0 145-6008/98/2202-0279$03.

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Ai.coi~oiI \ M : CI INICAL AND EXrl KIM1 N I A I

Vol. 22, No. 2

April 1998

Rl-sZ~Rcl1

A Review of the Neurobehavioral Deficits in Children

with Fetal Alcohol Syndrome or Prenatal Exposure to
Alcohol
Sarah N. Mattson and Edward P. Riley

of children of alcoholic parents, particularly alcoholic

mothers. . . . This report went virtually unnoticed in the
United States until 1973, when Seattle dysmorphologists
documented similar findings3and defined a specific pattern
of malformations in children born to chronic alcoholic
women as fetal alcohol syndrome (FAS).4
More than 20 years later, it is estimated that FAS affects
approximately 0.29 to 0.4SilOOO live born children. Prevalence estimates vary depending on socioeconomic and ethnic factors, and those that include Native American populations report incidences of up to 2.99/1000 births. In the
HROUGHOUT HISTORY, the negative effects of United States, at least 1200 children are born each year
maternal drinking on offspring have been suspected. with FAS, and the annual cost associated with caring for
Aristotle has been quoted as saying that foolish, drunken, such infants is estimated at 74.6 million dollar^.^ These
or hare-brain women, for the most part bring forth children estimates are strictly limited to those children who meet the
like unto themselves, morosos et Zanguidos, and in clinical criteria for FAS and do not include the spectrum of
Carthage and Sparta, laws prohibited the use of alcohol by effects caused by prenatal alcohol exposure. It is obvious,
newlyweds presumably to prevent conception during intox- however, that the effects of alcohol use during pregnancy
ication. During the gin epidemic in England, in the first are widespread and devastating, and that these problems
half of the 18th century, physicians warned against alcohol are entirely preventable.
consumption during pregnancy, claiming this was the cause
The effects of prenatal alcohol exposure fall on a conof weak, feeble, and distempered children. Such beliefs tinuum with FAS and perinatal death at one end and
continued until the early 20th century. In the postprohibi- relative normalcy on the other. Between these two endtion medical community, however, the idea that alcohol points are a variety of behavioral and physical features that
taken during pregnancy could be harmful to the developing are termed fetal alcohol effects (FAEs) or alcohol-related
fetus was dismissed as moralism. It was thought that harm- birth defects. The wide range of behavioral and cognitive
ful effects noted in the offspring of alcoholic women were effects associated with prenatal alcohol exposure is reprethe result of constitutional factors that also were the cause sentative of the continuous nature of alcohols behavioral
of the alcohol problem. It was not until the late 1960s and teratogenicity. Importantly, FAS represents only one point
early 1970s that interest in the adverse effects of alcohol on the continuum, and the effects of in utero alcohol
was renewed. In 1968, a group of French researchers pub- exposure on children without FAS should also be assessed.
lished the results of a study of 127 children of alcoholic
In the offspring, the diagnosis of FAS is based on a triad
parents.2 They reported the highly distinctive appearance
of features: (1) pre- and/or postnatal growth deficiency; (2)
a pattern of craniofacial malformations; and (3) central
From the Center for Behavioral Teratology, Department of Psychology, nervous system (CNS) dysfunction. Babies born with FAS
San Diego State University, San Diego, California.
are often small for gestational age4 and continue to show
Presented at the 1996 Borchard Foundation Symposium on the Behavioral
evidence
of growth deficiency.6For example, in a sample of
Effects in Children following Prenatal Alcohol Exposure, Missillac, France,
adolescents and adults with FAS, the mean height and
July 28-30, 1996.
This work was supported by the National Institute on Alcohol Abuse and weight were 2.1 and 1.4 standard deviations below the
Alcoholism Grant AA10417 and AA10820.
population mean, re~pectively.~
The pattern of craniofacial
Reprint requests: Sarah N. Mattson, Ph.D., Center for Behavioral Teramalformations
includes
microcephaly,
short palpebral fistolog?! 6363 Alvarado Court, Suite 209, San Diego State University, San
sures,
a
long
smooth
philtrum,
a
thin
vermilion border,
Diego, CA 92120.
epicanthal
folds,
and
flat
m
i
d
f
a
~
e
The
.
~
CNS
dysfunction is
Copyright 0 1998 by The Research Society on Alcoholism.
Fetal alcohol syndrome is a devastating developmental disorder
caused by prenatal exposure to high amounts of alcohol. In addition
to structural abnormalities and growth deficits, fetal alcohol syndrome is associated with a broad spectrum of neurobehavioral
anomalies. This paper reviews the behavioral and cognitive effects of
prenatal alcohol exposure. More than 20 years of research are discussed, with a focus on 10, activity, attention, learning, memory,
language, motor, and visuospatial abilities in children prenatally exposed to varying amounts of alcohol, including those with fetal alcohol syndrome.
Key Words: FAS, PrenatalAlcohol Exposure, Brain Function, Neuropsychological Effects.

Alcohol Clm Exp Res, Vol22, No 2, 1998: pp 279-294

279

MATTSON AND RILEY

280

Table 1. IQ Scores of Individual Cases of FAS or Alcohol-Exposed Individuals Reported in the Literature, Presented in Chronological Order Through 1996
_

Authors
Jones, Smith, Ulleland, 8 Streissguth3

Palmer, Ouellette, Warner, 8 Leichtman

Root, Reiter, Andrioia, 8 Ducken

Tenbrinck 8 B ~ c h i n ~
Ko~sseff~
Char
Mulvihill Klimas, Stokes, 8 Ri~emberg~
Bierich, Majewski, Michaelis, 8 Tillner40
Majewski, Bierich, Loeser, Michaelis, Leiber, 8
Bette~ken~
Ijaiya, Schwenk, 8 Gladtke14

Van BiervlietS5
Fryns, Deroover, Parloir, Goffaux, Lebas, & Van Den
Berghe 42
Dehaene, Walbaum, Titran, Samaille-Villette,
Samaille, Crepin, Delahousse, Decocq, Delacroix,
Caquant, 8 Q ~ e r l e u ~ ~

Koranyi 8 CsikyiiZ

Neidengard, Carter, 8 Smith

Ballesta 8 Cruz17
Slavney 8 Grau
Qazi, Masakawa, Milman, McGann, Chua, 8 HalleP

Qazi, Madahar, Masakawa, 8 McGann

Maller, Brandt, & T y g s t r ~ p ~ ~
Shaywitz, Caparulo, 8 Hodgson l 3

losub, Fuchs, Bingol, Stone, 8 G r ~ m i s c h ~ ~

Naselli. De Toni. Vianolo. Di Battista. 8 AicardP4

Age
14m
3m
57m
46m
40m
48m
34m
3yl Om
14.5m
22m
14.5m
22m
14.5y
11.7~
11.oy
9.9y
2y4m
3y5rn
1l Y
6m
NfA
5Y
3y7m
6y2m
7y9m
6y6m
lY
2y6m
15Y
1 6 ~
21Y
31-17
6m
7m
1Om
I am
26m
13Y
4y6m
7y3m
llm
21m
16Y
1lY
1OY
15Y
7Y
8Y
4y6m
7Y
6Y
16m
3yl m
4y4m
4yl Om
9Y
13Y
17Y
1OY
17Y
1am
4Y
6~
8y6m
6v6m

Tests

1 (case 1)
1 (case 2)
1 (case 3)
1 (case 4)
1 (case 6)
1 (case 7)
1 (case 8)
1 (case 1)
1 (case 2)

Bayley MDI
Bayley MDI
Stanford-Binet
Stanford-Binet
Stanford-Binet
Stanford-Binet
Bayley MDI
Stanford-Binet
Bayley MDI

1 (case 3)

Bayley MDI

1 (KC)
1 (AC)
1 (PC)
1 (RC)
1
1
1
1 (case 5)
1 (case 2)
1 (case 5)
1 (case 23)

NfA

1 (case 1)

HAWIK
(German WISC)
Stanford-Binet
Stanford-Binet
Griffith

1 (case 3)
1 (case 4)
1

1 (case 2)
1 (case 3)
I (case 4)
1 (case 7)
1 (case 10)
1 (case 11)
1 (case 12)
1 (case 13)
I (case 14)
1 (case 1)
1 (case 2)
1 (case 3)
1 (case 4)
1 (case 5)
1 (case 2)
1 (case 1)
1 (case 2)
1
1 (case 1)
1 (case 2)
1 (case 3)
1 (case 4)
1
1
1 (case 1)

1 (case 1)

1 (case 2)
1 (case 3)

Cattell
NIA
NfA
Cattell
Kramer
Kramer

NfA

Brunet-Lezine

NfA

N/A
N/A
WISC-R
NIA

Merrill-Palmer
Cattell
NfA
Leiter
NIA
NIA
WAlS
N/A
WAlS
Bayley MDI
Stanford-Binet
WlSC
WlSC
WlSC

IQ estimatet

Comments

59
83
75
57
79
70

150
65
56
76
59
70
80
75
112
68
36
75
85
41
93
84
105

76
a7
54
52
65
52
35
25
37
75
58
50
60
72
59
82
54
72
73
33
70
55
66
52
70
65
74
68
50
45
68 P a )
69 (DQ)
120
70

a0
67
60
72
50
50
50
50
46

Twins placed in foster home between

testings

Siblings; case PC had fewer

dysrnorphic features

Not identified as FAS by author$

Noonan syndrome

AEIf

Klippel-Feil malformation
Chromosomal abnormalities$
Schizophrenia
Renal anomalies

Chromosomal abnormalities$
Language disordered+

Siblings

NEUROBEHAVIORAL FINDINGS IN FAS

281

Table 1. Continued
Authors

Age*

Ticha, Santavy, & Matlochaz3

3Y
3Y
5m
4Y
<3Y
<3Y
4Y
6y2m
6y4m
<lY
1OY
4y9m
8Y
4Y
14Y
3Y
13Y
4Y
14Y
3Y
13Y
<lY
1OY
4Y
14Y
17m
5yl Om
5y4m
1Oy3m
2y2m
5yllm
12Y
14Y
1 6 ~

Tests

IQ estimate7

Comments

Aronson & OlegPrdZ4

Streissguth, Clarren, & Jones

Usowicz, Golabi, & Curry6

Marcus

Mattson, Riley, Jernigan, Ehlers, Delis, Jones, Stern,

Johnson, Hesselink, & B e l l ~ g i ~ ~
Mattson, Riley, Jernigan, Garcia, Kaneko, Ehlers, &
Jones45
Harris, MacKay. & O ~ b o r n ~ ~

Ernhart, Greene, Sokol, Martier, Boyd, & Ager23

41-17
6.5m
12m
19m
25m
9m
13.5m
20m
7m

1 (case 1)
1 (sib of C1)
1 (case 2)
1 (case 5)
1 (sib of C5)
1 (case 6)
1
1
1 (case 2)
1 (case 3)

Terman-Merrill
Terman-Merrill
Brunet-Lezine
Terman-Merrill
Brunet-Lezine
Brunet-Lezine
Terman-Merrill
N/A
Bayley MDI,
WISC, WISC-R,
Stanford-Binet,
or WPPSI*

1 (case 4)
1 (case 6)
1 (case 7)
1 (case 8)
1 (case 9)
1 (case 11)

1 (case 3)
1 (case 1)
1 (case 2 )
1 (case 3)
1 (case 4)
1 (case 5)
1 (case 1)
1 (case 2)
2 cases
with PEA
1 (case 1)

Bayley MDI
NIA

WISC-R
WISC-R
Bayley MDI

1 (case 2)

1 (case 3;
FAE)

13m
17m
25m
3y.4ylOm case 1
case 2
case 3
case 4
case 5
case 6
case 7
case 8

Stanford-Binet.
WPPSl

80
50
50 (DQ)
50
60-70 (DQ)
50 (DQ)
55
70
76
83
86
66
76
47
48
68
81
60
57
50
80
43
40
30
20
50
50
100
55
95
85
51
41
64, 69

89
77
<50
<50
69
<50
50
<50
81
57
63
54
95, 94
105,87
79,95
65, 79
83,87
78, 101
98, 87
50,25

Siblings of patients also were alcoholexposed and had at least some

features of FAS, if not frank FAS

Laryngeal web

Agenesis of corpus callosum

All three cases displayed autistic

behaviors

Testing at earlier dates also reported*

N/A, not applicable; sib, sibling.

* m, months: y, years.
t IQ estimates in italics are included in the mean (see text for details).
See text for details.
9 W, developmental quotient.
# Some of these cases overlap with Jones, Smith, Ulleland, & Streissguth (1973) listed above; however, since the 1973 publication, the normative data for the
0 scores for cases 3, 4, 6, and 7.
Stanford-Binet have been revised, which explains the revised 1

variable and can present as hyperactivity, attention deficits, leading known cause of mental retardation in the Western
world. The average IQ of children with FAS falls close to
learning disabilities, or mental retardation.
In
Although the diagnosis of FAS does not require frank 70, although the range is quite large (e.g., 20 to
exposed
children
who
do
not
meet
the
criteria
for
FAS,
mental retardation, intellectual capacity is very often compromised in these children. In fact, FAS has been called the some of the previously mentioned features may still be

282

MATTSON AND RILEY

Table 2. IQ Scores for Groups of Alcohol-Exposed Subjects Reported in the Literature, Presented in Chronological Order Through 1996
Authors

Age

Streisguth & R o h s e n o ~ ~ ~ * ~

8m
4Y
7Y
Dehaene, Samaille-Villette, Samaille, Crepin, NIA
Walbaum, Deroubaix, & B l a n ~ - G a r i n ' ~ ~ ' ~
9m-2.5y
Streissguth, Herman, & Smith26^Rb
2.51-5y
6-1 5y
20-21 y
Streissguth, Herman, & Smith54'R"
7m-21y
21m-22y
M a j e ~ s k i ~ ~ . Majewski
~ ~ . ' ~ ~&f ~ ;
5-9Y
Maje~ski"~~

5
10
3
2
17

Bayley MDI
Stanford-Binet
WISCNVISC-R
WAlS
Bayley MDI, Stanford-Binet,
WISCNVISC-R, or WAlS
Kramer IQ test

15-63
47-99
60-1 05
57-67
15-99
10-96
50-95
47-1 02
61-130

NIA

47.4
68.9
84.7
62
66
67
66 (AE Ill)
79 (AE II)
91 (AE I)
<70n = 9
70-85 n = 19
98.2

82-1 13

98
101
109
114
116
116
NIA

64-150+

4-25y

NIA

15

Streissguth, Barr, Martin, & Herman39*P

Em

losub, Fuchs, Bingol. & G r o m i ~ c h ~ " ~

1day-23y

10 (AAP 2 4)d
12 (AAP 2 3)
25 (AAP 2 2)
97 (AAP 2 1)
365 (AAP < 1)
216 (AAP 5 0.10)
63

Golden, Sokol, Kuhnert, &

Steinhausen, Nestler, & Spohr'

3-1 5y

12
32

Aronson & Oleglrd'32*R

6y3m (SD = 34m) 32

8y7m (SD = 15m) 16
1y6m-7y
13 pairs
7-9y
8 pairs
12m
25 total
(AAP 2 1.0)
(AAP < 1.0)
(AAP c 0.1)
6m
22 (cont. drinking)
11 (stopped drinking)
27 (never drank)
2.5-3oy
95

Fried & Watkir~son~'*~"

12m

Coles, Smith, 8 Falek66*P

10 (AA > 0.85)B

116 (AA < 0.14)
8 (AA > 0.85)
71 (AA < 0.14)
421

24m
Streissguth, Barr, Sampson, Darby, &
Ma~tin~~*~
IOffe 8 C h e m i ~ k ~ ~ ' ~
conry71'~

Streissguth, Barr, & S a m p ~ o n ~ ~ * ~

Fried 8 W a t k i n s ~ n ~ ~ * ~ ~

4Y
1.5-9m
5.2-18.5~
5.2-15.8~
5.2-18.5
7.5y
3Y
4Y

Streissguth. Aase, Clarren. Randels, LaDue,

& Smith7R
Carney & Chermak'Z''R
Forrest, Florey, Taylor, McPherson, 8
Y o ~ n g ~ ~ * ~
Streissguth, Randels. & Smith34Rc

Coles, Brown, Smith, Platzman, Erickson, &

Falek4'*'

12-4oy
8y6m (SD
18m
8.0~
16.9~
9.oy
16.0~
5yl Om

2.3y)

IQ range

79.93 (vs. 80.47)"

87.92 (vs. 95.69)
80.73 (vs. 94.90)
66

Oleglrd, Sabel, Aronsson, Sandin,

Johansson, Carlsson, Kyllerman, Iversen.
& HrbekZgfR
Shaywitz. Cohen, 8 S h a y ~ i t z ~ ~ ' ~

Steinhausen,
Spohr & Steinhau~en'~'~~;
Gobel, 8 N e ~ t l e ? ~ ' ~ ~
Aronson, Kyllerman. Sabel, Sandin, 8
Oleglrd3Z*R
O'Connor, Brill, & Sig~nan~O*~

Mean IQ

Bayley MDI
Stanford-Binet
WlSC FSlQ
Brunet-Lezine

4
9
48 total

12m

Tests

15
13
15
22

17
13 (FAS)
6 WE)
19 (controls)'
482
69 (AA/day 2 0.14)
64 ( W d a y < 0.14)
71 ( W d a y 2 0.14)
59 W d a y < 0.14)
38 (FAS)
14 (FAE)
10
592
27 (FAS)

WISC, WPPSI, or StanfordBinet

Bayley MDI

Bayley, Stanford-Binet.
Denver, Wechsler
Bayley MDI
Columbia Mental Maturity
Scale
Columbia Mental Maturity
Scale
Griffith
WISC
Bayley MDI

Bayley MDI

NIA
Bayley MDI

WPPSI
Bayley MDI
WPPSI, WISC-R, or WAIS-R

WISC-R
McCarthy GCI

WISC-WWAIS-R
WISC-R
Bayley MDI
WISC, WISC-R, StanfordBinet, WAIS, WAIS-R

13 (FAE)
25 (AA/week = 11.8)
21 (Wweek = 0)

K-ABC

33-1 12

50-97

86 (SD = 20)
89

NIA

NIA'

NIA

92 (controls = 111)
99 (controts = 114)
95 (SD = 2.99)
108 (SD = 8.48)
115 (SD = 7.72)
102.9
111.03
113.11
NIA
98.4
109.5
110.7
119.5
NIA'
67.4
60.1
86.0
87.3
NIA'
115.8
114.8
123.4
124.4
66
73
79
NIA'
66.0
66.7
79.5
82.2
83.91 (SD = 12.61)
91.91 fSD = 13.81)

<70 (n = 12)
70-85 (n = 33)

NIA
50-89
For FASIFAE:
40-1 01
NIA

20-1 05
50-91
NIA

NEUROBEHAVIORAL FINDINGS IN FAS

283

Table 2. Continued
Authors

Age

5 ( P P M > 3.5)9
11 (PPAA < 3.5)
97 (PPAA < 1)
39 (Abstainer)
6rn
297
Greene, Ernhart. Ager, Sokol, Martier, 8
279
1Y
275
2Y
269
3Y
4yl Om
260
LaDue, Streissguth, & Randels6"*R
12-42~
(mean = 18.4) 92 (FASIFAE)
Autt-Ramo, Korkman, Hilakivi-Clarke,
27m
20 (3 trimesters exp.)
Lehtonen. Halrnesmaki. & G r a n ~ t r o m ~ ~ * '
20 (2 trimesters exp.)
20 (1 trimester exp.)
71 ( W d a y > 0.14)
Fried, O'Connell, & W a t k i n s ~ n ~ ' * ~ ~
5Y
64 ( W d a y < 0.14)
67 ( W d a y > 0.14)
6Y
70 ( W d a y < 0.14)
382
Jacobson, Jacobson, Sokol. Martier, Ager,
13m
& Kaplan-Estrin7'*'
OConnor. Sigrnan, & K a ~ a r i ' ~ ~ * ~
12m
24 ( W d a y > 0.10)
20 ( W d a y < 0.10)
17m-30~
12 (FAS)
Streissguth 8 D e h a e r ~ e ~ ~ ~
7 (FAE)
10 (PEA)h
Caruso B ten B e n ~ e I ' ~ ~ ' ~
N/A
15
Steinhausen. Willms, & Spoh?s*Rc
15
5y4m (SD = 13m)
8y9m (SD = 24m)
5y5m (SD = 14m)
16
15ylm (SD = 25m)
31
9y10m (SD = 18m)
13y2m (SD = 19m)
41
Spohr, Willms, & S t e i n h a u ~ e n ' ~ ~ ' ~ ~ 15y4m (SD = 21.61-4
Russell, Czarnecki, Cowan, McPherson. &
MudaP7*'

Janzen. Nanson, & Block68'R

Larroque, Kaminski, Dehaene, Subtil,
Delfosse, & Q u e r l e ~ ~ ~ * ~
Mattson, Riley, Gramling. Delis. &

18m

52.7~1
(SD = 8.82m)
-4.5y
8 . 5 ~(SD = 3 . 8 ~ )
8 . 5 ~(SD = 4.0~)

10
32 2 1.5 oz/day
123 < 1.5 odday
34 with FAS
13 with PEA

Mean IQ

Tests

WPPSI VIQ/PIQ

Bayley MDI

101.1/101.7
111.8/99.9
107.7/101.9
107.8/100.7
N/A'

WAIS-WISC-R
Bayley

70
N/A'

McCarthy GCI

120.9
122.2
126.8
124.2
N/A'

Bayley MDI

107.79 (SD = 10.7)

113.1 (SD = 8.99)
69.6
93.0
91.7

Bayley MDI

Bayley, WISC-R, WAIS-R,

Stanford-Binet, TermanMemill, Brunet-Lezine
WISC-R
69.7
Columbia Mental Maturity
NIA'
Scale, WPPSI, or WISC-R

WPPSIMIISC-R

8G116; n = 10
71-85; n = 14
51-70; n = 6
36-50; n = 5
C35; n = 6

McCarthy GCI
McCarthy GCI

67.6

WPPSI-WWISC-R

89.5 (SD = 2.92)

103.2 (SD = 1.69)
74.4
83.6

IQ range

N/A

12-1 08
N/A

NIA

56-120

NIA
NIA

NIA
NIA
NIA

N/A, not applicable; FSIQ, Full scale IQ; GCI, General Cognitive Index; K-ABC, Kaufman Assessment Battery for Children: VIQ, Verbal IQ; PIQ, Performance IQ: exp,
exposure.
* Subjects are FAS: t subjects are AE 1-3; $ subjects are alcohol-exposed to varying degrees.
Retrospective study: prospective study.
a Values for controls included for comparison purposes.
This sample includes patients reported earlier in Jones, Smith, Ulleland. and Streissguth (1973).
Retest.
AAP = oz of absolute alcohol consumed/day in the month prior to pregnancy recognition; IAA = 1-2 drinks of beer, 2 drinks of wine, or 2 drinks of liquor.
AA = oz of absolute alcohol/day during pregnancy.
'See text for details.
PPAA = oz of absolute alcohol consumed prior to pregnancy recognition.
This study involves 16 sets of twins; PEA = prenatally exposed to alcohol, no diagnosis.

present. Importantly, in the absence of the specific facial

malformations, and thus the diagnosis of FAS, cognitive
deficits, even mental retardation can still be present.
The intent of this paper is to review the behavioral and
cognitive effects of prenatal alcohol exposure. More than
20 years of research are discussed, with a focus on IQ,
activity, attention, learning, memory, language, motor, and
visuospatial abilities in children prenatally exposed to varying amounts of alcohol, including those with FAS. Animal
studies will only be briefly discussed in support of human
studies.

INTELLIGENCE

In the more than 20 years since FAS was first described,

an array of cognitive and behavioral characteristics have
been identified in children and animals exposed to alcohol
Various authors have addressed the effect of
prenatal alcohol exposure on IQ, and in general, such
exposure leads to a decreased IQ score. Both individual
cases and group means have been reported in the literature. Although some comparability between reports is possible, there are differences in the measures that have been

284

MATrSON AND RILEY

used to evaluate intellectual functioning. The predominant ment at the ages of 3 years 10 months, 14.5 months, and
tests that have been used are the Bayley Scales of Infant 14.5 months of age, respectively. After the twins were
Mental and Motor Development (subsequently called the placed in a good foster home, they were reassessed and
Bayley), which provides a Mental Development Index earned MDI values of 76 and 70. Four new cases, who were
(MDI); the Stanford-Binet Intelligence Scale; and the all children of one alcoholic woman, were described by
Wechsler scales that include the Wechsler Preschool and Root et a1.12 All were diagnosed as having FAS, although
Primary Scale of Intelligence, original and revised versions one (PC, the third child) had fewer dysmorphic features.
(WPPSI and WPPSI-R); Wechsler Intelligence Scale for The IQ scores of these children were 80,75,112, and 68. It
Children, original and revised versions (WISC and WISC- is notable that PC, the third child, had fewer dysmorphic
R); and the Wechsler Adult Intelligence Scale, original and features and the highest IQ of the group. In a report
revised versions (WAIS and WAIS-R). The Stanford-Binet proposing a new syndrome, a child was described who
and the Wechsler scales provide Intelligence Quotients or seemed to meet the criteria for FAS and had an alcoholic
IQ scores based on comparison with large standardization mother. Although the author did not recognize the case as
groups. In the following discussion of IQ in FAS, the FAS, an editorial note identified the similarity between the
specific tests used will be mentioned if this information is case and the recent description of FAS by Jones and colavailable. Individual case reports that include IQ estimates leagues. This child had an IQ of 75.13
are listed in Table 1 and IQ reports of alcohol-exposed
Majewski et al. l4 reported three examples of alcohol
groups are listed in Table 2. Although general information embryopathy (AE), including one boy with AE I who had
about intelligence in FAS will be reviewed, only cases that an IQ of 105, using Kramers method of assessment. The
require more detailed description will be discussed here, term alcohol embryopathy is used in place of fetal alcohol
and the reader is referred to the tables for a complete list syndrome by German researchers who considered it more
of reports that include measures of IQ.
appropriate because the associated dysmorphology occurs
during the embryonic period of development. In addition,
the use of AE terminology includes a gradation of effects
Reports of Individual Cases of Children with FAS
that is not traditionally associated with the FAS terminolEarly reports of children with FAS were often descriptive ogy. Three degrees (I, 11, and 111) are used to describe
studies of very small groups of children or individuals. alcohol-exposed children with mild (I) to severe (111) alcoMeasurements of intelligence were not always included or hol-related e f f e ~ t s . ~
were described qualitatively (i.e., borderline or mentally
Intellectual functioning has been reported for children
retarded) rather than quantitatively. A review of the avail- with FAS who also have other disorders or malformations.
able reports, detailed in Table 1, reveals a mean IQ of FAS In 1976, a child with FAS and Noonan phenotype was
cases is 65.73 (SD = 20.2), with a range of 20 to 120. This reported to have an IQ of 85.16 Chromosomal abnormalimean encompasses all cases that are clearly FAS and had ties in children with FAS have been reported in three cases.
an exact IQ estimate (n = 79). When more than one testing The first report described two children with IQ scores of 66
was reported for the same individual, only the most recent and 55 and had the following chromosomal abnormalities:
score was included in the mean. Several of these cases 46, XY, inv. (3) (p13q27) and 45, XY, -14, -15, +t
deserve a more detailed discussion. The earliest reports of (14q15q). It is unclear what role these abnormalities had in
Jones and his colleagues3 on eight infants and young chil- the etiology of the dysmorphic and cognitive anomalies
dren with FAS documented MDIs and IQ scores for seven observed in these two children. It is notable that other
patients in the range of 50 to 83 (mean = 67.6) using the family members, including one mother, had similar dysmorBayley and the Stanford-Binet. In a 10-year follow-up, phic feature^.'^ The second report was of a girl with an IQ
these cases were rereported according to the revised Stan- of 50 and 47 chromosomes in all cells. In addition, a
ford-Binet normative data. The new range of the original 15-year-old girl with FAS and schizophrenia was deIQ scores for six of the seven children was rereported as 47 scribed. Her IQ was estimated to be 52, although psyto 83 (mean = 62.3). Two additional cases were also re- chotic symptomatology may have interfered with valid asported with IQ scores of 30 and 43 at the ages of 7 months sessment. IQ scores of additional cases of FAS with
and 4 years, respectively. At the 10-year follow-up, the IQ Klippel-Feil malformation2 and renal anomalies21 have
scores of these eight patients were 20 to 86 (mean = 61) also been noted.
using the Stanford-Binet and WISC6 The issue of the
In the 1980s, fewer case reports included a measure of
stability of IQ over time in individuals exposed to alcohol IQ, although a similar number of cases were reported.
prenatally is addressed later in this paper.
According to Abe1,22 245 cases of FAS were documented
In 1974, the cases of three siblings (one singleton and between 1973 and 1979, with 45 reports of IQ (18.4%).
monozygotic twins) born to an alcoholic mother were de- Alternatively, in the 205 cases reported between 1980 and
scribed by Palmer et al. These three children met the 1988, only 13 included IQ scores (6.3%). A review of the
existing criteria for FAS and had MDI/IQ scores of 65 literature uncovered four more IQ reports. Two come from
(Stanford-Binet), 56, and 59 (Bayley) at their first assess- a study included by Abel but not included in his listingz3

NEUROBEHAVIORAL FINDINGS IN FAS

and two from a review article by Aronson & OlegHrd.24

Since Abels comprehensive summary of FAS reports, very
few reports have included IQ scores or even individual case
descriptions. This decrease in case reports reflects the
growing recognition of FAS and the increase in retrospective and prospective group studies.
Reports of Groups of FAS or Alcohol-Exposed Children:
Retrospective and Prospective Studies
As the study of the effects of prenatal alcohol exposure
progressed, larger retrospective and prospective studies
were initiated. Retrospective studies have evaluated groups
of children with FAS or varying degrees of alcohol-related
effects and have reported results as a function of group
means for FAS/alcohol-exposed and nonexposed controls.
Benefits of this type of study include the value of larger
groups of subjects and the inclusion of control groups.
Alternatively, confounding factors, such as cultural or socioeconomic effects, as well as the possibility of an ascertainment bias, sometimes confuse the results. Additional
difficulties arise in these and other studies in terms of
potential confounding variables, such as maternal IQ, paternal effects, medication usage, and other comorbidity
factors. These factors are often not addressed in retrospective studies, but their relevance cannot be ignored. Wellcontrolled studies, including well-matched control groups,
help reduce the problem of confounds but ascertainment
remains a difficulty with this type of sample. In addition,
because the children in retrospective studies are identified
after birth and frequently medical records and/or contact
with the biological mother is unavailable, there is often
little reliable information about the degree of alcohol exposure. When only children with FAS are evaluated, less of
a problem exists because alcohol exposure is typically included in the diagnostic criteria and the relationship between such exposure and the resulting physical features is
clear. In other words, because alcohol exposure is part of
the traditional diagnostic criteria, children with unknown
prenatal histories are excluded by definition. When less
affected non-FAS children are evaluated, there is more
reliance on prenatal alcohol history for study inclusion.
Retrospective studies (see Table 2 for complete list),
such as the early Seattle s t ~ d i e s ~or
~ studies
~
out of German~,~-~
reported an overall mean IQ of 72.26 (range of
means = 47.4-98.2). This weighted mean (the mean was
adjusted for sample size differences) encompasses all retrospective group studies (17 studies) of children with FAS
or AE (total n = 269) as detailed in Table 2.
A few retrospective studies require more detailed discussion. Although traditional studies of intellectual functioning in FAS began with children of alcohotic mothers, Shaywitz et al.30started with a large group of learning disabled
children and discovered 15 who were born to alcoholic
Women. This group had a mean IQ of 98.2 (range =
80-113) using the WISC, WPPSI, or Stanford-Binet. The

285

authors, however, were interested in learning difficulties in

children of normal intelligence who were born to alcoholic mothers, and these children may not truly be representative of FAS. In a different group of 63 children with
FAS, IQ information was available for the 30 that were
over the age of 3 years. The IQ scores ranged from 50 to 97,
with most patients having IQ scores between 65 and 70, and
mental retardation was found in 14 of the 30 (46%).31 A
group of 21 alcohol-exposed subjects and a well-matched
control group were assessed by Aronson and colleagues32
using Griffiths Mental Developmental Scales and the
WISC. The mean performances of the alcohol-exposed
group were 19 and 15 IQ points below the control group on
the Griffiths and WISC, respectively. Only 10 of the 21
alcohol-exposed individuals met criteria for FAS, reiterating that the effects of alcohol are important even in the
nondysmorphic individual. Finally, in a long-term follow-up
of adolescents and adults with FAS (n = 38) or FAE (n =
14), mean IQ was determined to be 68 (range = 20-105).
The mean I Q of the FAS group, at 66, was lower than that
of the FAE group that was 73.7
Recently, the IQ performances of children with FAS were
compared with alcohol-exposed children with few if any features of FAS.33 All chddren in this study were exposed prenatally to high amounts of alcohol; however, only the FAS
group displayed the craniofacial anomalies and growth deficits
associated with the diagnosis. The other group was designated
as having prenatal exposure to alcohol (PEA) and had documented exposure to high levels of alcohol, but were not dysmorphic, microcephalic, or growth retarded. In comparison
with normal controls, both groups of alcohol-exposed children
displayed significant deficits in overall IQ measures, as well as
deficits on most of the subtest scores. Importantly, these
deficits in IQ were found in both alcohol-exposed groups.
Whereas the PEA subjects usually obtained marginally higher
IQ scores than those with FAS, few significant differences
were found between the two alcohol-exposed groups. These
results indicate that high levels of prenatal alcohol exposure
are related to an increased risk for deficits in intellectual
functioning and that these deficits can OCCUT in children without all of the physical features required for a diagnosis of FAS.
Similarly, individuals with the partial phenotype of FAS, or
FAE, display IQ d e f i ~ i t s .Our
~ , ~ PEA subjects may be somewhat similar to individuals identified by other groups as having
FAE; however, individuals with PEA display few if any of the
facial features of FAS, and are not growth retarded or microcephalic.
Prospective studies of the effects of prenatal alcohol
exposure have evaluated pregnant women using a variety of
prenatal measurements, including alcohol consumption.
The resulting offspring have been followed longitudinally,
up to 14 years in the case of Streissguth et al.35 The
strengths of such studies are obvious. They allow for a
better understanding of the exposure patterns and can
include measurement of other, possibly confounding, factors (e.g., smoking, other drug use). Although very often

286

MATSON AND RILEY

the children in these prospectively identified groups do not rospective studies is that they allow greater understanding
have FAS and the level of alcohol exposure is relatively low, of the effects of pregnancy drinking dose and pattern.
the use of large groups of mothers allows for an assessment Although animal studies (e.g., Refs. 45 to 47) clearly indiof the relationship between alcohol exposure and offspring cate the importance of pattern and timing of alcohol expobehavior. As a consequence of the design of these large sure and binge-drinking has been identified as a significant
prospective studies, relationships between the variables are risk factor for negative neurobehavioral outcome (e.g., Ref.
described, and group means are often not reported. How- 44), more information is needed. For example, beyond
ever, some prospective studies still include IQ values pre- trimester of exposure (e.g., Ref. 48), little is known about
the relationship between timing of alcohol exposure and
sented as a function of alcohol exposure level.
Similar to the retrospective studies, prospective studies later neurobehavioral outcome in humans. Future studies
have found decrements in IQ related to alcohol exposure. should emphasize more detailed analyses of factors such as
Golden et al.36 assessed twelve 1-year-old children who timing and dose of in-pregnancy drinking.
were identified as having FAS, based on prospectively gathered information on alcohol exposure and neonatal exam- Studies Finding No Effect of Prenatal Alcohol Exposure do
ination. Using the Bayley, the mean MDI for this group was Exist
estimated as 86. In 1990, Ioffe and C h e r n i ~ kreported
~~
a
Not all studies report decreases in intellectual performean MDI of 67.4 in a group of 17 alcohol-exposed infants
mance,
however. A 1991 report from Scotland used the
(1.5 to 9 months of age) identified prospectively. Additionally, a group of 20 prospectively identified, alcohol-exposed Bayley to assess five hundred ninety-two 18-month-olds
children (only six with FAS) whose mothers continued to and found an increase in performance related to pre- and
.~~
alcodrink throughout pregnancy had significantly lower scores postpregnancy alcohol c o n ~ u m p t i o n Furthermore,
hol
exposure
was
unrelated
to
cognitive
outcomes
on
the
on the Bayley than children whose mothers drank during
McCarthy
in
children
3
through
6
years
of
age.50751
As
the
the first trimester only.38
authors
point
out,
however,
the
exposure
levels
in
this
study
With the use of prospective investigation of alcohol use
during pregnancy, more information has become available were very low (mean = 0.43 to 0.45 M d a y ) in the higher
about the effects of different levels of alcohol exposure. exposure group. Another study of children exposed to low
Streissguth and her colleagues have followed the children amounts of alcohol (mean = 0.07 M d a y ) found no effect
of nearly 500 mothers from the prenatal period through the of alcohol exposure on the Bayley at ages 6 months and 1,
age of 14 years. In 1980, she reported a relationship be- 2, and 3 years, and the WPPSI at age 4 years, 10 monthss2
tween the amount of alcohol consumed and performance
on the Bayley at 8 months of age.39The mean MDIs ranged Concordance of IQ in Twins Exposed to Alcohol Prenatally
from 116 for infants of mothers who drank <0.10 AAP
Additional information on IQ as a function of in utero
(ounce of absolute alcohol per day prior to pregnancy alcohol exposure is also available in studies examining twin
recognition) to 98 for infants whose mothers consumed >4 pairs. In an interesting report of the concordance of diagnosis
AAP. O'Connor et a1.4' reported a similar result. In twenty- and IQ in twin children of alcoholic mothers, Streissguth and
five 12-month-old infants, mean Bayley MDI decreased DehaeneS3described 16 pairs of twins, both monozygotic and
from 115 with <0.1 AAP to 95 with >1 AAP.
dizygotic. For the most part, the twin pairs were concordant
Similarly, other groups have reported decreases in for diagnosis (i.e., FAS, FAE, or none). Monozygotic twins
MDI/IQ in relation to alcohol exposure. Moderate alcohol were exclusively concordant for diagnosis; and, as would be
use during pregnancy [mean consumption = 0.31 oz abso- expected, there was more variability in the dizygotic twins. In
lute alcohol per day ( M d a y ) ] was related to decreased no case, however, did one twin receive the diagnosis of FAS,
performance on the Bayley in 24-month-old ~ f f s p r i n g . ~whereas
~
the other received no diagnosis. In terms of mental
Furthermore, Coles et a1?* reported a decrease in overall development, the IQ scores for diagnosis-concordant pairs
mental processing on the Kaufman Assessment Battery for differed by an average of 8.1 points, whereas the discordant
Children in a group of children (mean age = 5 years, 10 pairs differed by 12.5 points. In the three pairs of monozygotic
months) whose mothers drank throughout pregnancy twins tested, the mean difference was 4.3 IQ points, and the
(mean consumption = 11.8 M w e e k ) . Importantly, Stre- dizygotic twins differed by an average of 11 points. For this
issguth has continued to find decreases in IQ in relation to sample, the mean IQ for the FAS, FAE, and no diagnosis (but
alcohol exposure as the study population matured. Specif- alcohol-exposed) groups were 69.6, 93.0, and 91.7, respecically, at 4 years of age, exposure to M d a y was related to tively.
a decrease in full-scale IQ of nearly 5 points43and exposure
to 1 M d a y was associated with a 6-point decrement in
full-scale IQ at age 7.44 IQ was not assessed at the 14-year Stability of IQ in Children Exposed to Alcohol Prenatally
follow-up (Streissguth, personal communication, October
The stability of IQ over time in patients with FAS was
1994).
evaluated in a report by Streissguth et al.54 Retest of 17
Importantly, one benefit of prospective studies over ret- patients 1 to 4 years (median interval = 1.75 years) after

NEUROBEHAVIORAL FINDINGS IN FAS

initial evaluation revealed a high correlation between test

and retest IQ scores, although four of these patients
(23.5%) achieved scores >1 SD from their original evaluation (two improved). The mean IQ from the first testing
was 66 (range = 15-99), and the second testing was 67
(range = 10-96). In the 10-year follow-up mentioned previously,6the mean improvement was 9.1 IQ points (range =
1-30), with only one patient (12.5%) improving >1 SD. In
an extension of these earlier studies, Streissguth reported
additional test-retest data of adolescents and adult^.'^ Over
an average test-retest interval of 8.3 years, the correlation
of IQ between testings was 0.78 for FAS patients (n = 27)
and 0.88 for FAE patients (n = 13). The mean IQ scores
were 66.0 (range = 29-105) at initial test and 66.7 (range =
20-91) at retest for the FAS group and 79.5 (range =
56-101) and 82.2 (range = 65-114) for the FAE group. In
all, only 7 of 40 patients (17.5%) were >1 SD from their
previous test performance (five improved). Other reports
of repeated
indicate relatively good stability
of IQ over time, with the most variability in younger patients (see Table 1 for summary). One study indicated
improvement in intellectual functioning over a 3-year peri~ d although
, ~ this
~ may have been due to a few children
who moved from the below average range (70-85) to average range (86-115) of i n t e l l i g e n ~ eIn
. ~the
~ children with
IQ scores in the mentally retarded (<70) and above average ranges (>115), there was no significant change in
performance. Later reports by the same authors suggest
greater stability over longer periods of time.59
WQ vs. PZQ in Individuals with FAS
It has been suggested that FAS is associated with greater
decrements in Verbal I Q (VIQ) than in Performance I Q
(PIQ).60,61However, a review of the studies where this
information is actually available suggests that the results
are equivocal. In eight case reports of individuals with FAS,
four cases16,19,62,63 displayed PIQ > VIQ, with a mean
difference of 8.5 IQ points (range = 3-22). However, six
cases11,56,64,65
demonstrated VIQ > PIQ, and the mean
difference was 17 IQ points (range = 11-26). In two case ~ ,there
~ ~
was, no~ difference
~
between the two subscales.
The average VIQ and PIQ scores from these case reports
are 61.00 (SD = 12.82) and 55.33 (SD = 13.45), respectively. In the 17 group studies of individuals with FAS
where the relevant data were available, 10 studies25,32,33,44,49,50,66-69
indicated no differential effect of prenatal alcohol exposure on verbal versus nonverbal abilities.
although the scores for VIQ and
In one of these
PIQ were equal, PIQ was more affected than VIQ. Howthe opposite was true. PIQ (or
ever, in another
PDI) was greater than VIQ (or MDI) in five group studies,7341,61270,71
whereas VIQ was greater than PIQ in two
s t ~ d i e s .In~ one
~ , ~of~ these studies,71 which has been cited
as evidence for the PIQ-VIQ differential, the FAS and
FAE subjects did in fact display greater PIQ than VIQ

2x7

scores. However, the greatest difference between these two

subscales was in the control group; in fact, PIQ appeared to
be more affected than VIQ when the alcohol-exposed subjects were compared with these controls. It is therefore
unclear whether VIQ is consistently affected to a greater
degree than PIQ in individuals with FAS. It is clear, however, that FAS is related to decreased intellectual functioning with an average IQ between 65 and 75, and that this
level of performance is stable across time. Furthermore this
decrease in performance is also seen in children with prenatal alcohol exposure in the absence of FAS.
OTHER NEUROBEHAVIORAL DOMAINS

The following sections detail the ability levels of children

with FAS in five neurobehavioral domains: activity and
attention, learning and memory, language, motor, and
visuospatial functioning. Studies involving children with
FAS or prenatal alcohol exposure are included, and brief
discussions of animal studies are included when appropriate. The results of neuropsychological studies of children
with FAS are summarized in Table 3.
ACTIVITY AND ATTENTION

Hyperactivity and attentional deficits are hallmark features

of prenatal alcohol exposure. In fact, offspring activity level
may be a more sensitive indicator of alcohols teratogenicity
than physical
Children with FAS have been described as tremulous, hyperactive, and irritable.74Caretakers
note that the children are always on the go, and never sit
In a long-term follow-up of children with FAS, hyperlanetic disorders were among the most frequently diagnosed disorders and persisted throughout ~hildhood?~
In addition, hyperactivity may occur in the absence of intellectual
impairment. One study of 15 alcohol-exposed children of
average intelligence (IQ range = 82-113, mean = 98.2) reported all but one as being hyperactive? Even in the absence
of the diagnosis of FAS, moderate levels of alcohol exposure
(mean = 0.45 AA/day) have caused offspring to be more
fidgety and less ~ompliant?~
Animal models of prenatal alcohol exposure have reiterated and emphasized the effect of maternal alcohol exposure on activity levels in o f f ~ p r i n g .In
~ ~a , review
~~
of the
literature concerning prenatal alcohol and hyperactivity,
Bond77 concluded that, if rats are exposed to alcohol
greater than 6-7 g/kg/day, and are tested prior to 70 days of
age, they exhibit an increase in activity in comparison with
control offspring. Hyperactivity in rats is easily tested in a
variety of ways, and all methods of prenatal treatment and
assessment appear to produce similar results.10778
In addition to hyperactivity, attentional deficits have long
been associated with FAS and prenatal alcohol exposure.
Early naturalistic observations of infants suggested that prenatal alcohol exposure was associated with an increased
nonalert state. That is, the infants spent more time with eyes

288

open, but not attending.79Such deficits in attention appear to

continue through
to those Of
and may be
children with Attention Deficit Disorder (ADD).8oBoth FAS/
FAE and ADD children showed deficits in investing, organizing, and maintaining attention and had an increase in impulsive responses. Similarly, adolescents and adults with FAS
demonstrated deficits in tasks involved in the focusing (Talland Letter Cancellation Test), encoding (WISC-R Digit
Span), and shifting [Wisconsin Card Sorting Test (WCST)] of
attention.8l Alternatively, in an examination of children with
and
with ADD the
performed similarly to controls and better than ADD children on
tests of reaction time and vigilance.
Attentional deficits have also been related to prenatal
alcohol exposure in non-FAS children. Four-year-old children of social drinkers (mean consumption = 0.45 AA/
day during pregnancy, 0.88 AA/day prior to pregnancy)
were observed to have poorer attention spans than control
children when parity, maternal smoking, home environment, and sex of the child were used as covariates.73Streissguth et al.83 also examined 4-year-old children for sustained attention using a continuous performance task.
After covarying maternal smoking, caffeine use, nutrition,
education, and childs birth order, prenatal alcohol exposure was significantly associated with an increase in errors
of omission, commission, and a decrease in the ratio of
correct to total responses. Importantly, in this study the
level of activity did not differ from normal controls,
indicating that hyperactivity did not play a significant role
in the attentional problems noted in this sample. At age 7,
this cohort again demonstrated an increase in reaction
time, and errors of commission and vigilance84;and, at age
11, maternal binge drinking was associated with behavioral
difficulties at school, including hyperactivity and attentional problems.85At age 14, prenatal alcohol exposure was
again related to attentional measures,86 as well as performance on the WISC-R Arithmetic ~ u b t e s twhich
, ~ ~ is commonly thought of as a measure of attention and freedom
from
Streissguths findings of deficits on
attentional measures were supported by Brown et al.,89who
reported deficits in the ability to sustain attention following
alcohol exposure throughout pregnancy.
Not all studies find effects on attention, however. Fried and
colleaguesg0found no relationship between alcohol exposure
and attentional measures at 6 years of age. In fact, there was
a decrease in impulsive responses and maternal perception of
behavior in relation to alcohol exposure. These authors suggest differences between study cohorts and measures as possible reasons for the discrepancies between their findings and
those of Streissguth et al.83Importantly, the alcohol exposure
levels in this cohort were very low. However, Boyd and colleagues also reported no effect of prenatal alcohol exposure
on sustained attention in preschool children of alcoholic
mothers who drank during pregnancy. The alcohol exposure
levels in this study, while still relatively low, were higher than
in the previous study.go

MATSON AND RILEY

LEARNING AND MEMORY

Although learning processes, per se, have not been systematically addressed until recently, learning abilities, broadly
defined, have been described in alcohol-exposed infants and
children. The earliest studies of Streissguth and colleagues
measured early learning and behaviors thought to be related
to learning. In an operant learning study, extinction after
reinforcement of two simple behaviors was measured in newborns exposed to alcohol and nicotine prenatally? Alcohol
and nicotine interacted to produce significantly poorer learning in the infants. In the same sample, decreased habituation
on the Brazelton Scale was related to alcohol use in mid
pregnancy.93Deficits in learning continue to be reported from
the Seattle cohort. Decreased academic achievement and increased parent and teacher ratings of learning problems at 7%
years of age were related to maternal binge drinkinga and
measures associated with learning ~kills.8~
In addition, learning difficulties were also observed in children with IQ scores
within the average range who were born to alcoholic mothers: although this sample was selected from a learning disabilities clinic.
Studies targeting more specific aspects Of learning and
learning
are now being reported*
and memory were assessed in 2o
with FAs.94
When compared with children matched for age, sex, and
race, the children with FAS demonstrated deficits in both
learning and recalling a word list. Their recall was impaired
on both free and recognition recall trials, and they made an
increased number Of intIllSiOn, perseveration, and falsepositive errors. These errOr.5 are COnSiStent with deficits in
response inhibition. However, given their decreased level
Of learning, their retention Of the material Was relatively
intact. This Same pattern Of impaired learning and relatively unimpaired retention was also dtmonstrated in
adults with FAS95and are suggestive of pervasive deficits in
encoding verbal information.
Reports from the Seattle cohort also SukXest a relationship
between memory functioning and Prenatal alcohol exposure.
For example, deficits have been noted in auditory memoIy,8196
memory for stories and designs97and spatial memoryF6 Other reports of spatial memory deficits have been reported in chMren with FAS98 as have deficits on some
measures of working
Alternatively, in the Ottawa
cohort, prenatal alcohol exposure was not related to performance on the memory component of the McCarthy Scales of
Childrens Abilities in 3- or 4-year-old childred or 5- or
6-year-old children.51In addition, prenatal alcohol exposure
was not related to Visual recognition memory in alcoholexposed infants in a study of the Detroit cohort.00
The animal literature is replete with studies of learning
deficits following prenatal alcohol exposure.lo Offspring of
rats given alcohol during gestation show learning deficits
that include active avoidance,75passive avoidance, discrimination and reversal, and taste aversion learning.lo3
Memory deficits have also been reported in rats exposed to

NEUROBEHAVIORAL FINDINGS IN FAS

289

alcohol prenatally. Specifically, deficits in spatial memo- between maternal alcohol use and offspring Word Atry104,105and retention of learned tasks'06 have been re- tack performance at 14 years of age.87Word Attack is a
ported following prenatal alcohol exposure. Other studies, subtest of the Woodcock Reading Mastery Tests and
however, suggest that long-term retention of information involves reading of nonwords. This task requires a
after learning is relatively i n t a ~ t . ~ ' " Whereas
' ~ ~ ' ~ ~a~com- knowledge of pronunciation rules and is related to readplete discussion of the findings of animal studies, as well as ing ability. To summarize, children with FAS appear to
their strengths and limitations, is beyond the scope of this have deficits in speech and language, and similar deficits
paper, several reviews of the literature
are noted in some groups of prospectively identified
alcohol-exposed children.
LANGUAGE

The effects of prenatal alcohol exposure on language

have been mixed. Case reports suggest the presence of
speech and language disturbances resulting from prenatal
alcohol exposure. Abe122lists 53 reports of speech delay or
impediment in 550 FAS cases published between 1973 to
1988. These reports range from complete lack of intelligible
speech"' to mild dysarthria"' or lisping."2 Both receptive
(e.g., Ref. 113) and expressive (e.g., Ref. 114) language
deficits have been noted as have articulation disord e r ~ ~and~ developmental
, ~ ~ , ~ ~
Group studies of language functioning in children with
FAS also find deficits in speech and language functioning
(e.g., Refs. 38 and 118). Reported deficits include word
c o m p r e h e n s i ~ n ,l9~naming
~ , ~ ~ ~ability,'"
~ ~ ~ ~ articulation,"'
and expressive and receptive language skills.68,'21On tests
of verbal fluency, children with FAS display impairments in
letter fluency although category fluency appears to be less
affected.993122
In contrast, a recent report of eight children
with FAS documented relatively intact language development, when compared with controls.'23
In prospective studies of children exposed to varying
amounts of alcohol, however, the results are not as clear. In
a sample of alcohol-exposed children from Ottawa, Canada, decreases in language comprehension were found in
13-m0nth-old,~'2-year-0ld,~'and 3-year-old5' children exposed to relatively low levels of alcohol (mean exposure =
0.31 M d a y for the entire 2-year-old sample, 0.45 M d a y
for the "heavier" exposed group in the 3-year-old sample).
No deficits were found, however, in the same cohort at' ;4
5, or 651years of age. Furthermore, no effect on expressive
or receptive language skills was found in a separate group
of alcohol-exposed children at 1, 2, or 3 years of age.124
Like the Ottawa cohort, this group of children were exposed to relatively low levels of alcohol exposure (mean
exposure = 0.07 M d a y ) .
Other studies have documented effects of alcohol on
language, however. Russell and colleagues67 reported
deficits in offspring receptive language functioning related to indications of maternal problem drinking (e.g.,
an individual's perceptions of what others think about
their drinking or reported alcohol-related family problems). This same report also documented deficits in
WPPSI Verbal IQ, which has a significant language component. Finally, a recent report from the Seattle prospective study demonstrated a dose-response relationship

MOTOR ABILITIES

In addition to alcohol's effects on higher level cognitive

functions, there is also an effect on the developing motor
system. Although a few studies find no effect of prenatal
alcohol on motor d e v e l ~ p m e n t , ~ ~most
- ~ ~studies
. ' ~ ~ of motor development and motor skills suggest an effect of prenatal alcohol exposure. Early descriptions of children of
chronic alcoholic mothers3 reported delayed motor development and fine-motor dysfunction. One report noted a
"nonspecific dyscoordinated motor pattern," hemiplegia,
ataxia, and an increase in cerebral palsy in children of
alcohol abusing women.29Later studies also noted delayed
motor development in infants and children exposed to
alcohol prenatall~9,'00,'26and fine- and gross-motor dysfunctions were noted in children of alcoholic mothers127
and social drinkers.12' In addition, Marcus'" noted axial
ataxia and kinetic tremor in children with FAS. Finally,
several reports exist of deficits in motor speed/precision,
finger tapping speed, and grip strength in children with
~~s.68~71~119

Animal models have also provided evidence for motor

dysfunction following prenatal alcohol exposure. Gait dist u r b a n c e ~ , 'delays
~~
in reflex de~elopment,'~'and poor
balan~e'~'
have all been reported in rats exposed to alcohol
during the perinatal period.
VlSUOSPATlAL ABILITIES

Visuospatial abilities in children with FAS have not been

well documented. Many studies report deficits in simple
drawing tasks like the Beery Developmental Test of Visual
Motor I n t e g r a t i ~ n ~ ~ and
, ~ ~the
, ~ Frostig
~ , " ~ Developmental
Test of Visual P e r ~ e p t i o n ~ ~ ~however,
" ~ , ' ~ ~ ;very few studies have addressed more complex visuospatial abilities in
FAS. As mentioned previously, spatial memory appears to
be impaired in children with FAS.81,96,98
Interestingly, the
study of Uecker and Nadel suggested deficits in memory
for the location of objects but not for the objects themselves. In addition, this study documented alcohol-associated deficits in clock drawing, a traditional measure of
visuospatial ability.133In a recent
of more specific
visuospatial ability, children with FAS displayed deficits in
local processing of hierarchical stimuli. These children
were impaired in recalling and copying local (details) but
not global (configural) features of the stimuli. These defi-

92 adolescents and adults with FAS/

FAE
16 FAS Ss with borderline (6) or
normal (10) IQ
8 children with FAS and cpntrols

LaDue, Streissguth, &

Randels"
Don, Kerns, Mateer, &
Streissguthg5
Ernhart, Greene, Sokol,
Martier, Boyd, & AgerlZ3
Kodituwakku, Handmaker,
Cutler, Weathersby, &
HandmakePg

15 children with FAS and controls

Children with alcohol exposure (25

dysmorphic, 62 nondysmorphic),
ADHD. and controls
20 children with FAS and controls

Uecker & NadeIg8

Coles, Platzman, RanskindHood, Brown, Falek, &

Smith"
Mattson, Riley, Delis, Stern, &
Jonesg4
Mattson, Gramling. Delis,
Jones, & Riley134
Mattson, Riley, Gramling,
Delis, & Joneslig

CVLT-C, PPVT-R, Boston Naming Test, Grooved

Peg Board Test, Children's Category Test, WRATR, VMI

Global-Local Test

-/+

-/+

-/+

-/+

LearningIMemory

Attention

+/-

Language

Motor

-/+

Visuospatiai

+/-

Other

Test-Children's Version.

assessments were conducted in this area and deficits were reported.

Ss, Subjects; PPVT-R, Peabody Picture Vocabulary Test-Revised; ADHD, attention deficit hyperactive disorder; K-ABC, Kaufman Assessment Battery for Children; CVLT-C, California Verbal Learning

+, assessments were conducted in this area and no deficits were reported; -,

14 children with FASIPEA and

controls
15 children with FAS; 10 children
with PEA; and controls

10 preschoolers with FAS and

controls

Janzen, Nanson, & Block6'

10 FASIFAE children and controls

Adolescents and adults with FAS

Carmichael Olson, Sampson,

Barr, Streissguth, &
BooksteinS5

Sequenced Inventory of Communication

Development
Raven's Standard Progressive Matrices, PPVT-R,
Wide Range Assessment of Memory and
Learning, Attentional Capacity Test, Progressive
Planning Test, Delayed Response Tasks,
Controlled Oral Word Association Test, SubjectOrdered Task, WCST, Competing Motor Programs
(go-no-go)
McCarthy Scales of Children's Abilities, Grooved
Peg Board Test, VMI, Recognition-Discrimination
Test, Test of Early Language Development
Memory for 16 Objects task, VMI, K-ABC Facial
Recognition Test, Draw-a-Clock test, WISC-R
Mazes
WISC-R Coding, K-ABC Number Recall, Paired
Associate Memory Task, CPT (including simple
reaction time and vigilance measures), WCST
CVLT-C

20 FASlFAE Ss vs. ADD and

controls
7 adults with FASIFAE and controls

Nanson & Hiscock''

Gray & Streissguthg6

Tests
Frostig Test of Visual Perception, Illinois Test of
Psycholinguistic Abilities
Frostig Test of Visual Perception, Human Figure
Drawing Test
Peabody Picture Vocabulary Test-Revised (PPVT-R),
Expressive One Word Picture Vocabulary Test,
Finger Tapping, Grip Strength, Finger Localization,
Reaction Time, Motor Speed and Precision Test,
Beery's Developmental Test of Visual Motor
Integration (VMI)
Choice Reaction Time Test, Delay Reaction Time
Test, Vigilance Test
Stepping Stone Maze, Seashore Rhythm Test,
Dynamic Visual Retention Test, Memory for Faces,
PPVT-R, Wechsler Memory Scale
Digit Span, Seashore Rhythm Test, Stepping Stone
Maze, Nissen Serial Reaction Time Test,
Wisconsin Card Sorting Test (WCST), Continuous
Performance Test (CPT), Talland Letter
Cancellation Test
PPVT-R, Wide Range Achievement Test-Revised
(WRAT-R)
California Verbal Learning Test (CVLT) and others

Subjects

32 children (from a larger sample)

with FAS
21 children of 30 alcoholic women
(10 with FAS) and controls
19 Ss with FAS (13) or FAE (6) and
controls

Authors

Steinhausen, Nestler, &

Spohr' l6
Aronson, Kyllerman, Sabel,
Sandin, & OlegArd32
conry71

Table 3. Summary of Neuropsychological Findings in Children with FAS, Presented in Chronological Order Through 1996

<

m
r

-2=

NEUROBEHAVIORAL FINDINGS IN FAS

cits were not due to the size of the stimuli or to deficits in

memory, and suggested a specific impairment in processing
local features of hierarchical visual information. Similar
deficits have been noted in other d e ~ e l o p m e n t a l and
~~
d e m e n t i ~ ~ disorders.
g~~
OTHER NEUROPSYCHOLOGICAL ABILITIES

In addition to the abilities already discussed, a few studies have documented other specific neuropsychological deficits in individuals with FAS. The WCST is a test of nonverbal problem solving, which requires both problem
solving and cognitive flexibility, and has been proposed to
be sensitive to frontal system dysfunction. Adolescents and
adults with FAS display decreased accuracy,81 achieve
fewer categories, and make more perseverative responses99
on the WCST. Alternatively, the computerized version of
the WCST was found to be only moderately sensitive to
prenatal alcohol exposure in the 14-year assessment of the
Seattle cohort.s6 Our data suggest that, whereas children
with FAS perform more poorly than controls, these deficits
are considerably less severe than we would expect, given
their overall level of ability (i.e., IQ).i37
Finally, tests of planning ability are also thought to be
sensitive to frontal systems dysfunction, although few such
studies have been done in individuals with FAS. On the
Progressive Planning Testy9 which is similar to the Tower
of London Test, children with FASFAE had difficulty
with planning ahead and tended to perseverate on incorrect
strategies.
SUMMARY

In summary, FAS is a devastating developmental disorder that is associated with a wide variety of neurobehavioral
deficits. Studies of FAS have documented consistent deficits in language, motor, learning, and visuospatial functioning. Memory seems to also be affected; however, studies
that include a comparison of learning and recall suggest
that, at least in the verbal domain, retention is fairly normal. That is, learning deficits (i.e., encoding) may be at the
root of observed memory deficits and that once information is learned it can be retained. In addition, most studies
of attention suggest deficits in this domain, although the
study of Coles et a1.82 suggests that further, more specific
evaluation of the components of attention is necessary. In
addition, visuospatial functioning and problem solving are
two, as yet, understudied areas in FAS. Existing studies
suggest deficits in simple visuospatial functioning, but more
complex abilities are yet to be described. Similarly, several
studies show deficits on the WCST, although it is unclear
how these deficits relate to overall cognitive ability. Many
of these deficits have been supported by cohort studies that
provide invaluable information about the role of prenatal
alcohol exposure in the development of neurobehavioral
abilities. Future research is required to more clearly delin-

291

eate whether areas of relative strength or weakness exist in

children with FAS and how their cognitive abilities relate to
other types of mental retardation. In addition, correlation
of neuropsychological and neuroanatomical data may help
us understand the role of abnormal brain development in
cognitive ability. Taken together, results from these two
types of studies can help provide the background for educational and training programs specific to individuals with
FAS or prenatal alcohol exposure.
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