single-Level Stimuli Children exposed to alcohol prenatally were also less able to recall single-level stimuli in general (see Figure 3). A 2 x 2 ANOVA, with group and stimulus size (large vs. small) as variables, indi- cated that the children in the alcohol-exposed group were less able than controls to recall these stimuli (F( 1,26) = 5.44, p < .05). However, there was no difference due to size of the stimuli, nor was there a significant interaction between group and size on single-level recall (p's > .05). Thus, the selective deficit in local analysis found with the hierarchical stimuli could not be attributed to a size effect per se.

Copy of Hierarchical Stimuli Alcohol-exposed children were also impaired at copying global-local stimuli. As in the recall component, the impairment appeared to lie at the local level. This is supported by a significant Group x Level interaction (F( I .26) = 7.54, p < .05) in the 2 x 2 ANOVA, with level as the within-subject variable. Follow-up Newman- Keuls tests revealed that the alcohol-exposed group was impaired at the local level (p < .05) but not the global level. In addition, significant main effects of group (F(1,26) = 10.05, p < .01) and hierarchical level (F( 1,26) = 12.46, p < .05) were also found (see Figure 4).

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PRENATAL ALCOHOL AND GLOBAL-LOCAL PROCESSING 169

Y Y Y Y Y

Y Y Y

Y Y Y Y Y Y

Y

E 0 0

0 0 0 0 0 0 0 0

F

G

0 H

Fig. 1 . Two examples of hierarchical test stimuli (A & E), and drawings of one normal control (B & F) and two alcohol-exposed children (C, D, G, & H).

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170 SARAH N. MATTSON ET AL.

50 - 40-

30 -

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Fig. 2.

5 -

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Fig. 3.

Global Local Level

0 Control

Recall of hierarchical stimuli by alcohol-exposed and normal control children (* = p < .05).

-I- I-

Global IAcal Level

Recall of single-level stimuli by alcohol-exposed and normal control children.

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PRENATAL ALCOHOL AND GLOBAL-LOCAL PROCESSING 171

10 -

8-

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0 Global Local

Level

Copy of hierarchical stimuli by alcohol-exposed and normal control children (* = p < .05).

Intelligence Quotient and Global-Local Performance In order to evaluate the relationship between level of psychometric intelligence and perfor- mance on the Global-Local Test, Spearman rank correlations were performed. A combined global-local score was computed by adding the two scores together. The children with histories of prenatal exposure to alcohol exhibited a high correlation between their performance on the Global-Local Test and their Full Scale IQ ( @ = .79, p < .Ol) . In the normal control group, this correlation did not reach significance ( @ = .35, p > .05), although this may have been due to a ceiling effect in the global-local performance of this group.

DISCUSSION

This study demonstrated a possible dissociation of visuospatial processing in children exposed to alcohol prenatally. When compared to an age- and sex-matched group of normal control chil- dren, the alcohol-exposed group was impaired in processing local but not global features of visual hierarchical stimuli.

One possible explanation for these results is that the alcohol-exposed children might simply have problems with the smaller size of the local stimuli. However, these children were not dif- ferentially impaired in recalling either small or large stimuli in the single-level condition (i.e., when either individual small or individual large stimuli were presented alone). Thus, the impair- ment in recall of the local stimuli was due to the hierarchical relationship of the stimulus compo- nents and not to their absolute size.

Another possibility is that the local process- ing deficit in the alcohol-exposed group is the result of an overall impairment in memory. Cer-

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172 SARAH N. MATTSON ET AL

tainly, memory impairments following prenatal alcohol exposure could result in similar findings on this measure. However, the differential im- pairment in local but not global processing in both the perceptual (copy) and memory stages of processing suggests that this is not the case. Thus, children with prenatal alcohol exposure are more impaired in local than global analysis of hierarchical visual stimuli, and this deficit is independent of the memory deficits usually as- sociated with such exposure.

A third explanation for the local processing deficit is that an attention-motivation impair- ment may be interfering with the ability to draw the hierarchical stimuli. Children with FAS are frequently described as having attentional defi- cits (Nanson & Hiscock, 1990). However, if the current findings were simply the result of atten- tional or motivational factors, then one might have expected an overall deficit in the alcohol- exposed subjects under all testing conditions. This was not the case because they tended to perform in the normal range in copying and re- calling the global stimuli.

These three factors (perception, memory, at- tention) may all be involved in the Global-Local Test. In addition, other skills are likely to be involved. For example, a deficit in the ability to shift perceptuaVattentiona1 sets might interfere with successful completion of the task. That is, the alcohol-exposed subjects might have attend- ed first to the global features of the stimuli and then were unable to shift their attention to the local features, given the limited exposure time. This is clearly a possibility and may be related to neuroanatomical reductions in the cerebellar vermis in children with FAS and PEA (Sowell et al., 1996). This area of the brain has been impli- cated in the shifting of attention (Courchesne et al., 1994).

Another feature noted in the reproductions of the alcohol-exposed subjects was the tendency to perseverate when drawing the local features. This tendency may be suggestive of a deficit in executive functioning or, more specifically, in response inhibition. This type of deficit is con- sistent with previous reports of perseverative behavior in children (Driscoll, Streissguth, & Riley, 1990; Martin, Martin, Lund, & Streiss-

guth, 1977; Mattson, Riley, Delis, Stern, & Jones, 1996a) and animals (Riley, Lochry, & Shapiro, 1979) exposed prenatally to alcohol. In addition, perseverative behavior may be related to dysfunction of the frontal-subcortical brain systems. Interestingly, children exposed to alco- hol prenatally show reductions in the volumes of the basal ganglia (Mattson et al., 1994; Mattson, Riley, Sowell et al., 1996b).

In an investigation of adults with unilateral brain damage, Delis et al. (1988) found evidence of a fractionation in visuospatial component pro- cesses. Individuals with left hemisphere damage exhibited difficulty processing local figures, whereas individuals with right hemisphere dam- age exhibited difficulty processing global fig- ures. Do the present findings of a selective defi- cit in local processing in children with prenatal alcohol exposure suggest that these children have predominantly left hemisphere involve- ment? Because children in the alcohol-exposed group likely had abnormal brain development, the general “adult” rules of lateralization of cognition may not apply. However, in other glo- bal-local studies conducted with children with Williams and Down syndromes, relationships were found between visual hierarchical process- ing and other cognitive functions (Bihrle et al., 1989). Children with Down syndrome exhibited a primary deficit in local processing, and their verbal skills were typically lower than their spa- tial abilities. In contrast, children with Williams syndrome exhibited a primary deficit in global processing, and their spatial skills were usually more impaired than were their verbal skills. In- terestingly, children exposed to alcohol prena- tally may have lower verbal than spatial skills (LaDue et al., 1992). In our alcohol-exposed group, for example, the mean difference be- tween WISC-R Performance IQ and Verbal IQ was 8.7 points (PIQ > VIQ), which provides further support of a relationship between local processing and verbal abilities.

The differential performance by children with Williams syndrome and Down syndrome also raises the question of whether diminished intel- lectual ability has an effect on the global-local processing assessed here. The children in the present study were matched only for chronologi-

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cal age, not mental age. Alcohol-exposed chil- dren are known to have lower intelligence levels than the general population. Our alcohol-ex- posed subjects varied in Full Scale IQ from Low Average to Mentally Deficient, whereas our nor- mal controls varied from Low Average to Very Superior, according to the traditional classifica- tion of WISC-R scores. This lower overall func- tioning might have played a role in the poor visuospatial performance of the alcohol-exposed children and their local processing deficit.

However, the question remains whether this local processing deficit is a direct result of lower overall functioning or represents a specific weakness. It is clear from the studies of children with Down and Williams syndromes that intel- lectual deficiency is not sufficient, in itself, to cause a specific pattern of deficits in visuo- spatial processing. Therefore, although having general deficits in visuospatial processing might be related to reductions in overall ability, the specific nature of the deficit is probably related to other factors. More specifically, it is unlikely that the local processing deficit displayed by the alcohol-exposed children in the current study is due solely to a general intellectual deficit. Nev- ertheless, in the future it might be beneficial to include a comparison group of children with equivalent intelligence levels.

Thus, it is unlikely that a general reduction in intellectual ability is the sole or even a sufficient cause of the local processing deficit noted in this group of alcohol-exposed children. However, this pattern of weakness may be related to other strengths and weaknesses exhibited by alcohol- exposed children. As mentioned, there is some suggestion that in children with FAS, VIQ is more affected than PIQ. Although this was true for the current group of children, several other research groups, including our own, have not always shown this discrepancy. Beyond this VIQ-PIQ discrepancy, information is starting to emerge that suggests that FAS is not related to a unitary decline in cognitive functioning but, in- stead, may best be represented as a pattern of weaknesses and relative strengths. For example,

both children (Mattson, Delis et al., 1996a) and adults (Don et al., 1993) with FAS displayed impaired learning but relatively intact memory for verbal information. And on a spatial memory test, children with FAS displayed normal imme- diate, but impaired delayed, recall (Uecker & Nadel, 1996). In addition, the results from the current study suggest that prenatal alcohol expo- sure is related to impairments in local but not global visuospatial processing.

Finally, it is interesting to note that the two children included in this study who did not have enough of the traditional features to warrant a diagnosis of FAS also demonstrated the deficit in local processing. In fact, the performances of these two children were similar to the average performance of the alcohol-exposed group as a whole. Thus, it appears that even in the absence of full FAS, high levels of prenatal alcohol ex- posure can affect visuospatial functioning. In contrast, an inspection of the data revealed that the alcohol-exposed children with other sus- pected exposures performed similarly to the other alcohol-exposed subjects.

In summary, this study assessed the visuo spatial functioning of children with prenatal ex- posure to alcohol. The results indicate that these children have specific deficits in processing lo- cal stimuli. This deficit was present in both the memory and visuoconstructional conditions of the global-local task. Furthermore, although overall deficits on the Global-Local Test might be influenced by lower intellectual ability in the alcohol-exposed children, the specific nature of the deficit (i.e., local processing) is probably related to other factors. The nature of the local processing deficit displayed here may have im- portant ramifications for the development of educationallvocational training programs de- signed specifically for children with FAS and PEA. For example, training programs designed to assist alcohol-exposed children should con- tain ways to encourage systematic processing of visual information, so that children do not ne- glect to perceive details in information pre- sented visually.

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