Cogniie, Creier, Comportament / Cognition, Brain, Behavior Vol.

IX(3), 317-328, 2005 Romanian 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. We examined individual differences in this skill as a function of temperament and neural activity in nine-month-old infants. We found that maternal ratings of temperament were associated with joint attention, an important index of early social communication. More specifically, maternal ratings of pleasure were associated with joint attention bids that were accompanied by positive affect, while maternal ratings of fearfulness were associated with joint attention bids that were accompanied by negative affect. We also found that initiating joint attention 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 development of 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 20742 Email: knichol3@umd.edu

substantia nigra are established well enough to allow for the inhibition of reflexive orienting 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 and colleagues (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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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 positive temperament 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 stressrelated 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 association with 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 social communication 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 Communication Scales (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 active mechanical 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 site by 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 or intense 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
IJA total IJA positive IJA neutral IJA negative IBR total IBR positive IBR neutral IBR negative Pleasure Fearfulness Mean 0.92 0.21 0.69 0.02 0.55 0.09 0.45 0.01 5.05 2.60 SD 0.46 0.22 0.42 0.05 0.30 0.12 0.28 0.04 0.78 0.71 n 203 203 203 203 203 203 203 203 190 189

Table 2. Correlations between Initiating Joint Attention and Initiating Behavioral Requests
IJA total IJA positive IJA neutral IJA negative IBR total IBR positive IBR neutral IBR negative IJA Total 1.00 0.39 * 0.87 * 0.17 * 0.13 0.03 0.12 0.01 IJA Pos 1.00 -0.10 -0.06 0.07 0.46 * -0.13 -0.02 IJA Neutral IJA Neg IBR Total IBR Pos IBR Neutral IBR Neg

1.00 0.09 0.11 -0.21 * 0.21 * -0.01

1.00 -0.01 -0.02 -0.03 0.25 *

1.00 0.32 * 0.90 * 0.19 *

1.00 -0.10 0.00

1.00 0.07

1.00

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n = 203; * p < .05

First 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 subsequent analysis. 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.
Table 3. Predicting Initiating Joint Attention Predicting Initiating Joint Attention
Variable Step 1 (df 1/160) Left Frontal Power Step 2 (df 2/159) Left Frontal Power Right Frontal Power R 0.025 0.047 Adj-R 0.019 0.035 0.369 -0.259 0.158 p 0.05 0.05 0.05 0.01

Table 4. Initiating Behavioral Behavioral Requests Predicting Predicting InitiatingRequests 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 Iunie 2005 Cogniie, Creier, Comportament 323

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 likely to 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 in accordance 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 if the 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 presumably decreased 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 of neuroanatomical 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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