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2000 John Wiley & Sons, Inc.

Peter M undyDepartment of Psychology

University of MiamiMiami, FL 33146

Judith Card

N athan FoxDepartment of Human Development

University of MarylandCollege Park, MD 20740

EEG Cor relates of the

D evelopm ent of I nfant Joint

Attention Skills

Received 19 August 1999; accepted 7 December 1999

ABSTRACT: The development of the capacity for social attention coordination, or jointattention, is a major milestone of infancy. Data from a recent study of handicapped infantshave raised the hypothesis that the tendency to initiate bids for joint attention may reflect

processes associated with the frontal cortex to a greater extent than other forms of infantattention coordination (R. Caplan et al., 1993). This hypothesis was examined in a longitudinalstudy of 32 normally developing infants. The results indicated that EEG data at 14 monthsindicative of left frontal, as well as left and right central cortical activity, was associated withthe tendency to initiate joint attention bids (IJA) at 14 and 18 months. In contrast, a patternof left parietal activation and right parietal deactivation at 14 months was associated with thedevelopment of the capacity to respond to the joint attention bids (RJA) of others at 14 and 18months. These results were interpreted to be consistent with a general anterior posterior modelof attention development (M. Posner & S. Petersen, 1990). The implications of these results

for current conceptualizations of joint attention development, as well as for understanding thedisturbance of joint attention skill development in autism are discussed. 2000 John Wiley &Sons Inc. Dev Psychobiol 36: 325338, 2000

Keywords: EEG; joint attention; infant development

The acquisition of the ability to coordinate attention

with a social partner is a major milestone of infancy

that is critical to infants active participation in social

learning opportunities (e.g., Adamson, 1995; Baldwin,

1993; Butterworth & Jarrett, 1991; Corkum & Moore,

1997; Mundy & Willoughby, 1998; Scaife & Bruner,

1975; Trevarthen, 1979; Tomasello, Kruger, & Ratner,

1993; Werner & Kaplan, 1963). Consistent with this

view, individual differences in this capacity among in-

fants have been observed to be significantly related to

Correspondence to: P. MundyContract grant sponsor: NICHDContract grant number: 26768Contract grant sponsor: NIDCDContract grant number: 00484

intellectual, language, and social development (e.g.,

Carpenter, Nagell, & Tomasello, 1998; Claussen,

Mundy, & Willoughby, 1999; Morales, Mundy, & Ro-

jas, 1998; Mundy & Gomes, 1998; Sheinkopf, Mundy,

Willoughby, & Claussen, 1999; Tomasello; 1995; Ul-

vund & Smith, 1996). Thus, understanding the nature

of individual differences in infant attention coordina-

tion is an important issue in the study of early devel-

opment (Mundy & Gomes, 1998).

Understanding these individual differences, how-

ever, is complicated by the observation that there are

different types of infant attention coordinating behav-

iors that may reflect distinct as well as common pro-

cesses (Mundy & Gomes, 1997). One category of be-

haviors has been referred to as protoimperative, or


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326 Mundy, Card, and Fox

requesting skills, in which infants initiate or respond

to bids for coordinated attention to elicit aid in obtain-

ing an object or event (Bates, Benigni, Bretherton, &

Camaioni, 1979; Bruner & Sherwood, 1983; Seibert,

Hogan, & Mundy, 1982). Examples include using eye

contact and reaching to obtain a distal toy, or respond-ing to a palm-up hand gesture to give an object to a

social partner. Another category of coordinated atten-

tion involves a less instrumental and more social func-

tion of sharing experience with others vis-a-vis an ob-

ject or event. These are called joint attention or

protodeclarative behaviors (Bates et al., 1979; Bruner

& Sherwood, 1983). As with requesting skill, infants

may initiate or respond to joint attention bids. In the

nomenclature of this article, responding to joint atten-

tion (RJA; Seibert et al., 1982) refers to the ability to

monitor and correctly follow gestures, such as point-

ing, and/or a shift in the direction of gaze and the head

orientation of others (Butterworth & Jarrett, 1991;Scaife & Bruner, 1975). Initiating joint attention skill

(IJA; Seibert et al., 1982) refers to the use of eye con-

tact and gestures, such as showing or alternating eye

contact, to spontaneously establish episodes of shared

attention with others vis-a-vis some object or event

(Bates, Camaioni, & Volterra, 1975; Mundy, Kasari,

& Sigman, 1992).

Recently, data have been presented that suggest that

individual differences in IJA may display a specific

association with frontal cortical processes. Caplan et

al. (1993) used Positron Emission Tomography (PET)

to examine cortical metabolism in a small sample of13 infants and toddlers prior to hemispherectomy for

intractable seizure disorder. Higher rates of preopera-

tive glucose metabolism in the prefrontal region, es-

pecially the left frontal region, was a positive predictor

of the postoperative tendency to initiate joint attention

bids but was not a predictor of other types of social

attention coordination skills. Thus, processes associ-

ated with the left frontal cortex may distinguish the

development of the tendency to initiate joint attention

bids relative to other infant attention coordinating be-

haviors. Several lines of theory are consistent with this

observation.

Working memory and related dual-task processing

(Stuss, Shallice, Alexander, & Picton, 1995), as well

as the representational encoding of stimuli (Goldman-

Rakic, 1987), may be a fundamental function of the

frontal cortex. Initiating joint attention skill may also

involve a working memory and representational de-

mands wherein infants hold information on line about

their own focus of interest (e.g., a toy) while attending

to and interacting with a social partner. Moreover,

these demands may be greater in IJA than in other

types of social attention coordinating bids, such as re-

questing acts (Baron-Cohen, 1989, 1995).

Frontal functioning may also be involved in the de-

velopment of infants ability to inhibit responses. For

example, infants are increasingly able to tolerate delay

in the A not B task in the first year of life (Diamond,1988) and this has been related to increased left frontal

EEG activation (Bell & Fox, 1992). Initiating joint

attention may involve inhibiting visual regard for an

object in order to share attention to a greater extent

than requesting skills (McEvoy, Rogers, & Penning-

ton, 1993). Indeed, behavioral response inhibition has

been associated with initiating joint attention skill, but

not other forms of infant attention coordination be-

haviors, in developmentally disordered children

(McEvoy et al., 1993; Giffith, Pennington, Wehner, &

Rogers, 1999).

Finally, in addition to cognitive processes, the de-

gree to which spontaneously sharing attention be-comes rewarding for infants may effect their tendency

to initiate joint attention bids (Mundy, 1995; Mundy

et al., 1992; Mundy & Willoughby, 1998). Alterna-

tively, social reward sensitivity or experience may

play a lesser role in the more instrumental functions

of requesting bids (Mundy, 1995). Frontal systems, in

turn, may play a role in integrating the reinforcement

value of the stimuli or motivational processes with

cognitive factors in the regulation of behavior

(Thorpe, Rolls, & Maddison, 1983). Moreover, a func-

tional lateralization has been observed such that, by

10 months, behaviors associated with positive indicesof social motivation, including social orienting, posi-

tive affect, and approach behaviors, are also related to

left frontal processes (Fox, 1991; Fox & Davidson,

1987). Thus, individual differences in a left frontal

system involved in the mediation of positive social

motivation may play a more important role in the de-

velopment of the capacity to initiate joint attention

bids than in other forms of infant attention coordina-

tion (Mundy, 1995; Mundy & Willoughby, 1998).

These elements of theory make a cogent case for

the involvement of frontal processes in IJA develop-

ment. However, the results of Caplan et al. (1993),

which provide an initial basis for this hypothesis, may

only be viewed as preliminary because they were

based on a small sample whose development was com-

plicated by severe neurological disturbance. If bona

fide, though, the observation of a specific linkage be-

tween frontal functions and initiating joint attention

skill development would be important for several rea-

sons. Such an observation may be important to under-

standing the nature of the robust disturbance in initi-

ating joint attention skill development that is a cardinal


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Cortical Activity and Joint Attention 327

symptom of autism (Mundy, 1995). Furthermore, it

may also enrich the understanding of the observed

connections between individual differences in infant

IJA skill and childhood IQ (Ulvund & Smith, 1996),

language development (Mundy & Gomes, 1998), at-

tachment (Claussen et al., 1999), and childhood socialcompetence (Sheinkopf et al., 1999; Sigman & Rus-

kin, 1999). Therefore, this study was designed to pro-

vide an a priori test of the frontal mediation hypothesis

of initiating joint attention in a sample of infants who

were not effected by neurological disturbance.

The question arises, however, as to how best to

investigate this putative brainbehavior relation.

Caplan et al. (1993) observed neurological predic-

tors of IJA development using baseline rather than

event-related measures of brain activity. Therefore, to

maintain consistency with the methodology of Caplan

et al. (1993), baseline measure of brain activity were

used in this study. However, here baseline EEG ratherthan PET data were utilized.

In this regard, it has been argued that baseline EEG

data may be a valid marker of important aspects of

brain maturation and integration that precedes the

emergence of skills at different points in infancy (Fi-

scher & Rose, 1994; Hudspeth & Pribram, 1992;

Thatcher, 1994), especially visual attention skills (Par-

melee et al., 1994). Thatcher (1994) has also argued

for the use of measures of baseline EEG coherence to

examine aspects of brain and behavior maturation. Co-

herence is a measure of phase synchrony or shared

activity between spatially separated [EEG] generators(Thatcher, 1994, p. 233). A two-component model of

coherence has been proposed in which maturation of

the left hemisphere may be reflected in a pattern of

integration of differentiation or a reduction in co-

herence among proximal cortical sites, followed by an

increase in coherence among more distant cortical sites

in baseline EEG (pp. 251254). Maturation of right

hemisphere functions may be characterized by dif-

ferentiation of integration (pp. 251254) or a reduc-

tion of distal coherence followed by an increase in

proximal coherence among cortical areas. Further-

more, coherence measures are assumed to reflect the

integration or organization of brain processes that are

involved in the acquisition phase of a skill. Thus, co-

herence measures may be markers of differences in

brain integration processes that precede the acquisition

or consolidation of a skill (Bell & Fox, 1996; Fischer

& Rose, 1994).

In accordance with this literature, baseline EEG

measures of brain activity and cortical coherence were

used in this study to examine the frontal mediation

hypothesis of initiating joint attention skill develop-

ment in the 14- to 18-month period, a period of con-

solidation for this skill (Adamson, 1995).

M ETH O D S

Participants

Thirty-six healthy, full-term 14-month-olds (18 girls,

18 boys) participated in this study. All of these tod-

dlers were born within 2 weeks of their due dates.

They required no oxygen or major medical interven-

tion after birth and were negative for neurological dis-

orders or complications. The toddlers were recruited

from a major metropolitan area via mailing lists com-

posed of parents with middle to upper-middle SES and

a minimum education of graduation from high school.

Of the mothers of children in this study, 3 (9%) had

advanced degrees or training, 25 (78%) had completedsome or all of college, and 4 (13%) had completed

high school. Ethnicity of the mothers was primarily

Caucasian American (29, 91%), two were Black

American and one was Latin American. Only toddlers

born to two-right handed parents were recruited for

this study. Missing or compromised EEG data on 4

infants reduced the sample to 32 infants (14 girls, 18

boys) with complete longitudinal data on all measures.

Procedures

The electrophysiological and joint attention data col-lection required approximately 90 min, and the tod-

dlers were seen within 10 days of each of their 14-,

16-, and 18-month birthdays.

Electrophysiological Recording. Brain electrical ac-

tivity (EEG) was recorded during the 14-month visit

from 12 head sites: frontal, central, temporal, parietal,

and occipital regions for both the left and right hem-

ispheres (F3, F4, F7, F8, C3, C4, T3, T4, P3, P4, O1,

O2) referenced to the vertex (Cz). Facial activity, such

as mouth and jaw movements, crying, or changes in

facial affect, may be expected to affect data from F7,

F8, T3, and T4 to a greater extent than from other sites.

Visual inspection from these sites confirmed that in a

number of instances these data were confounded with

high-frequency motor artifact. Therefore, data from

these sites were eliminated from the analyses.

Baseline EEG was recorded for 3 min while the

toddler sat quietly in a highchair next to his or her

mother. During EEG recording, the toddler attended

to a novel display of a rotating bingo wheel with

brightly colored balls. This procedure has been found


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to be successful in garnering extended bouts of visual

attention while keeping the toddler quiet with reduced

eye movement and motor activity during the 3-min

period. The mother was instructed to refrain from talk-

ing or moving during the recording. The EEG was

recorded using a stretch lycra cap containing elec-trodes in the 10/20 placement system pattern (Jasper,

1958). After measuring the toddlers head to determine

the appropriate cap size and placing the cap on the

toddler, small amounts of abrasive gel and conductive

gel were inserted into the electrodes of interest. The

blunt end of a q-tip was used to gently abrade the scalp

after inserting each type of gel. Electrode impedances

were measured and accepted if below 5K ohms. Ad-

ditional abrading was sometimes necessary if initial

impedances measured greater than 5K ohms. Eye

movement (EOG) was recorded using Beckman min-

iature electrodes placed on the external canthus and

the supra orbit of the right eye.Prior to the recording of each subject, a 10-Hz .477

Vrms sine wave was input through each amplifier of

the polygraph. The amplifiers were set so that output

of the signal represented 50 uV peak to peak, with a

gain of 10,000. The EEG from each site of interest

was amplified using separate Grass amplifiers (Model

7P11) and bandpassed from 1 to 100 Hz, with a notch

filter at 60 Hz. The EEG signal was digitized on-line

at 512 samples per second for each channel to ensure

the data were not affected by aliasing. The raw data

were stored for later analysis. The EEG data were an-

alyzed using software by James Long Company. First,the EEG data were re-referenced via software to an

average reference configuration. The average refer-

enced EEG data were scored for eye movement and

motor artifact, and epochs containing artifacts were

eliminated from analysis. The data were analyzed with

a Discrete Fourier Transform (DFT) using a Hanning

window of 1 s with a 50% overlap. Prior to the com-

putation of the DFT, the mean voltage was subtracted

from each data point to eliminate any power results

due to DC offset. Power was computed for the 4- to

6-Hz and the 6- to 9-Hz frequency band. Past research

with infants has demonstrated that the majority of

spectral power can be found in this range, and espe-

cially these two bandwidths (see Calkins, Fox, & Mar-

shall, 1996). The power was expressed as mean square

microvolts and the data were transformed using the

natural log (ln) to normalize the distribution.

EEGANAL software was used to perform spectral

coherence calculations across EEG sites by averaging

the normalized complex cross-spectral density with

bands and epochs after the method of Saltzberg,

Burton, Burch, Fletcher, and Michaels (1986). Two

types of coherence variables were considered in this

study. A short-distance coherence variable between

frontal and central sites was computed within the 4-

to 6-Hz and 6- to 9-Hz bands for the 14-month EEG

data, as was a long-distance coherence variable be-

tween frontal and occipital sites. These two coherence

variables were computed separately for left and righthemisphere sites. Similar to previously used methods

(Thatcher, Krause, & Hrybyk, 1986), a summary co-

herence score for each hemisphere was calculated re-

flecting the ratio of short-distance coherence divided

by long-distance coherence (FrontalCentral Coher-

ence/FrontalOccipital Coherence).

Joint Attention Measures. Data on nonverbal joint at-

tention and requesting behaviors were collected with

the revised Early Social Communication Scales

(ESCS; Mundy, Hogan, & Doehring, 1996; Seibert et

al., 1982). The ESCS is a 20-min videotaped struc-

tured assessment designed to measure the develop-ment of a variety of nonverbal communication skills

in the 6- to 30-month period. For this assessment an

experimenter and an infant, sitting in his caregivers

lap or independently in a child chair, are seated facing

each other across a small table. A set of toys is visible

to the child but out of reach on the experimenters side

of the table. Posters are placed on the walls 90 degrees

to the childs left and right, and 180 degrees behind

the child. A video camera is positioned approximately

10 feet behind the experimenter. The camera is ori-

ented to capture a three-fourths face image of the child

with a profile view of the experimenter as well as theposition of the toys and posters.

The experimenter presents the child with a se-

quence of three activated wind-up toys (three trials

each), three hand-operated mechanical toys (three tri-

als each), opportunities to play a tickle, turn-taking

game (two trials), opportunities to play an object turn-

taking game, such as catch with a ball (two trials),

opportunities to take turns wearing a hat, comb, and

glasses (three trials), and an opportunity to look at pic-

tures in a book with the tester (one trial). The tester

also presents the child with multiple requests to give

toys to the tester. Finally, the tester presents the child

with two sets of three trials in which the tester attracts

the childs attention, and then turns to visually fixate

a wall poster while pointing at the poster and saying

the childs name three times with increasing emphasis.

Trials to the left, right, and behind the child are con-

ducted in each set.

Observations of the testerchild interaction in the

ESCS yielded frequency of behavior scores in six cat-

egories: Initiating Joint Attention (IJA); Responding

to Joint Attention (RJA), Initiating Behavioral Re-

questing (IBR), Responding to Behavioral Requesting


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Table 1. Brief Description of the Early Social

Communication Scale Variables

INITIATES JOINT ATTENTION

(a) Makes eye contact while manipulating toy; (b) alter-

nates eye contact between active mechanical toy and tes-

ter; (c) points to active mechanical toy or distal objects intesting room; (d) shows objects (raises objects toward the

testers face).

RESPONDS TO JOINT ATTENTION

The percentage of trials the child correctly turns head and

eyes in direction of testers point. On side trials, direction

of gaze must shift beyond the testers extended finger (ap-

proximately 45 degrees off midline). On behind trials, the

child must turn head more than 90 degrees off midline.

INITIATES BEHAVIOR REQUESTS

(a) Makes eye contact when object moved out of reach or

reaches to objects out of reach; (b) Makes eye contact

while reaching to objects out of reach; (c) Points to inac-

tive objects on the table or to the collection of visible but

out-of-reach toys; (d) Gives inactive toys to the tester

(e.g., moves toys toward testers hands).

RESPONDS TO BEHAVIOR REQUESTS

The frequency of trials on which the child correctly re-

sponds to testers gestural (i.e., palm-up hand extended)

and verbal request to give it to me.

(RBR), Initiating Social Interaction (ISI), and Re-

sponding to Social Interaction (RSI). Both the Joint

Attention and Behavioral Requesting involve the co-

ordination of attention to objects and events. Alter-

natively, the Social Interaction scales assess turn-tak-

ing and interaction maintenance but not necessarilycoordination of attention to objects and events. There-

fore, given the focus of this study, only data from the

former will be considered in analyses. Briefly, these

are operationalized in the following manner. IJA

scores refer to the frequency with which the child

spontaneously points, shows, and uses eye contact to

share the experience of an active mechanical toy with

the tester. In the age range in this study, the sponta-

neous use of eye contact to alternate attention between

an object and social partner is the most common be-

havior scored on this measure. RJA refers to the per-

centage of trials on which a child correctly turns her

visual regard in the direction of the testers visual re-gard and pointing gesture. IBR scores refer to the fre-

quency with which the child uses eye contact, reach-

ing, giving, and pointing to elicit aid in obtaining

objects or reactivating objects. RBR refers to the fre-

quency of trials on which a child correctly responds

to the experimenters hand out, palm up gesture and

verbalization of give it to me while the child is hold-

ing or examining a toy. A more complete description

of the behaviors observed within each category is pre-

sented in Table 1. The raters were blind to the other

data collection procedures as well as the hypotheses

of this study.Reliability for the ESCS measures used in this

study are well established (e.g., Mundy & Gomes,

1998; Mundy, Kasari, Sigman, & Ruskin, 1995;

Mundy, Sigman, & Kasari, 1994). Estimates of inter-

rater reliability based on 12 independent paired obser-

vations of data for this study yielded rs .87, .95,

.82, & .79, p .001, for the total frequency scores for

IJA, RJA, IBR, and RBR, respectively. IJA displayed

a significant degree of stability (test-retest reliability)

in this study with correlations among the 14-, 16-, and

18-month IJA measures ranging from r(31) .57 to

.83, p .001. RJA also displayed evidence of stability

between the 14-month and 18-month measure,

r(31) .51, p .002. The relations between the 14-

and 16-month RJA measure and 16- and 18-month

measure approached significance, r(31) .25 and .28,

p .08 and .06, respectively. The IBR and RBR mea-

sures displayed no evidence of significant stability in

this study, r(31) range .13 to .24. Thus, the IJA

and RJA measures displayed more optimal psycho-

metric characteristics than did IBR and RBR in this

study.

Covariance among the different types of infant at-

tention coordination measures was modest. Of the pos-

sible 54 interscale correlations among the 14-, 16-, and18-month ESCS measures, just 12 were significant.

Across the types of joint attention measures, only 14-

month RJA was correlated with 14-month IJA, r

.36, p .05 (one tailed), and 16-month IJA, r .33,

p .05. However, at 18 months the IJA and RJA

correlation was r .05. IJA and IBR were not signif-

icantly correlated, but IJA was correlated with RBR at

18 months, r .34, p .05. Thus, the different ESCS

measures appeared to assess unique or distinct aspects

of the development of social attention coordination

skill in this study.

RESU LTS

D evelopment of Joint Attention Skil ls

The means of the four types of infant attention coor-

dination skills at the three ages of assessment are pre-

sented in Table 2. Preliminary analyses were con-

ducted to evaluate the effect of gender and age-related

changes on these measures. Because of their difference

in scaling (percentage data), RJA scores were first con-


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Table 2. Means, with Standard Deviations in Parentheses, for the ESCS Variables at 14, 16, and 18 Months of Age

ESCS Variables 14 Months 16 Months 18 Months

Initiates joint attention (IJA)

Girls 19.5 (10.4) 16.1 (9.5) 19.8 (8.8)

Boys 15.9 (8.6) 14.7 (10.2) 16.3 (8.2)

Total 16.5 (8.0) 15.4 (10.1) 17.5 (8.6)Responds to joint attention (RJA)

Girls 87% (12%) 78% (25%) 81% (27%)

Boys 76% (25%) 81% (20%) 83% (23%)

Total 82% (20%) 81% (21%) 83% (24%)

Initiates behavior regulation (IBR)

Girls 33.6 (11.3) 35.0 (10.2) 41.5 (7.3)

Boys 30.5 (13.2) 33.6 (10.6) 36.1 (14.4)

Total 32.4 (12.0) 34.0 (10.7) 38.2 (12.4)

Responds to behavior regulation (RBR)

Girls 2.9 (1.2) 3.2 (1.3) 3.5 (1.4)

Boys 3.5 (1.5) 3.2 (1.7) 4.1 (2.3)

Total 3.4 (1.4) 3.2 (1.5) 3.9 (2.1)

sidered in a separate ANOVA using arc sine transfor-

mations. This analysis revealed no effects of gender

or age for RJA in this study. Next, a 2 3 3 (Gen-

der Age ESCS Scores) ANOVA was computed

for the IJA, IBR, and RBR variables. No effects as-

sociated with gender were significant. The main effect

for age was significant, F(2, 62) 3.68, p .05, but

the Age ESCS Scores interaction was not signifi-

cant.

The main effect for age indicated that the children

displayed a general increase in facility with coordi-nated attention bids with age (see Table 2). Pairwise

bonferronni comparisons for the main effect for age

revealed that 18-month-olds displayed significantly

higher ESCS scores than did 14-or 16-month-olds,

p .05. The 14- and 16-month-olds did not differ,

p .74. Within individual scales of the ESCS, this

effect reached significance for IBR on the 18-versus

14-month comparison, p .05. Therefore, to reduce

the data and constrain the number of analyses, only

data from the 14- and 18-month measures were con-

sidered in examinations of the relations between EEG

and ESCS variables in this study.

EEG Prediction of Joint Attention and O therN onverb al Skil ls

The covariance among the EEG data from the eight

leads (two frontal, two central, two parietal, and two

occipital) was considerable. For example, the average

correlation among the eight leads for the 4- to 6-Hz

band data was: r(30) .65, range .30 to .87. Av-

erage covariance for 6- to 9-Hz data was even

stronger: r .72, range .42 to .92. Consequently,

hierarchical multiple regression analyses (Cohen &

Cohen, 1983) were conducted to determine if 14-

month baseline EEG indices of left frontal activity

would display significant and unique predictive rela-

tions with the development of individual differences

in 18-month IJA. Analyses were also computed to

compare the associations of 14-month EEG data with

the three other ESCS measures at 18 monthsRJA,

IBR, and RBR. In each analysis, data from the left and

right hemisphere ratio EEG coherence scores (frontal

central coherence/frontal/occipital coherence) wereentered on Step 1. On Steps 2, 3, 4, and 5, the log

power data from the eight EEG leads (left and right

frontal, central, parietal, and occipital pairs) were en-

tered, respectively. This set order of data entry re-

flected the a priori emphasis in examining the relations

of ratio coherence and frontal EEG data with individ-

ual differences in joint attention. In addition, the 14-

month IJA and RJA scores were significantly corre-

lated with their respective 18-month scores (see

Methods) and were entered on the first step of analyses

of the 18-month IJA and RJA scores, respectively.

These regression analyses yielded a set of significant

equations for several of the different types of infant

attention coordination skills using EEG data from the

4- to 6-Hz band. However, none of the regression

equations using the 6- to 9-Hz band EEG data were

significant. Therefore, only the results of the former

have been reported in this article.

The results of the analyses for IJA and RJA are

presented in Tables 3 and 4. To be considered signif-

icant, a step in these analyses needed to be associated

both with a significant increase in R2 as well as a sig-

nificant overall effect for the regression equation. Data


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Table 3. Significant 14-Month EEG Predictors of the 18-Month Initiating Joint Attention

Steps and Variables R R2a p

Step 1 (df 3/28) .67 .39 .001*

Left hemisphere coherence .37 .02*

Right hemisphere coherence .03

14-month IJA .49 .002*Step 2 (df 5/26) .69 .38 .003*



14-month IJA .53 .002*

Left frontal EEG .28

Right frontal EEG .30

Step 3 (df 7/24)b .77 .48 .001* (.05*)



14-month IJA .61 .001*

Left frontal EEG .80 .025*


Left central EEG .02

Right central EEG .70 .05*

Follow-up (df 4/27) .77 .52 .007*


14-month IJA .61 .001*

Left frontal EEG .68 .012*

Left central EEG .73 .007*

aR2 estimate adjusted for sample size. bThe p value for a significant change in R2 is presented in parentheses after the p value for the entire

equation.

are presented up through those steps that met these

criteria. Follow-up analyses are also presented for

equations obtained after the removal of blocks of var-iables with nonsignificant, p .10, standardized re-

gression coefficients.

Step 1 of the analyses of 18-month IJA was signif-

icant (see Table 3). The 14-month IJA score was a

significant positive predictor of 18-month IJA. In ad-

dition, the left hemisphere ratio coherence score dis-

played a significant negative . On Step 2 of these

analyses, the addition of the left and right frontal EEG

power data did not yield a significant increase in R2.

However, on Step 3 a significant increase in R2 was

observed in the analyses of 18-month IJA with the

addition of 14-month central EEG power data (see Ta-

ble 3). A positive (hypoactivation) right central EEG

component at 14 months was a significant predictor of

18-month IJA scores. Moreover, a suppressor effect

was evident so that a unique and significant relation

of left frontal activation at 14 months with 18-month

IJA became apparent on this step after considering var-

iance in coherence and central EEG data. Thus, Step

3 of these analyses, as well as the follow-up analyses

(see Table 3), revealed that a combination of 14-month

baseline EEG measures including the left hemisphere

ratio coherence measure, left frontal activation, and

right central hypoactivation displayed unique paths of

association with subsequent individual differences in

IJA.To better understand the nature of the correlation

between 18-month IJA and 14-month EEG coherence,

we examined the individual components of this ratio

measure. Coherence between left frontal and occipital

sites at 14 months was not correlated with 18-month

IJA, r .11, but coherence between left frontal and

central sites was negatively correlated with 18-month

IJA, r .48, p .005. This negative correlation

suggests that lower coherence between left frontal and

central cortical sites at 14 months, possibly indicative

of individual differences in differentiation of left cor-

tical activity (Thatcher, 1994), was related to IJA de-

velopment at 18 months in this sample.

The data in Table 4 revealed that the pattern of

significant EEG predictors of RJA appeared to be quite

different from the pattern of predictors of IJA. Aside

from significant effects associated with 14-month RJA

observed on Step 1, these analyses revealed a signifi-

cant effect at Step 4 with the addition of the log power

EEG data from the parietal electrodes. As can be seen

most clearly in the follow-up analysis, after removing

other EEG variables in the EEG data set, both indices

of left parietal activation and right parietal hypoacti-


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Table 4. Significant 14-Month EEG Predictors of the 18-Month Responding to Joint Attention


Step 1 (df 3/28) .56 .24 .012*

Left hemisphere coherence .19


14-month RJA .56 .002*Step 2 (df 5/26) .58 .21 .05*



14-month RJA .55 .003*



Step 3 (df 7/24)b .62 .21 .075



14-month RJA .62 .001*




Right central EEG .03

Step 4 (df 9/22) .72 .33 .05* (.05*)



14-month RJA .41 .05*




Right central EEG .10

Left parietal 1.10 .05*

Right parietal .51

Follow-up (df 3/28) .63 .33 .003*

14-month RJA .40 .025*

Left parietal .89 .025*Right parietal .85 .03*


equation.

vation displayed significant paths of association with

RJA at 18 months (see Table 4).

The analyses of IBR and RBR also revealed distinct

patterns of data. None of the steps in the analyses of

IBR approached significance. In these analyses, only

activation of the left parietal EEG power data at 14

months approached significance in predicting 18-

month scores, .87, p .10. In contrast, a sig-

nificant regression equation, R .57, F(4, 28) 3.32,

p .025, and a significant increase in adjusted R2,

R2 .16, F 4.01, p .03, was observed for the

18-month RBR variable, on Step 2, with the entry of

the frontal EEG log power data. However, unlike with

the IJA data, a right frontal activation component,

.82, p .009, and a left frontal hypoactivation,

.72, p .02, were associated with IBR. Follow-

up analyses revealed that these two frontal variables

alone were associated with RBR, R .49, adjusted

R2 .19, p .02; right frontal activation, .89,

p .004, and left frontal hypoactivation, .71,

p .02.

Concurrent Correlat ions Betw een the EEG

and ESCS VariablesThe patterns of concurrent multiple correlations be-

tween the EEG and ESCS variables were also exam-

ined at 14 and 18 months using hierarchical regression

analyses with the same order of data entry as previ-

ously described for the predictive regression equa-

tions. The analyses of concurrent correlates of IJA at

14 months yielded a marginally significant regression

equation (see Table 5). Nevertheless, a combination of

the left hemisphere frontal coherence ratio, as well as


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Table 5. Concurrent EEG Correlates of IJA at 14 Months Initiating Joint Attention


Step 1 (df 2/29) .25 .01



Step 2 (df 4/27) .38 .03Left hemisphere coherence .29




Step 3 (df 6/25)b .53 .13 .078* (.078*)







Follow-up (df 3/28) .49 .16 .007*





equation.

left central EEG hypoactivation and right central EEG

activation, displayed unique paths of association with

14-month IJA (see Table 5).

In these data, though, neither of the individual com-

ponents of the coherence measure were correlatedwith

14-month IJA: left frontal and left central component,r .14, left frontal and left occipital component,

r .13.

The results of the other 14-month concurrent anal-

yses may be summarized as follows. For RJA, a sig-

nificant effect associated with the increase in adjusted

R2, R .58, R2 .20, adjusted R .10, p .05,

was again observed for Step 4 of the analyses with the

addition of the parietal data. Left parietal activation,

1.2, p .02, and right parietal hypo-activation,

.88, p .065, were associated with 14-month

RJA. However, follow-up analyses did not reveal ef-

fects for parietal processes when considered in isola-

tion from the other EEG variables. Analyses of IBR

at 14 months yielded a significant effect for Step 1,

R .43, p .055, with follow-up analyses indicating

that relatively greater short distance left frontal to cen-

tral coherence was associated with IBR at 14 months,

r .39, p .03. Alternatively, a marginally signifi-

cant effect on Step 1 for the analyses of RBR was also

observed, R .41, p .07, due to an association

between greater right hemisphere long distance frontal

to occipital coherence, r .34, p .056.

Only two significant effects were observed for the

concurrent 18-month analyses, and both of these sug-

gested a shift from 14 to 18 months in the brain activ-

ity correlates of IJA and RJA. For the analyses of both

IJA and RJA, marginal to significant increases in ad-

justed R2

were observed for Step 5 with the additionof the 18-month occipital data, R .63, R2 .20,

adjusted R2 .09, p .06 for IJA, and R .63,

R2 .24, adjusted R2 .10, p .05 for RJA. Fol-

low-up analyses revealed that only left occipital hy-

poactivation was associated with 18-month IJA, r

.44, p .015. Alternatively, a pattern of right occipital

hypoactivation, .60, p .01, and right central

activation, .66, p .006, was associated with

RJA at 18 months, R .51, adjusted R2 .21, p

.015.

D ISCU SSIO N

An important feature of the results of this study was

that individual differences in baseline measures of left

frontal brain activity were uniquely and specifically

related to the subsequent development of infant IJA in

this study of normally developing infants. This obser-

vation was consistent with the findings of Caplan et

al. (1993) and provides further support for the hypoth-

esized involvement of frontal process in IJA devel-


10/14


opment (Mundy, 1995). Unexpectedly, though, left

central activity was also associated with IJA devel-

opment. Furthermore, different types of infant social

attention coordination skills were related to different

patterns of cortical activity. Because aspects of this

pattern of results were not anticipated, it may be usefulto go beyond theory reviewed in the Introduction on

the frontal processes that may be associated with IJA

and consider theory on the early development of at-

tention regulation more broadly conceived.

The emergence of attention regulation in infancy

has been described in terms of an anteriorposterior

model of development (Posner & Petersen, 1990;

Rothbart, Posner, & Rosicky; 1994; Stuss et al., 1995).

The posterior component of this system is thought to

develop before the anterior component (Rothbart et al.,

1994). Between 3 and 6 months of age, infants become

capable of shifting attention by inhibiting or disengag-

ing attention from an immediate focus ( Johnson, Pos-ner, & Rothbart, 1991). The development of this ca-

pacity is thought to reflect a posterior orienting

attention system regulated, in part, by components of

the parietal cortex as well as associated midbrain and

thalamic areas (Posner & Petersen, 1990). The regu-

lation of behavior via this system may be best thought

of in terms of implicit learning, where this refers to

the action of relatively less voluntary neurobehavioral

processes (Rothbart et al., 1994).

From this theoretical perspective, the data in this

study suggest that responding to joint attention skill

development may reflect the operations of this poste-riorparietal attention system to some significant ex-

tent. The parietal lobe function of enabling shifts of

attention by disengaging attention from its current fo-

cus (Rothbart et al., 1994, p. 637) may be employed

when an infant redirects his or her attention in re-

sponse to the head and gaze shift of an experimenter

on an RJA trial. Furthermore, RJA functions appear

to become part of many infants behavioral repertoire

by 6 months of age (Butterworth, 1995; Morales et al.,

1998; Scaife & Bruner, 1975), and data also suggest

that the parietal orienting system becomes functional

just prior to this age, in the 4- to 6-month period (John-

son et al., 1991).

Other circumstantial evidence points to a link be-

tween RJA and parietal lobe functioning. The parietal

lobes, in conjunction with occipital functions, may

serve to encode spatial location of stimuli relative to

body position and eye orientation (Andersen &

Mountcastle, 1983; Goldman-Rakic, 1987; Motter,

Steinmetz, Duffy, & Mountcastle, 1987). This is con-

sistent with the hypothesized importance of spatial an-

alytic skill in the acquisition and development of RJA

skill (Butterworth, 1995; Butterworth & Cochran,

1980; Butterworth & Jarrett, 1991). In addition, recall

that RJA skill has been linked to early receptive lan-

guage development (Baldwin, 1991, 1993; Morales et

al., 1998; Mundy & Gomes, 1998; Mundy et al.,

1995). Similarly, cortical evoked response data sug-

gest that the left parietal as well as the left temporalprocesses are involved in the discrimination of com-

prehended versus noncomprehended words in the sec-

ond year (Mills, Coffey-Corina, & Neville, 1994).

Thus, there are numerous strands of theory and re-

search that are consistent with the linkage observed

here between parietal EEG and RJA.

Alternatively, the frontal correlates of IJA, and to

a lesser extent IBR and RBR, may reflect the influence

and maturation of an anterior attention regulation net-

work. This network becomes functional after the pos-

terior parietal system, and is manifest in increasing

volitional control of attention deployment (Rothbart et

al., 1994). The anterior attention system plays a centralrole in the capacity to share attention across dual tasks

or foci of attention (Stuss et al., 1995), as well as in

the regulation of voluntary, goal-directed orienting as

affected by both cognitive and motivational constraint

and activation parameters (Neafsey, Terreberry, Hur-

ley, Ruit, & Frysztak, 1993; Rothbart et al., 1994).

Thus, consistent with theory espoused in the Introduc-

tion, the connection of IJA to a frontal anterior atten-

tion system may reflect cognitive, executive, and/or

motivational processes.

There is also some evidence that the dorsolateral

and midfrontal cortex, including the anterior cingulategyrus, may contribute to this anterior executive atten-

tion network (Cummings, 1995; Rothbart et al., 1994;

Stuss et al., 1995). This area, especially the cingulate

gyrus, has interconnections to the limbic system as

well as the central motor areas (Rothbart et al., 1994),

including those involved in head and eye movements

involved in attention and orienting (Neafsey et al.,

1993). The latter connections may provide a starting

point in considering why an integrated pattern of 14-

month left frontal and central cortical components was

associated with 18-month IJA, and to a lesser degree

14-month IJA. The results suggested that, at 14

months, a pattern of right central deactivation and left

frontal activation as well as a decrease in the syn-

chrony of activation of left frontal and central cortical

sites was related to IJA development. This pattern, es-

pecially the latter component, suggests that IJA in the

second year may be related to developmental brain-

maturation processes involving the differentiation of

left cortical functions (Thatcher, 1994). In particular,

IJA development at 18 months may have been pre-

saged by the differentiation and emphasis of frontal

relative to central contributions to attention regulation.


11/14


Alternatively, concurrent correlations at 14 months

suggested that, although IJA was beginning to become

associated with a frontal central differentiation, central

components were primary to IJA at this point in de-

velopment.

Of course, such a rich interpretation of a single dataset may be premature. Caution should be exercised in

interpreting this relatively unprecedented data set.

Nevertheless, this analysis serves to facilitate a poten-

tially edifying integration between more general as-

pects of research on human attention processes (e.g.,

Posner & Petersen, 1990; Rothbart et al., 1994) and

contemporary research on infant social attention co-

ordination (e.g., Baldwin, 1991; Baron-Cohen, 1995;

Corkum & Moore, 1997; Mundy & Gomes, 1998)

that, heretofore, has gone unrecognized. For example,

the notion that IJA and RJA may, respectively, reflect

a later developing anterior attention regulation net-

work versus an earlier arising parietal attention regu-lation network may assist in understanding why these

measures have been observed to display different pat-

terns of behavioral correlates in typical and atypical

samples (Claussen et al., 1999; Mundy & Gomes,

1998; Sigman & Ruskin, 1999; Ulvund & Smith,

1996).

This dual neural-network hypothesis of joint atten-

tion development may also have implications for un-

derstanding the disturbance in this skill domain that is

characteristic of autism (Mundy, 1995). Children with

autism display deficits in both IJA and RJA, with the

former being more robust with development than thelatter (Mundy et al., 1994; Sigman & Ruskin, 1999).

The data in this study lead to the suggestion that both

left frontal and parietal processes may be involved in

this area of disturbance for children with autism. This

notion is consistent with other research on autism. For

example, abnormal seretonin synthesis in the left fron-

tal hemisphere may be characteristic of a substantial

number of children with autism (Chugani et al., 1997).

Recent functional MRI (fMRI) data have also sug-

gested that socialcognitive task performance may be

associated with a left medial frontal system of activity,

and that individual disorders related to autism may

display a disturbance in the functions of this medial

frontal system (Fletcher et al., 1995; Happe et al.,

1996; for discussion see Mundy & Neal, in press).

Indeed, the combination of results of these fMRI stud-

ies and this study provides some support for the hy-

pothesis that deficits observed in children with autism

in joint attention skill as well as in later socialcog-

nitive, or so-called Theory of Mind facility, may be

linked in some fundamental fashion (Baron-Cohen,

1995; Mundy & Neal, in press). Finally, studies have

also reported observations of parietal lobe abnormal-

ities in individuals with autism (Piven, Arndt, Bailey,

& Andreasen, 1996), as well as individuals with the

often-related disorder of fragile X syndrome (Schapiro

et al., 1995).

This dual neural-network hypothesis of joint atten-

tion development may also prove instructive with re-gard to a prevailing notion that all forms of infant so-

cial attention coordination primarily reflect a common

epistemological process, such as understanding inten-

tions in self and other (Carpenter et al., 1998; Toma-

sello, 1995; Wellman, 1993), or a single modular sys-

tem of socialcognitive development (Baron-Cohen,

1995). In contrast, the relative lack of significant cor-

relations among infant social attention coordination

measures observed here, and the differential pattern of

their correlations with EEG data, was consistent with

theory that suggests that different types of infant at-

tention coordination acts may reflect distinct constel-

lations and integrations of neurological, psychologi-cal, and experiential processes as well as common

processes (Mundy, 1995; Mundy & Gomes, 1997).

Thus, in the study of the development of infant atten-

tion coordination skills, it may be useful to consider

the possibility that different skills reflect divergent as

well as convergent processes in their development.

The data also provided some support for Fischer

and Roses (1994) notion that, at different points in

the development of a skill, different integrations of

frontal, central, parietal, and occipital EEG associa-

tions may be manifest. Indeed, based on data from

Hudspeth and Pribram (1992), Fischer and Rose sug-gested that more anterior brain functions may be in-

volved in the early phases of skill development,

whereas more posterior brain functions may underpin

later phases of consolidation. The transition from con-

current and predictive associations with a frontal/cen-

tral system for IJA and a parietal system for RJA at

14 months to concurrent associations with an occipital

activity for both variables by 18 months in this study

was consistent with this view of a complex, shifting

pattern of cortical correlates of behavioral develop-

ment.

Finally, several methodological issues bear men-

tion. First, all the parents of infants in this study were

right-handed. Perhaps, then, the left hemisphere as-

sociations in this study reflected a bias in infants use

of their right hands to point or gesture. This issue war-

rants further consideration. However, similar behav-

iors, such as pointing, were observed in both the IJA

and IBR measures in this study (see Table 1), but these

measures had different patterns of cortical correlates.

Hence, it seems unlikely that a right-handed bias could

fully account for left hemisphere brainbehavior re-

lations observed in this study.


12/14


Second, it is important to note that the 14- to 18-

month period of this study may be especially sensitive

to consolidation of individual differences in IJA skills.

If frontal functions are generally prominent during

sensitive periods of skill development (Fischer &

Rose, 1994), then the specific association of IJA withleft frontal EEG activation and frontal EEG coherence

may have been observed only because of the devel-

opmental window chosen for study. For example, the

peak consolidation period for RJA may be somewhere

in the 6- to 15-month period (Butterworth & Jarrett,

1991; Morales et al., 1998; Scaife & Bruner, 1975).

Perhaps examination of the EEG correlates of RJA in

that period would yield a different and comparably

complex pattern of cortical correlates.

Finally, the IJA measure displayed the strongest

and most consistent evidence of longitudinal stability

or test-retest reliability in this study. This difference

in the psychometric properties of the variables understudy could have effected the pattern of the results.

However, the stability of the IJA measure may also

attest to its relative importance. IJA may be a valid

index of a variety of cognitive, temperamental, and

environmental factors that culminate in individual dif-

ferences in infants tendencies to self-organize and

contribute to opportunities for social observational

learning (Claussen et al., 1999; Mundy & Neal, in

press; Ulvund & Smith, 1996) and these opportunities

may be critical to fostering young childrens cognitive

assimilation of cultural information and adaptive so-

cial development (e.g., Adamson, 1995; Bruner, 1975;Mundy & Willoughby, 1998; Tomasello et al., 1993;

Trevarthen, 1979; Ulvund & Smith, 1996). As such,

IJA, and the capacity to initiate sharing of information

with others, may be a major milestone of early devel-

opment that serves as a behavioral fulcrum around

which multiple domains are integrated and organized

early in development (Mundy, 1995). Hence, the

unique frontal component and relative complexity of

the pattern of cortical correlates of IJA observed in

this study may be consistent with the hypothesized

central importance of this domain for early develop-

ment.

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