Early Social and Emotional Communication in the Infant
Siblings of Children with Autism Spectrum Disorders:
An Examination of the Broad Phenotype
Tricia D. Cassel Æ Æ Daniel S. Messinger Æ Æ
Lisa V. Ibanez Æ Æ John D. Haltigan Æ Æ
Susan I. Acosta Æ Æ Albert C. Buchman
? Springer Science+Business Media, LLC 2006
Spectrum Disorders (ASD-sibs) are at risk for socio-
emotional difficulties. ASD-sibs were compared to
infants with typically developing older siblings (TD-
sibs)using the face-to-face/still-face
6 months and the Early Social Communication Scale
(ESCS) at 8, 10, 12, 15, and/or 18 months. ASD-sibs
smiled for a lower proportion of the FFSF than TD-
sibs and lacked emotional continuity between episodes.
With respect to TD-sibs, ASD-sibs engaged in lower
rates of initiating joint attention at 15 months, lower
rates of higher-level behavioral requests at 12 months,
and responded to fewer joint attention bids at
18 months. The results suggest subtle, inconsistent,
but multi-faceted deficits in emotional expression
and referential communication in infants at-risk for
Infants with older siblings with Autism
At-risk ? Emotion ? Facial expressions ? Joint attention
Autism spectrum disorders ? Siblings ?
Autism Spectrum Disorders (ASD) are pervasive
developmental disorders adversely affecting the social,
cognitive, and frequently, the intellectual functioning,
of diagnosed individuals (Ritvo, Freeman, Pingree, &
Mason-Brothers, 1989). There is evidence that a broad
ASD phenotype characterizes relatives of individuals
diagnosed with ASDs (Bailey, Palferman, Heavey, &
Le Couteur, 1998; Constantino et al., 2006; Dawson
et al., 2002). The purpose of this paper is to assist in the
identification of early social and emotional deficits
characteristic of the broad ASD phenotype by exam-
ining infant siblings of children with an ASD.
The Broad ASD Phenotype
ASDs are genetically linked developmental disorders
involving key deficits in communicating positive emo-
tion, initiating joint attention (IJA), engaging in
reciprocal interaction, and using language. Autism is
characterized by difficulties in three separate areas:
social and emotional functioning, communication, and
sensory concerns or restricted or repetitive interests.
Other disorders on the autism spectrum include most,
but not all, of these deficits. The broad phenotype of
autism involves more subtle ASD-linked deficits, such
as language delays, difficulties with sensory integration,
and potential difficulties with emotion regulation and
ASDs present a broad range of manifestations, often
within the same family. In identical twin pairs, one
member of whom has autism, the concordance rate for
autism is 60% and the concordance rate for a disorder
on the autism spectrum is more than 90% (Veenstra,
Vanderweele, & Cook, 2003). More than 10% of full
siblings of probands with autism show deficits associ-
ated with an ASD diagnosis (Landa & Garrett Mayer,
2006; Zwaigenbaum et al., 2005). Among adult full
siblings of probands with autism, as many as 20% show
a deficit in social or communicative functioning as
T. D. Cassel ? D. S. Messinger (&) ?
L. V. Ibanez ? J. D. Haltigan ? S. I. Acosta ?
A. C. Buchman
Department of Psychology, University of Miami, P.O. Box
248185, Coral Gables, FL 33124-0751, USA
J Autism Dev Disord
indicated by family history (Bolton, Macdonald,
Pickles, & Rios, 1994; Pickles et al., 2000; Rutter,
2000). Deficits in social responsivity among sibling pairs
illustrate the concept of the broad ASD phenotype
(Constantino et al., 2006). Levels of social responsivity
in twin-pairs are associated even when neither twin is
diagnosed with an ASD (Constantino & Todd, 2003).
ASDs are typically not diagnosed until late toddler-
hood or pre-school age. Parents, however, report that
the mean age of ASD symptom recognition is between
16 and 20 months (Chakrabarti & Fombonne, 2005;
Ozand, Al Odaib, Merza, & Al Harbi, 2003; Short &
Schopler, 1988; Spitzer & Siegel, 1990; Volkmar, Stier,
& Cohen, 1985) and many parents report developmen-
tal deficits within the first year of life (Zwaigenbaum
et al., 2005). Little, however, is known about ASD-
related deficits in infancy. ASDs occur in approxi-
mately one in every 150–250 pre-school children,
making the disorder too rare to study prospectively
in the general population (Bryson & Smith, 1998;
Chakrabarti & Fombonne, 2001).
Retrospective studies of home videotapes suggest that
deficits are present as early as 3–8 months of age in
infants who are later diagnosed with autism (Adrien,
Faure, Perrot, & Hameury, 1991; Werner, Dawson,
Osterling, & Dinno, 2000; Werner & Dawson, 2005;
Werner, Dawson, Munson, & Osterling, 2005). Parent
report may be confounded by selective recall, at times
lack of knowledge about development, and difficulties
associated with admitting developmental difficulties in
their child (Chawarska & Volkmar, 2003; Stone, Hoff-
man, Lewis, & Ousley, 1994), making prospective exam-
ination of the development of ASDs important. This is
the rationale for the current study of the early autism
phenotype in young siblings of children with ASD.
We investigated whether infant siblings of children
with an ASD (ASD-sibs) showed developmental dif-
ferences associated with the broad ASD phenotype
between the ages of 6 and 18 months. We compared
ASD-sibs to infants with typically developing siblings
(TD-sibs) and focused on early measures of emotion
expressed in parent–child interactions and later mea-
sures of joint attention.
Emotional Expression and the Broad ASD
The first degree relatives of individuals with autism
evidence an increased expression of personality charac-
Wzorek, Landa, & Lainhart, 1994; Wolff, Narayan,
& Tanguay, 1995). They also show increased expression
of personality traits such as anxiousness, impulsiveness,
and irritableness (Murphy et al., 2000).
Retrospective studies of the early development of
children with autism suggest thatattenuationof positive
affect, or of the tendency to socially direct positive
affect, may be one of the earliest markers of atypical
development (Baranek, 1999; Osterling, Dawson, &
Munson, 2002; Wimpory, Hobson, Williams, & Nash,
2000). Parents of a child with an ASD perceive their
child’s emotional expressions to be more negative and
less positive than parents of children who are mentally
retarded (Capps, Kasari, Yirmiya, & Sigman, 1993).
The face-to-face/still-face (FFSF) is an interactive
protocol useful for assessing the positive and negative
emotional expressivity of infants (Adamson & Frick,
2003; Tronick, Adamson, Wise, & Brazelton, 1978).
Parents are asked to play normally with their infant,
hold a still face, and then resume play. Positive engage-
ment declines and negative engagement increases when
the parent ceases play and holds a still face (Tronick
et al., 1978). The resumption of play in the reunion is
characterized by moderate levels of both positive and
negative emotional expressions (Moore, Cohn, &
Campbell, 2001). In normative (Weinberg, Tronick,
Cohn, & Olson, 1999) and at-risk (Acosta, Messinger,
Cassel, & Bauer, 2004) samples, infants showed be-
tween-episode stability in emotional expressivity. Lev-
face (FF), still face (SF), and reunion (RE) episodes, as
are levels of positive affect.
Children with autism display flatter or more neutral
(Yirmiya, Kasari, Sigman, & Mundy, 1989). In a recent
prospective study, 4-month-old ASD siblings showed
more neutral affect than TD siblings in response to a
maternal SF. Fewer ASD than TD siblings engaged in
differences in negative affect did not achieve signifi-
cance (Yirmiya et al., 2006). In another prospective
study, 12-month-old ASD siblings who later revealed
autistic symptomatology showed deficits in social smil-
ing, displaying less positive emotion than typically
developing infant siblings (Zwaigenbaum et al., 2005).
Weexpected ASD-sibstodisplayless positive andmore
negative emotion in the FFSF than TD-sibs at 6 months
of age, but also expected they would have a propensity
toward neutral, potentially disengaged, affect.
Referential Communication and the Broad ASD
Referential communication involves conventional ges-
tures used to attain objects and responses to and
J Autism Dev Disord
initiations of joint attention. The Early Social Commu-
nication Scales (ESCS) were developed to assess for
these early communicative behaviors in young children
who do not yet use language as their primary mode of
communication (Mundy, Hogan, & Doehring, 1996;
Mundy et al., in submission). IJA refers to the use of
communicate about an object or event in the environ-
ment (Jones & Carr, 2004; Messinger & Fogel, 1998).
IJA behaviors are precursors to language and may be
especially important as predictors of later differences in
social, cognitive, and behavioral outcomes. IJA behav-
iors at 18 months predict language development at
2 years of age (Mundy et al., in submission). Deficits in
IJA (Baranek, 1999; Jones & Carr, 2004) and other
broader social deficits (Werner et al., 2005) are com-
mon in children with an ASD, and are frequently
evident in children with early onset (e.g., non-regres-
sive) autism before 1 year of age. In fact, such deficits
discriminate approximately 80–90% of children with
autism from children with other developmental delays
(Lewy & Dawson, 1992; Mundy, Sigman, Ungerer, &
Sherman, 1986), but not until after the first birthday. In
a recent study, ASD siblings (14–19 months of age)
exhibited significantly less IJA than young TD children
(10–19 months of age) (Goldberg et al., 2005).
Responding to joint attention (RJA) refers to the
child’s ability to follow the joint attention behavior
(i.e., pointing) of the examiner. Associations have been
found between RJA and later language development
in infants between 6 and 18 months of age (Morales
et al., 2000). Examinations of RJA in young ASD
siblings have yielded mixed results (Goldberg et al.,
2005; Presmanes, Walden, Stone, & Yoder, 2007;
Yirmiya et al., 2006). While Yirmiya et al. (2006)
found no RJA differences between groups, others
have found ASD-sibs to show RJA decrements (Gold-
berg et al., 2005) and related deficits in responding to
an adult’s referencing behaviors (Presmanes, Walden,
Stone, & Yoder, 2007).
requests for help or an object (Mundy et al., 1996).
Lower level IBR behaviors include making eye contact
in order to request a toy or reaching toward a toy.
Higher level IBR behaviors include pointing at a
desired toy or giving the examiner a toy. Yirmiya et al.
(2006) found that ASD siblings engaged in fewer
higher-level IBRs than TD-sibs while Goldberg et al.
(2005) found ASD-sibs engaged in significantly less
IBR of all types than young TD children. We expected
ASD-sibs to display lower levels of IJA, RJA, and IBR
than TD-sibs during the Early Social Communication
Scales (ESCS) between 8 and 18 months of age.
Infants with older siblings (N = 31) were assessed with
respect to their social and emotional functioning in the
first year and a half of life. Infants in this study were
part of a larger sample investigating the social, emo-
tional, and cognitive development of ASD-sibs and
TD-sibs. Infants were included in this sample if they
participated in a 6-month assessment and participated
in at least one of the 8, 10, 12, 15, or 18-month
There were twelve ASD-sibs. Eleven infants had
older full-siblings on the autism spectrum and one
infant had a half-sibling on the autism spectrum
(included in the ASD-sibs group). There were 19
TD-sibs. The status of the older sibling was obtained by
parent report at the initial telephone contact. Infants
were included in the ASD-sibs group if their older
sibling was diagnosed with Autism, Asperger’s Disor-
der, or Pervasive Developmental Disorder-Not Other-
wise Specified (PDD-NOS). We are currently in the
process of confirming this information via independent
assessments conducted at our laboratory. Currently, 15
TD-sibs are 18 months of age or older and six ASD-
sibs are 18 months of age or older. The older typically
developing siblings ranged in age from 2.22 to
15.18 years (M = 6.66, SD = 3.29) and the older sib-
lings diagnosed with an ASD ranged in age from 3.56
to 11.27 (M = 7.25, SD = 2.55), a non-significant dif-
ference, p = .60. The TD-sibs were Hispanic (36.8%),
Caucasian (47.4%), African American (5.3%), Asian
(5.3%), and biracial (5.3%). The ASD-sibs were
Hispanic (66.7%) and Caucasian (33.3%).
All infants participated with a parent in the FFSF
protocol(Tronick,Als,& Brazelton,1977) atameanage
of 6.15 months (SD = .33; range 5.03–6.87 months).
There was no age of FFSF administration difference
betweengroups,p > .50.IntheFFSFparentswereasked
to play with their baby without toys for 3 minutes (FF),
stop playing and maintain a still face with no emotional
expression for 2 minutes (SF), and resume play for
another 3 minutes (RE). Infants were placed in a car
seat during the FFSF and videotaped with two separate
cameras to ensure the best view possible of their faces.
The presence of infants’ smiles and cry-faces in the
FFSF were coded bycoderscertifiedinthe FacialAction
Coding System (FACS) (Ekman & Friesen, 1978) and
trained in its application to infants, BabyFACS (Oster,
J Autism Dev Disord
2000, Unpublished monograph and coding manual).
Smiles and cry-faces are, respectively, infants’ proto-
typical expressions of positive and negative emotion.
The upward turning of the lip corners produced by the
contraction of the zygomatic major defines smiling
(AU12). In cry-faces, the lips are stretched laterally by
the risorius muscle (AU20) and the brows are lowered
by the corrugator muscle (AU4). Neutral affect
consisted of the proportion of time in which the infant
was not smiling or exhibiting a cry-face. Approxi-
mately 23% of infants were coded for reliability with
mean 86% agreement between coders (mean j = .67).
The main and reliability coders were not blind to
FFSF episodes were terminated if the infant cried
for >20 s or if the parent elected to terminate the
episode. One parent of an ASD-sib elected to stop the
FFSF procedure after the FF episode because her infant
was upset. Thus, this child was included only in the FF
portion of the analyses and not in the SF, RE, or
elsewhere. The durations of the episodes can be found
in Table 1. The FF episode was significantly shorter for
ASD-sibs than TD-sibs F(1, 29) = 4.41, p = .05. There
were no duration differences for the SF or RE episodes.
All analyses were conducted using the proportion of
time spent either smiling, in a cry face, or with a
neutral expression as the dependent variable. In order
to calculate the proportion of time infants were
engaged in neutral, smiling, and cry-face expressions
during a given FFSF episode, the duration of the
expression was divided by the duration of the episode
excluding time during which the coder could not see
the face of the child (see Table 2). We also created
time-based (not episode-based) proportions of neutral,
smiling, and cry-faces throughout the FFSF protocol
(excluding time in which the coder could not see the
face of the child). Doing so allowed us to include data
from all infants enrolled in the study, including the
child who completed only the FF portion of the FFSF.
Because the FF and RE episodes had baseline dura-
tions of 3 minutes, and the still-face 2 minutes, the
total proportion variables were not simply the sum of
the proportions of smiling or cry-faces in each episode
(see Table 2).
To examine stability of smiling and cry-faces across
FFSF episodes, correlations were calculated for each
group. These correlations were transformed to Z-
scores to test for differences in the stability of inter-
episode emotional expression between the two groups
(Meng, Rosenthal, & Rubin, 1992).
All infants were administered the Early Social
Communication Scales (ESCS) (Mundy et al., 1996)
at least once between 8 (M = 8.24, SD = .25), 10
(M = 10.41, SD = .28), 12/13 (M = 12.79, SD = .61),
15 (M = 15.41, SD = .43), and 18 months (M = 18.23,
SD = .41) of age. There were eight infants who partic-
ipated in only one visit, four infants who participated in
two visits, five infants who participated in five visits,
seven infants who participated in four visits, and seven
infants who participated in all five visits. The number of
participants at each assessment can be found in Table 3.
The ESCS is a semi-structured assessment which elicits
early social communication, particularly joint attention
and behavioral requesting, and the sharing of positive
affect with an examiner. Parents are instructed not to
initiate contact with their child while their child sits on
their lap and is presented with attractive toys and
objects by an examiner. The ESCS, which is designed
for children between the ages of 8 and 24 months, takes
approximately 15–25 minutes to administer.
Responding to joint attention refers to the child’s
ability to follow the joint attention behavior (i.e.,
pointing) of the examiner. RJA was coded when
infants followed the examiner’s point combined with a
vocalization (i.e., the child’s name) to a distal stimulus.
IJA refers to a child’s ability to share his or her
interest or joy in an object. IJA was coded when
infants made eye contact with the experimenter while
manipulating a static or active toy or alternated eye
contact between a distal, active mechanical toy and the
experimenter. If an infant alternated eye contact after
a mechanical toy became inactive, IJA episodes were
only coded within 2 seconds of the time the toy
became inactive. This ensured that the infant’s behav-
ior was indeed related to the object. Episodes in which
the experimenter’s overt behaviors (e.g., talking or
moving) may have elicited the infant’s attention were
Table 1 Duration (in
minutes) of the face-to-face/
still-face (FFSF) episodes
* Significant group difference
p £ .05
Episode Autism Spectrum Disorders
Typically developing siblings
n Mean (SD) Rangen Mean (SD) Range
Face to face (FF)
Still face (SF)
J Autism Dev Disord
There are both lower and upper level behaviors
associated with IJA. Lower level IJA behaviors include
gazing at an examiner while watching or holding an
active toy, or making eye contact while holding or
touching an inactive toy. Higher level IJA behaviors
include pointing, with or without eye contact, at an
object of interest or clearly holding up a toy and
showing it to the examiner.
Episodes of IBR refer to requests for help or
responses to a direct question. IBR occurs when the
child requests something from another person or would
like the person todosomething for him or her.There are
lower and higher level IBR behaviors. Lower level IBR
behaviors include making eye contact to request a toy or
Higher level IBR behaviors include pointing at a desired
toy, either with or without eye contact, or giving the
examiner a toy, either with or without eye contact.
The ESCS was coded by two main coders and one
reliability coder. One of the main coders was blind to all
but 2 infants’ status, and the other main coder was blind
to all but 13 infants’ status. The reliability coder was not
blind to subject status. Each main coder coded each
child in at least one time point. Approximately 20% of
infants were double coded by a reliability coder with
mean intra-class correlations of ‡.70 for all behaviors
coded including lower level IJA, higher level IJA, total
IJA, lower level IBR, higher level IBR, total IBR, and
RJA. The occurrence of each of these behaviors was
expressed as a rate per minute with respect to the total
duration of the ESCS with the exception of RJA which
was expressed as the number of correctly followed trials
(out of 8 trials). These variables were used in all
subsequent analyses. Due to the low number of children
present at every one of the longitudinal assessments
(TD-sibs n = 5, ASD-sibs n = 2), we were unable to
conduct a repeated measures ANOVA for the ESCS
variables. Instead, we compared groups at each age
using two-tailed tests with an alpha level of .05. Only
approximately half of the sample was 2 years of age or
older, the age of our first standardized developmental
assessment, at time of writing. This precluded matching
participants on developmental and cognitive measures
(Shaked & Yirmiya, 2004).
To screen for group and protocol differences in the
FFSF, we used 2 (group) by 3 (episode) separate
Table 2 Proportion of time spent smiling, in cry-faces, and in neutral affect in the face-to-face/still-face (FFSF)
Episode Smile mean (SD)p (d)Cry-face mean (SD)p (d) Neutral affect mean (SD)p (d)
ASDTD ASD TDASD TD
Face to face (FF)
Still face (SF)
Note: The total variable is not the sum of the proportions in each episode (which differ in length) but the proportion of either smiling,
in cry-faces, or in neutral affect in the total time in the FFSF
Table 3 Mean levels of behaviors in the early social communication scales
Agen Total initiating
p (d)Lower initiating
p (d)Passed responding to
joint attention (RJA)
ASD TD ASD TD ASDTD ASD TDASD TD
8 Months9 16.80
.69 .07 .12
(.50) (1.40) (1.14)
(.67) (.86) (1.79)
10 Months8 14 .56 .172.38
12/13 Months 6 10.49.141.60
18 Months610 .67.513.17
J Autism Dev Disord
repeated measures Analysis of Variance (ANOVA).
We conducted these analyses and their follow-ups
using the proportion of time first in smiles, then in cry-
faces, and finally in neutral as dependent measures.
The use of these proportions corrects for differences in
the duration of episodes between infants. The one child
who did not complete the entire FFSF protocol was
excluded from all repeated measures analyses but was
included in the analyses focusing on the FF episode.
The repeated measures ANOVA of smiles produced a
still-face effect in that smiling decreased during the SF
portion of the FFSF, F(2, 28) = 5.01, p = .03, gp
(see Fig. 1). There were no significant status or
interaction effects, ps > .40. However, our planned
time-based group contrast of the entire FFSF protocol
indicated that ASD-sibs smiled significantly less than
TD-sibs over the entire FFSF protocol t(29) = 2.21,
p = .04, gp
analyses revealed a non-significant trend for ASD-sibs
to smile less than TD-sibs in the FF portion of the
FFSF only, t(29) = 1.86, p = .07, d = .69 (see Table 2).
A repeated measures ANOVA indicated that
infants also showed a still-face effect such that time
exhibiting cry-face expressions increased during the SF
portion of the FFSF, F(2, 28) = 4.96, p = .03, gp
for all infants (see Table 2). There were no interaction
or status effects for cry-face expressions.
In a 2 (group) by 3 (episode) design, there were no
group differences in neutral affect (times in which the
infant was not smiling or exhibiting a cry-face),
p = .12(see Table 2 and Fig. 2). Our planned time-
based group contrast of the entire FFSF protocol
indicated that there was a trend for ASD-sibs to show
more neutral affect than TD-sibs in the RE portion of
the FFSF, but this effect was not significant, t(28) = –
2.00, p = .06, d = –.77. There were no significant
neutral affect differences between the groups over
the course of the FFSF protocol.
2= .14 (see Table 2). The planned follow-up
Correlations of levels of expressive behaviors
across the FFSF episodes revealed group differences
(see Table 4). Both groups showed comparable levels
of smiling stability between the FF and RE episodes.
TD-sibs, but not ASD-sibs, showed stable levels of
cry-faces between the FF and SF (Z¢ = 2.49, p = .01),
and between the SF and RE episodes (Z¢ = 2.00,
p = .05). ASD-sibs, but not TD-sibs, showed an
unexpected positive correlation between cry-faces in
the FF and smiling in the SF (Z¢ = 2.46, p = .01).
These effects reflect both differences between the
significance and non-significance of each group’s
correlations and significant differences between the
Early Social Communication Scales
The mean rate per minute of IJA in the ESCS can be
found in Table 3. Preliminary analyses of higher-level
and lower-level IJA revealed expected low rates of
higher-level IJAs through 12 months. Results for lower-
level IJAs mirrored those for total IJA, which are
reported here. ASD-sibs had a smaller proportion of
total IJA than TD-sibs
t(15.84) = 3.05, p < .01, d = 1.34.1There were no status
differences in rates of high and low IJA at any other age.
ASD-sibs responded to the examiner’s joint atten-
tion bids (RJA) fewer times than TD-sibs at 18 months
of age, t(14) = 2.36, p = .03, d = 1.18 (see Table 3).
There were no status differences in RJA at other ages.
The mean rate per minute of IBR in the ESCS can
be found in Table 3. ASD-sibs engaged in less higher
level IBR at 12 months of age, t(11.90) = 2.99, p = .01,
d = 1.401There were no group differences for this
variable at other ages.
at 15 monthsof age,
Face to FaceStill Face
Fig. 1 Smiling in the face-to-face/still-face (FFSF)
Face to FaceStill Face
Fig. 2 Neutral affect in the face-to-face/still-face (FFSF)
1Levene’s Test indicated a significant difference between group
variances, prompting the correction evident in the non-integer
J Autism Dev Disord
In order to determine if there were associations among
emotional expressions in the FFSF and indices of joint
attention and related competencies in the ESCS, we
correlated the total proportion of time spent smiling,
exhibiting a cry-face, or in neutral affect in the entire
FFSF protocol with average rates of IJA, RJA, and
high and low IBR at all ages. There were no significant
correlations for the ASD-sib group, the TD-sib group,
or both groups combined.
Infant siblings of children with autism are at increased
risk for developing an ASD or deficits within the broad
phenotype. Much research on the early deficits asso-
ciated with ASD has been conducted retrospectively
making it difficult to ascertain valid levels of early
functioning. In this current prospective study, we
examined the broad phenotype of ASD in the younger
siblings (between the ages of six to eighteen months) of
children diagnosed with ASD. We found evidence for
some differences between ASD-sibs and TD-sibs as
early as six months of age and inconsistent differences
in IJA, RJA, and IBR.
At six months of age, ASD-sibs smiled for a
significantly lower proportion of time during the FFSF
protocol with their parent than did TD-sibs. There was
a non-significant trend for ASD-sibs to exhibit more
neutral affect than TD-sibs in the reunion portion of
the FFSF. ASD-sibs engaged in significantly lower
rates of IJA than TD-sibs in the ESCS at 15 months
and in lower rates of higher-level IBR at 12 months.
They also responded to the joint attention bids of the
examiner (RJA) significantly less frequently than TD-
sibs at 18-months of age.
Limitations of the study include its small sample size
and the lack of ESCS measures from each participant at
each age and lack of outcome data for the siblings. Not
and their longitudinal patterns of attendance for the
ESCS administrations were variable. The small number
of children present at each and every longitudinal
assessment precluded the use of a repeated measures
ANOVA for the ESCS variables. Multiple comparisons
conducted for the FFSF variables and an alpha level of
.05 increased the possibility that significant group
differences might emerge by chance. We adopted these
strategies so as to not overlook potentially important
behavioral differences between ASD-sibs and TD-sibs
in this initial sample. Nevertheless, results should be
body of research characterizing the developing ASD
Using overall time in the FFSF as the metric for
comparison, ASD-sibs smiled less than TD-sibs, a large
Table 4 Correlations between infant smiling and crying in the face-to-face/still-face (FFSF)
Episode FF-smile SF-smileRE-smileFF-crySF-cry RE-cry
Typically developing siblings (TD-sibs)
Autism Spectrum Disorders (ASD)-sibs
Face to face (FF)-smile
Still face (SF)-smile
* p £ .05, ** p £ .01
Note: An underlined correlation indicates that these effects reflect both differences between the significance and non-significance of
each group’s correlations and significant differences between the correlation coefficients at p £ .05
J Autism Dev Disord
effect size explaining 14% of the variance. An episode-
based repeated-measures examination of these did not
reveal thiseffect. Thisdiscrepancyreflectstheincreased
impact of the FF and RE episodes of the protocol in the
time-based analysis. It also reflects the influence of an
and did not complete the remainder of the FFSF
protocol. Yirmiya et al. (2006) did not find smiling
deficits in ASD-sibs at 4 months. The current results
nevertheless mirror reports of positive affect attenua-
tion in prospective and retrospective studies involving
& Poustka, 2003; Bolton et al., 1998; Capps et al., 1993;
Murphy et al., 2000; Osterling et al., 2002; Wimpory
et al., 2000; Yirmiya et al., 1989). Our findings are
similar to parental reports of a reduction of emotionally
positive behaviors during the play of children with ASD
(Capps et al., 1993). Like Yirmiya et al. (2006), we
found no differences in infants’ mean levels of negative
facial expressions during the FFSF.
There was a tendency for ASD-sibs to show greater
neutral affect than TD-sibs during the reunion episode
of the FFSF. This trend was non-significant and not
independent of the smile and cry-face results (neutral
affect was defined as their absence). Nevertheless, it is
similar to Yirmiya et al.’s (2006) findings of greater
ASD-sib affective neutrality during the still-face
portion of the FFSF protocol. It is noteworthy that
these findings of heightened neutral affect occurred in
the typically stressful still face and reunion episodes,
which present a challenge to the emotional regulation
capacity of infants. Our findings are also consistent
with observations of decreased smiling and of parent
reports of passivity and a decreased activity level using
the infant behavior questionnaire (IBQ) in 12-month-
old ASD-sibs who proceeded to an ASD diagnosis
(Zwaigenbaum et al., 2005). A growing literature
suggests that reductions in affect expression manifested
both as atypical neutrality and reductions in positive
emotion are characteristic of the broad ASD pheno-
type in the first year of life.
TD-sibs showed continuity in facial expressions of
negative affect between the FF and SF and between
the SF and RE portions of the FFSF at four months.
These continuities also have been documented in
at-risk and normative samples (although gender
differences with regard to emotional continuity have
also been noted) (Acosta et al., 2004; Weinberg et al.,
1999). ASD-sibs, however, had non-significant levels of
negative emotional continuity and their levels of
continuity were significantly lower than those of TD-
sibs. Both groups showed continuity in levels of smiling
between the FF and RE episodes. However, ASD-sibs
who smiled more in the SF, a period of parental non-
responsivity, showed greater negative affect when their
parent re-engaged with them. These findings, com-
bined with research suggesting that early ASD-related
passivity is followed developmentally by increased
distress and negativity (Zwaigenbaum et al., 2005),
suggest a pattern of emotional instability and dysregu-
lation. We did not find developmental continuities
between emotional expression and referential commu-
nication difficulties, suggesting that much remains to be
learned about the development of ASD-linked pat-
terns of communicative development in the first
2 years of life.
Yirmiya et al. (2006) examined ASD-sib infant-
mother synchrony in a free play FF episode, finding
that synchrony was weaker in the SIBS-A dyads, only
for infant-lead/mother-follow interactions. A limitation
of the current study is that neither maternal expres-
sions nor dyadic synchrony were examined. Neverthe-
less, it may be that ASD-sibs’ potential emotional
lability makes it more difficult for mothers to follow
changes in their infants’ moment-to-moment levels of
emotional engagement and valence.
We investigated potential deficits in referential
communication by examining IJA, RJA, and IBR
during repeated administrations of the ESCS between
8 and 18 months of age. ASD-sibs initiated a lower rate
of total IJA than TD-sibs at 15-months of age.
Although this was a large difference accounting for
22% of the variance, no differences were found at
other ages. Unreported analyses indicated a lack of
significant differences in rates of high and low IJA
behaviors at any age. Such inconsistent findings also
characterize the existing literature. Goldberg et al.
(2005) reported that ASD-sibs showed deficits in IJA
and did not differ significantly from their older affected
siblings. Yirmiya et al. (2006), however, found no IJA
deficits at 14 months of age.
ASD-sibs responded to the joint attention bids of
the examiner less than TD-sibs at 18-months of age, a
large effect size accounting for 29% of the variance.
Previous research has shown ASD-sibs in the second
year of life have more difficulty locating the target of
an adult’s attention than do TD-sibs (Presmanes,
Walden, Stone, & Yoder, 2007). Specific examinations
of RJA in the ESCS in the first 2 years of life have
yielded both reports of no differences (Yirmiya et al.,
2006) and findings of an ASD-sib RJA decrement
(Goldberg et al., 2005). The findings suggest that
ASD-sibs may have difficulties in either understand-
ing or responding to an adult’s conventional request to
orient attention to an object. These difficulties are
J Autism Dev Disord
consonant with deficits in children with ASDs who are
less likely to respond to the examiner’s joint atten-
tion bids than are typical children and children
diagnosed with other developmental delays (Dawson
et al., 2004).
Deficits in initiating and RJA bids are core deficits
in children with ASD (Baranek, 1999; Dawson et al.,
2004; Jones & Carr, 2004; Lewy & Dawson, 1992;
Mundy et al., 1986; Werner et al., 2005). In early joint
attention bids, infants share their interest in an object
or event with another. In responding to these bids,
infants manifest their understanding of conventional
attempts to engage another’s attention. The early—
albeit inconsistent—differences in these abilities doc-
umented here may be important precursors to Theory
of Mind (ToM) abilities. A decreased propensity to
engage the attention of others and to respond to their
bids for attention may contribute to deficits in the
ability to understand mental states of others, a devel-
oping disability in individuals on the autism spectrum
(Baron Cohen, Leslie, & Frith, 1985; Mundy, 1995).
ASD-sibs showed fewer higher-level behavioral
requests than ASD-sibs at 12 months of age, a large
effect accounting for more than 20% of the variance.
Although we did not observe differences at 8, 10, 15, or
18 months of age, others have also observed deficits in
requesting. Yirmiya et al. (2006) found that ASD-sibs
engaged in fewer higher-level behavioral requests at
14-months of age than TD-sibs and Goldberg et al.
(2005) found that ASD-sibs (14–19 months of age)
engaged in less overall IBR than young TD children
(10–19 months of age).
This paper contributes to a growing body of research
suggesting deficits in requesting behaviors—particularly
higher-level conventional requests such as points—
among ASD-siblings during the second year of life. This
may reflect difficulties in engaging socially to attain
desired objects or acts. Specific ASD-sib deficits in
generating conventional requests may index an inability
to employ socially learned communicative behaviors,
such as pointing, to achieve their goals. Such deficits are
common among children on the autism spectrum
(Osterling & Dawson, 1994) and may be an early
manifestation of the tendency of children with ASD to
requesting behaviors with others (Stone & Caro-Marti-
In sum, ASD-sibs appear to show a range of
inconsistent, but potentially related, difficulties with
referential communication. These include subtle diffi-
culties in IJA, later developing difficulties in respond-
ing to these joint attention bids, and deficits in
requesting, particularly in conventional requests. These
deficits in referential communication all occurred in
the second year of life. A likely explanation is that such
complex referential skills involving the more inten-
tional use and comprehension of gaze and its coordi-
nation withmore conventional
crystallizing and developing during this period. Only
as TD-sibs integrate these behaviors into their reper-
toires at stable levels in the second year of life are
differences with ASD-sibs likely to emerge. Another
possibility is that ASD-sibs may have a tendency
toward passivity in interactions that is manifested in
neutral affect in early infancy and scattered difficulties
with IJA and IBR later in toddlerhood.
Heterogeneity among ASD-sibs is also likely to
play a role in the inconsistent nature of the current
findings. This preliminary study focused on group
comparisons of infants with siblings on the autism
spectrum and those with typically developing siblings.
Unfortunately, only two of the ASD-sibs have com-
pleted the ADOS-G, a well-validated measure of
ASD symptomatology (Lord, Rutter, DiLavore, &
Risi, 1999). In addition, only approximately half of the
sample is 2 years of age or older, the age of our first
standardized developmental test (the Mullen Scales of
Early Learning). As standardized measures of ASD
severity are completed, we will investigate whether,
within the ASD-sibs group, children who go on to an
ASD diagnosis differ from children who do not attain
this diagnosis but go on to show deficits associated
with the broad ASD phenotype (i.e. language delay or
sensory impairment) and whether such children, in
turn, differ from ASD-sibs who develop none of these
symptoms. It will be particularly important to deter-
mine if ASD-sibs who are later diagnosed with an
ASD evidence differences in emotional expressions
and rates of IJA, RJA, and IBR when compared to
more typically developing ASD-sibs. Continued lon-
gitudinal study may also reveal ASD-sibs who show
regression in development. Such infants may show
typical development within the time frame considered
in this study but show regressive increases in ASD
symptomatology after 18 months of age. Some studies
suggest that 20–40% of cases follow this developmen-
tal trajectory (Kobayashi & Murata, 1998; Maestro
et al., 2002; Rogers, 2004).
We have noted subtle deficits in early emotional
expression andlater referentialcommunication abilities
in ASD-sibs that may index important early difficulties
in emotional communication associated with the broad
phenotype of ASD. We did not find developmental
continuities between emotional expression and refer-
ential communication difficulties, suggesting that much
remains to be learned about the development of ASD-
J Autism Dev Disord
linked patterns of communicative development in the
first 2 years of life. Recent research suggests that
children diagnosed with an ASD who undergo early
and intensive intervention have better outcomes when
compared to individuals who receive treatment later in
life (Kazdin & Weisz, 2003). This paper contributes to a
growing body of literature suggesting subtle, communi-
cative deficits for ASD-sibs in the first 2 years. Deter-
phenotype in the first 18 months of life and diagnosable
ASD that can benefit from intervention remains a topic
for continued research.
participating in this research. Funding for this study was
provided by a grant from NICHD (047417).
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