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Cogniie, Creier, Comportament / Cognition, Brain, Behavior

Vol. IX(3), 317-328, 2005Romanian Association of Cognitive Sciences

INDIVIDUAL DIFFERENCES IN THE DEVELOPMENT

OF SOCIAL COMMUNICATION:

JOINT ATTENTION AND TEMPERAMENT

Kate E. NICHOLS*, Jennifer N. MARTIN, Nathan A. FOX

University of Maryland, USA

ABSTRACT

Social communication is an important skill that emerges during infancy. Weexamined individual differences in this skill as a function of temperament andneural activity in nine-month-old infants. We found that maternal ratings oftemperament were associated with joint attention, an important index of early

social communication. More specifically, maternal ratings of pleasure wereassociated with joint attention bids that were accompanied by positive affect,while maternal ratings of fearfulness were associated with joint attention bidsthat were accompanied by negative affect. We also found that initiating jointattention was associated with decreased left frontal electroencephalogram(EEG) power, and initiating behavioral requests were associated with

decreased left frontal EEG power.

KEY-WORDS:joint attention, affect, temperament, EEG, social

communication

Infants communicate with social partners for many reasons. Some forms of

social communication may emerge out of an intrinsic motivation system as

described in models of intersubjectivity development (Trevarthen & Hubley,

1978). Infants who are high in approach may have a lower threshold for

experiencing reward and may more easily elicit and display positive affect during

social communication. In contrast, infants who are temperamentally fearful, high in

avoidance or withdrawal motivation, may be less inclined to interact socially with

unfamiliar persons, and more likely to communicate with familiar others as a way

of maintaining contact in unfamiliar situations. Little research has investigated the

associations between infant temperament or motivational bias and the developmentof social communication. The current study sought to address this issue by

assessing relations between temperament and social communication in infants.

Infants are able to communicate from an early age through eye contact and

gestures. By nine-months, the neural circuitry of the basal ganglia and the

*Corresponding address:

Kate E. Nichols,University of Maryland, 3304 Benjamin Bldg, College Park, MD 20742Email: [email protected]


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Iunie 2005 Cogniie, Creier, Comportament318

substantia nigra are established well enough to allow for the inhibition of reflexiveorienting responses, the initiation of purposeful goal-driven saccades, and the

maintenance of focused attention on objects of interest to the child (Johnson,

1990). Shifting gaze, particularly in a meaningful or voluntary fashion, is thought

to substantially influence an infants ability to explore their environment and to

participate in early forms of social communication (Butcher, Kalverboer, & Geuze,

2000).

According to Bates (1976) early social communication is comprised of

protodeclarative and protoimperative acts. Protodeclarative acts describe instances

where an infant uses eye contact or gestures to spontaneously begin a period of

coordinated attention with a social partner. On the other hand, protoimperative acts

describe instances where an infant uses eye contact or gestures to elicit aid in

obtaining an object or modifying an event. Recently, Mundy and colleagues(Seibert, Hogan, & Mundy, 1982; Mundy et al., 2003) have developed a procedure

for eliciting these different acts of communication with infants in the second half of

the first year of life and into the second year of life. The procedure, called the Early

Social Communication Scale (ESCS; Mundy, et al., 2003) provides a context in

which both protodeclarative acts (referred to as Initiating Joint Attention; IJA) and

protoimperative acts (referred to as Initiating Behavioral Requests; IBR) may be

observed. Individual differences in IJA have been associated with varying levels of

social and language development, and in particular, deficits in IJA have been

related to autism (Carpenter, Nagell, & Tomasello, 1998; Mundy, Sigman,

Ungerer, & Sherman, 1986).

Temperament can be thought of as the disposition of the infant to react or

respond with a particular emotion to novel or unfamiliar stimuli. Vaughn andcolleagues (2003) have found that infant temperament, as assessed by measures of

positive and negative reactivity on the Rothbart Infant Behavior Questionnaire

(IBQ, Rothbart, 1981), is related to IJA. The association between the bias to

express positive affect and joint attention is consistent with the idea that IJA

involves sharing experiences with others in a positively valenced interaction

(Mundy, 1995; Mundy & Sigman, in press), and that IJA is intrinsically motivated

by a neural system for engaging in shared awareness (Trevarthen & Hubley, 1978).

It has also been suggested that the basic motivational system for engaging in

episodes of shared awareness with others develops in two stages (Trevarthen &

Hubley, 1978). The first stage, primary intersubjectivity, involves systems that

promote social attention, including the ability to respond to eye contact and facial

affect. Through interactions during this stage infants are provided with experiences

that allow them to represent self as distinct from other. When infants experience

the same affect as their social partner, it motivates them to continue the interaction,

especially when the experience is positive. With increased interactions and

cognitive maturation the infant becomes capable of the second stage, namely

secondary intersubjectivity, or awareness that both self and others are sharing an

experience (Trevarthen & Hubley, 1978). These experiences lead the infant to

initiate more periods of shared attention. In general, research has shown that IJA,


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Iunie 2005 Cogniie, Creier, Comportament 319

as compared to IBR, is more often accompanied by positive affect (Adamson &Bakeman, 1985; Mundy, Kasari, & Sigman, 1992). This supports the hypothesis

that when infants share mutual eye contact and attention on a common object, they

find it rewarding. Furthermore, autistic children rarely experience positive affect

while sharing attention with a social partner (Kasari, Sigman, Mundy, & Yirmiya,

1990), which may mean that children with autism are less likely to engage in joint

attention for an inherent social reward (Mundy, 1995). Thus failure to assign

reward value to social stimuli has been proposed as a possible explanation for

autism (Dawson, Osterling, Rinaldi, Carver, & McPartland, 2001; Dawson et al.,

2001).

In the current study we investigated individual differences in the frequency

of IJA accompanied by positive or negative affect in relation to infant temperament

in a typically developing sample. We hypothesized that infants with a positivetemperament will exhibit IJA accompanied by positive affect while infants with a

fearful temperament will exhibit IJA accompanied by negative affect will be most

prevalent in infants with a fearful temperament. In support of this notion, Vaughn

and colleagues (2003) suggest that IJA may be associated with a vigilant or wary

style of attention. This interpretation is in line with the hypothesis that the fear

system is related to increased vigilance and orienting to environmental cues that are

threatening or novel (LeDoux, 2000).

Another area that has linked negative reactivity and social contact seeking

is the attachment literature. Bowlby (1969) first conceived attachment as a stress-

related biobehavioral system that was the key system involved in maternal

bonding. Attachment theory suggests that the system is activated in response to

threat and stress. Negative reactivity may result from increased threat responses,which in turn may result in increased signals for social connection and comfort. De

Laguna (1927) has suggested that both language and nonverbal forms of

communication, such as eye contact in humans (Scheflen, 1963) and grooming in

non-human primates, (Dunbar, 1991) are, at their most basic level, strategies for

developing and maintaining social relationships. Locke (2001) suggests that many

infant vocalizations and gestures, including joint attention, are analogous to the

Testing. Testing. vocalization used when an adult tests a microphone system.

The voice and shared attention offers a means of maintaining continuous contact

with key figures in the infants social world. However, little research has

investigated the affective quality of communication that is motivated by negative

reactivity and vigilance. At the physiological level, positive reactivity and negative

reactivity have been linked to differences in frontal brain systems. Within the first

year of life, social motivation, social orienting, positive affect, and approach

behaviors have been associated with left frontal EEG activity, and greater relative

right frontal EEG activation has been associated with crying in response to a brief

period of maternal separation and behavioral inhibition (Fox, 1991; Fox &

Davidson, 1987; Davidson & Rickman, 1999; Fox, Henderson, Rubin, Calkins, &

Schmidt, 2001).


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These EEG lateralization differences have also been studied in associationwith IJA. Mundy, Card, and Fox (2000) studied typically developing infants from

14 to 18 months and found that EEG power in the alpha band in left but not right

frontal sites was associated with IJA. The authors suggested that the left frontal

EEG activation associated with IJA may reflect individual differences in approach

tendencies. However, other research (Henderson, Yoder, Yale, & McDuffie, 2002)

suggests that both right and left frontal EEG power is associated with IJA. These

data are consistent with data from Vaughan et al. (2003) that suggests that IJA may

also be associated with negative affect and motivation tendencies that have been

related to relative right frontal EEG activation (Mundy & Sigman, in press).

In the current study, we investigated infant temperament, joint attention,

and left and right frontal EEG power. Affect was coded during the ESCS procedure

in order to examine the relations between affective expression and socialcommunication in infancy. Parents also completed a standard infant temperament

questionnaire in order to assess the role of maternal report of infant temperament

on early social communication skills. We had three hypotheses: first, it was

expected that positive affect would accompany joint attention more than behavioral

requests. Second, we anticipated that mothers ratings of infant temperamental

fearfulness would be associated with initiating joint attention bids accompanied by

negative affect. Third, we expected that frontal EEG power would vary in

accordance with the different affective measures of IJA and IBR.

Method

Participants. Infants were classified based on their 4-month observed

behavioral reactivity scores and assigned to one of two different temperament

groups: fearful or exuberant . The fearful group was high in motor and negative

reactivity (n = 88), and the exuberant group was high in motor and positive

reactivity (n = 66). An unselected sample was also recruited and served as a control

group (n = 96). At 9 months, all three groups of infants returned to the laboratory

and IJA and IBR were assessed with the Early Social Communication Scale

(ESCS; Mundy, Hogan, & Doehring, 1996). Maternal report of temperament was

collected using the Infant Behavior Questionnaire (IBQ; Rothbart, 1981).

Measures

Early Social Communication Scale. Data on nonverbal joint attention and

requesting behaviors were collected with the revised Early Social CommunicationScales (ESCS; Mundy et al. 2003). The ESCS is a structured assessment designed

to measure the development of nonverbal communication skills in infants and

toddlers during the 6- to 30-month age period. The experimenter and child, in his

or her mothers lap, are seated facing each other across a table for a series of

activities involving mechanical and windup toys. Seven toys were presented across

21 trials.

Observations of the experimenter-toddler interactions yielded scores for

joint attention and behavioral requests. Initiating Joint Attention (IJA) describes the


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raw number of times the toddler alternated eye contact between the activemechanical toys and the tester, pointed to the toys, or showed the toys in order to

share the experience with the tester. Initiating Behavior Requests (IBR) describes

the number of times the toddler reached for a mechanical toy beyond his/her grasp,

spontaneously gave a toy to the experimenter, or made eye contact with the

experimenter after a mechanical toy had stopped in order to elicit aid from the

tester. Two coders became reliable with 19 cases on the ESCS training tape, IJA

alphas = .81 and .91, IBR alphas = .87 and .93. The coders rated an additional 25

cases from the sample. Alphas for total IJA, neutral IJA, total positive IJA, low

intensity positive IJA, high intensity positive IJA, and negative IJA were .98, .85,

.90, .85, .92, and .90 respectively. Alphas for total IBR, neutral IBR, total positive

IBR, low intensity positive IBR, high intensity positive IBR, and negative IBR

were .95, .94, .81, .84, .95, and .79 respectively.EEG data collection. At 9 months, each infant was seated in his or her

mothers lap to minimize fussiness and movement. They watched a metal bingo

wheel placed on a table in front of them, where an experimenter placed 1, 3, or 7

brightly colored balls and spun the wheel for six trials each lasting 20 s and

separated by 10-s intervals. Prior to recording EEG for each infant, a 50 V Hz

signal calibration signal was input into each of the channels, amplified, and

recorded. The infants head was measured in order to select an appropriate sized

Lycra stretch cap with electrodes for EEG recording sewn into the fabric according

to the 1020 system of electrode placement (Jasper, 1958). In order to ensure that

the cap stayed in place during recording, elastic straps on each side of the cap were

attached to a chest strap.

A small amount of Omni-Prep gel was inserted into each of the active (F3,F4, F7, F8, Fz, C3, C4, P3, P4, Pz, O1, O2, T7 and T8) and referenced sites (CZ)

and then each site was gently abraded with a blunt end of a Q-tip. Next a small

amount of electrolyte gel was inserted and the Q-tip was used to ensure contact

with the scalp. Impedances were measured at each site and were considered

acceptable if they were below 10 K ohms.

One channel of electrooculogram (EOG) was recorded from the left eye

using two Beckman mini-electrodes, one placed at the supra orbit, and the second

at the outer canthus position. EEG and EOG were amplified with a high pass

setting at .1 Hz and a low pass setting at 100 Hz on custom bio-amplifiers made by

SA Instrumentation. The EEG data were digitized at a rate of 512 Hz throughout

the experiment and then re-referenced using software that analyzed the data with

using the average reference configuration. The digitized data were then displayed

graphically for artifact scoring. Portions of EEG marked by movement artifact

were removed from all channels of the EEG record prior to further analysis. The

blinks were regressed out of the portions of EEG marked with eye movement.

The re-referenced, artifact-scored EEG data were submitted to discrete

Fourier transform analysis and power in picowatt ohms (or microvolts squared) for

each channel was computed. Spectral power data in single Hz frequency bids from

130 Hz were computed for each of the stimulus conditions at each of the


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collection sites. Power in the 69 Hz frequency band was computed for each siteby summing the single hertz bins in these four frequencies for each stimulus

condition. The 6-9 Hz band was utilized since this band for 9 month olds is thought

to reflect alpha like activity (Marshall, Hardin, & Fox, 2005). The data used in the

analyses were the log power data from the frontal regions (F3 and F4). Activation

and power in the Alpha band are thought to be reciprocally related (Davidson,

1988), where high power reflects low activation and low power reflects high

activation.

Maternal report of infant temperament. Mothers were asked to complete

an infant report of temperament using the Infant Behavior Questionnaire at 9

months (IBQ; Rothbart, 1981). The IBQ is an 87-item parent report that asks

parents to rate the frequency of behaviors using a 7- point scale. The scales used in

this study were the Fear (distress and extended latency to approach novel orintense stimuli), and Smiling and Laughing scales.

Results

We conducted multiple analyses in order to study the relations of early

social communication, temperament, and frontal power. For means and standard

deviations see Table 1 and for correlations see Table 2. Only those children who

received at least 14 of the possible 21 trials were included in the analysis. Sixteen

children had an inadequate number of trials (3 exuberant children, 4 fearful

children, and 9 control children) and therefore were not included in the analysis.

Table 1. Descriptive Statistics

Table 2. Correlations between Initiating Joint Attention and Initiating Behavioral Requests

Mean SD n

IJA total 0.92 0.46 203

IJA positive 0.21 0.22 203

IJA neutral 0.69 0.42 203

IJA negative 0.02 0.05 203

IBR total 0.55 0.30 203

IBR positive 0.09 0.12 203

IBR neutral 0.45 0.28 203

IBR negative 0.01 0.04 203

Pleasure 5.05 0.78 190

Fearfulness 2.60 0.71 189

IJA IJA IJA IJA IBR IBR IBR IBR

Total Pos Neutral Neg Total Pos Neutral Neg

IJA total 1.00

IJA positive 0.39 * 1.00

IJA neutral 0.87 * -0.10 1.00

IJA negative 0.17 * -0.06 0.09 1.00

IBR total 0.13 0.07 0.11 -0.01 1.00

IBR positive 0.03 0.46 * -0.21 * -0.02 0.32 * 1.00

IBR neutral 0.12 -0.13 0.21 * -0.03 0.90 * -0.10 1.00

IBR negative 0.01 -0.02 -0.01 0.25 * 0.19 * 0.00 0.07 1.00


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n = 203; * p < .05First we investigated whether positive affect was more likely to accompany

joint attention than behavioral requests. We calculated the percentage of IJA bids

that were accompanied by positive affect and the percentage of IBR bids that were

accompanied by positive affect and compared them in a paired sample t-test.

Positive affect was significantly more likely to accompany joint attention than

behavioral requests (t(1,201)=4.501,p < .001).

Next we investigated whether maternal report of pleasure and fearfulness

was correlated with joint attention. As a preliminary analysis, we investigated

whether there were any differences in maternal report of temperament at 9 months

between the 4-month temperament groups in an ANOVA. No differences were

found for pleasure ratings (F(2,187) = .271, ns) and fearfulness ratings (F(2,186) =

.862, ns). Therefore, we combined the temperament groups in the subsequentanalysis. The ratio of joint attention and behavioral request bids was used because

the total number of segments was related to the number of joint attention and

behavioral request bids. We found that fearfulness ratings were related to total IJA

bids (r= .204,p < .01, n = 189), neutral IJA bids (r= .145,p < .05, n = 189), and

negative IJA bids (r= .177,p < .05, n = 189). We also found that pleasure ratings

were related to positive IJA bids (r = .166, p < .05, n = 189). There were no

significant relations between IBR and maternal report of pleasure or fearfulness.

In addition, wee also investigated whether frontal activation was related to

IJA and IBR (see Table 3). We predicted total IJA at 9 months in a model with left

frontal power (6 to 9 Hz) and right frontal power (6 to 9 Hz). The model with left

frontal power was significant (F(1,160) = 4.089,p < .05; (= .158, t(159) = 2.022,p < .05). The model with left and right frontal power was also significant (F(2,159)

= 3.944, p < .05). Only the main effect for left frontal power was significant (=

.37, t(159) = 2.754, p < .01). None of these relations were significant when

predicting positive or neutral IJA attempts.

Predicting Initiating Behavioral Requests

Variable R Adj-R p

Step 1 (df 1/160) 0.006 0.000

Left Frontal Power -0.081

Step 2 (df 2/159) 0.025 0.012

Left Frontal Power -0.271 0.05

Right Frontal Power 0.233

Table 4. Predicting Initiating Behavioral Requests

Predicting Initiating Joint Attention

Variable R Adj-R p

Step 1 (df 1/160) 0.025 0.019 0.05

Left Frontal Power 0.158 0.05

Step 2 (df 2/159) 0.047 0.035 0.05

Left Frontal Power 0.369 0.01

Right Frontal Power -0.259

Table 3. Predicting Initiating Joint Attention


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To assess whether frontal activation was related to IBR (see Table 4) we

predicted total IBR at 9 months in a model with left frontal power (6 to 9 Hz) and

right frontal power (6 to 9 Hz). The model with left frontal power was not

significant. The model with left and right frontal power was also not significant.

However, the main effect for left frontal power (= -.27, t(159) = -1.998,p < .05)

was significant. There were no significant relations for predicting positive or

neutral IBR.

Discussion

The major goal of this study was to describe how reactivity relates to early

social communication. Infants who are temperamentally fearful may be more likelyto initiate joint attention because they are more vigilant while infants who are

temperamentally positive may be more likely to initiate joint attention because they

have positive experiences that they want to share with a social partner. In our

investigation of these processes we took into account the affective quality of each

initiating joint attention or behavioral request bid.

Our findings suggest positive affect is more likely to accompany joint

attention than behavioral requests, and that differences in temperament are

associated with the display of joint attention that varies in affective valence. When

we investigated maternal report of temperament we found associations with IJA

but not with IBR. Vaughn et al. (2003) also found that IJA, but not IBR, was

related to maternal report of pleasure and fearfulness. One explanation for this

finding is that mothers may base their temperament ratings on salient moments of

their interactions with their infants (Hane, Fox, Polak-Toste, Ghera, & Guner,

under revision). Periods of shared attention may be particularly salient instances of

a mothers time with her infant. More specifically, we found that infants who were

rated as more fearful at 9 months initiated more joint attention. When the affective

quality of the IJA bid was considered, IJA bids accompanied by both negative and

neutral affect were related to maternal report of fearfulness while IJA bids

accompanied by positive affect were related to maternal report of pleasure.

Interestingly, when we analyzed frontal power in our sample, IJA was

associated with left frontal hypoactivation and greater right activation. Although

this finding is inconsistent with previous EEG findings, which have suggested a

greater relation between joint attention and left frontal activation, the results are inaccordance with an emerging notion that IJA may be more strongly associated with

negative affect and cautious motivation tendencies, particularly in younger infants.

The display of negative affective motivation tendencies associated with relative

right frontal activation is also logical within the particular methodology used to

examine joint attention skills in this experiment. Specifically, the ESCS paradigm

in this study examined IJA and IBR behaviors that occurred between the infant and

a relatively unfamiliar adult. One can concede that this version of the paradigm

may naturally lend itself to the observation of more vigilant behaviors with the


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infant alternating focus between the novel object and the novel adult, especially ifthe infant is high in negative reactivity.

These frontal activation patterns can also be considered in the framework

of their connections with other neural regions. In particular, the developing

prefrontal cortex is known to have connections with limbic regions including the

amygdala, which is the predominant structure associated with affective functions.

A significant amount of research has highlighted the role of the amygdala in

emotional processes (LeDoux, 1996), and especially in the context of fear

conditioning (LeDoux, 1993). Recently, Davidson (2004) has suggested that the

prefrontal cortex may play a primary role in inhibiting amygdala activity. This

region may both inhibit the amygdala and moderate activity in parts of the neural

circuit that control affective responses. This notion fits well with our finding that

IJA in 9-month-olds was associated with greater right activation and presumablydecreased inhibition of the amygdala. Furthermore, this explanation becomes more

plausible when one considers that a substantial amount of attention we observed

may be more closely related to information seeking or vigilance instead of

information sharing. Lastly, when we investigated the role of frontal power with

just those instances of joint attention that were accompanied by positive, neutral, or

negative affect, no relations between frontal sites and IJA were found.

With regards to IBR, our findings indicate a frontal power pattern opposite

of that found in IJA with left frontal activation. This result suggests that IBR are

related to approach tendencies, which is consistent with prior neural activation

findings of greater left frontal activation in association with approach behaviors

(Davidson & Rickman, 1999; Fox, 1991; Fox & Davidson, 1987; Fox et al., 2001).

The underlying circuitry of approach behaviors has been put forth in a variety ofneuroanatomical models, most of which reference the prominent role of dopamine

transmission and corresponding states of appetitive motivation (Depue & Collins,

1999; Derryberry & Rothbart, 1997).

Despite the seemingly disjointed patterns found between frontal power in

IJA and in IBR, the results may actually help to clarify our understanding of

attention skills that contribute to, or facilitate, the development of social

communication. For instance, IJA and IBR are unique components of social

communication, each of which develops in a slightly different manner (Mundy et

al, 2000; Nichols, Fox, & Mundy, 2005). However, the question remains as to

whether, or in what manner, IJA and IBR mutually influence each other in the

progression of social abilities.

Several limitations are worth noting. In these analyses highly reactive

children were over sampled and thus the findings are most generalizable to highly

reactive infants. Another limitation involves the frequency that negative and

positive bids were observed. Instances of negatively toned IJA were rare, and

therefore, caution should be used when interpreting the findings. Future studies

should continue to investigate individual differences in emotional reactivity and

frontal brain systems in order to better understand how they relate to the

development and expression of early social behavior.


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