greater right frontal eeg asymmetry and nonemphathic behavior are ...

Intern. J. Neuroscience, 114:459–480, 2004 Copyright  Taylor & Francis Inc. ISSN: 0020-7454 / 1543-5245 online DOI: 10.1080/00207450490422786

GREATER RIGHT FRONTAL EEG ASYMMETRY AND NONEMPHATHIC BEHAVIOR ARE OBSERVED IN CHILDREN PRENATALLY EXPOSED TO COCAINE NANCY AARON JONES Florida Atlantic University John D. MacArthur Campus Jupiter, Florida, USA

TIFFANY FIELD Touch Research Institute University of Miami School of Medicine Miami, Florida, USA

MARISABEL DAVALOS University of Miami Coral Cables, Florida, USA

SYBIL HART Texas Tech University Lubbock, Texas, USA Responses to emotion-inducing stimuli were examined in 27, 3- to 6year-old children, who were prenatally exposed to cocaine, and 27 unexposed controls. Children were monitored for EEG activity and their Received 26 July 2003. We would like to thank the mothers and infants who participated in this research. This research was conducted at the University of Miami School of Medicine. This research was supported by a March of Dimes Grant (#FY961016) to Tiffany Field. Address correspondence to Nancy Aaron Jones, Florida Atlantic University, John D. MacArthur Campus, 5353 Parkside Dr., Jupiter, FL 33458, USA. E-mail: [email protected]

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N. A. Jones et al. affect during an infant crying, simulated maternal distress, and a mildly frustrating task. Multivariate analyses indicated that the cocaine-exposed children had greater right frontal EEG asymmetry, showed fewer empathic reactions to a crying infant as well as to their own mothers, and they were less proficient in completing a cooperative task. These findings highlight the need for continued longitudinal research on the effects of early drug exposure for later socioemotional development. Keywords cocaine use, EEG, emotions, empathy, frustration, preschoolers

A mothers’ cocaine and polydrug use poses risks to infants and children. Recent theories and research efforts have begun to focus on neuroregulatory behaviors, yet few studies have extended beyond the first year of life. Lester and Tronick (1994), in their theoretical model, argue that behavioral dysregulation noted in infants and children who are cocaine-exposed are manifested in deficits in attention, arousal, affect, and action. For example, cocaine-exposure has been associated with infants’ irritability, mood swings, and poor scores on behavioral assessment scales, leading several investigators to hypothesize that cocaine effects the development of the central nervous system (Eisen, Field, Bandstra, Roberts, Morrow, Larson, & Steele, 1991; Giacola, 1990; Rodning, Beckwith, & Howard, 1989a). Although several studies have assessed neurobehavioral regulation during infancy (Eisen et al., 1991; Giacoia, 1990; Scafidi, Field, Wheeden, Schanberg, Kuhn, Symanski, Zimmerman, & Bandstra, 1996; Zuckerman & Bresnahan, 1991), few studies have examined the long-term effects of cocaine-exposure on biobehavioral regulation patterns. Therefore, the purpose of the present study was to examine affective and physiological responses in preschool and elementary school-aged children known to be exposed to cocaine during the prenatal period. Infants prenatally exposed to cocaine experience various developmental deficits. These deficits include physical and maturational delays (Chasnoff, Griffith, MacGregor, Dirkes, & Burns, 1989; Dominguez, Vila-Coro, Slopis, & Bohan, 1991; Hadeed, & Siegel, 1989; Lester, Corwin, Sepkoski, Seifer, Peucker, McLaughlin, & Golub, 1991; Lipshultz, Frassica, & Orva, 1994; Lutiger, Graham, Einarson, & Koren, 1991; MacGregor, Keith, & Chasnoff, 1987; Scafidi, Field, Wheeden, Schanberg, Kuhn, Symanski, Zimmerman, & Bandstra, 1996; Singer, Garber, & Kliegman, 1991; Woods, Plessigner, &

Cocaine, Empathy, and EEG

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Clark, 1987; Zuckerman, Frank, Hingson, Amaro, Levenson, Kayne, Parker, Vinci, Aboagye et al., 1989), as well as cognitive delays (Azuma, & Chasnoff, 1993; Bendersky, Alessandri, Sullivan, & Lewis, 1995; Chasnoff, Griffith, Freier, & Murray, 1992; Lifschitz, Wilson, Smith, & Desmond, 1985; Mayes, Bornstein, Chawarska, & Granger, 1995; Singer, Arendt, Farkas, Minnes, Huang, & Yamashita, 1997). Although we know that emotional responses are altered by cocaine’s effects on specific areas of the brain in adult users (Alper, Chabot, Kin, & Prichep, 1990; Giacoia, 1990; Prichep, Alper, Kowalik, Vaysblat, Merkin, Tom, John, & Rosenthal, 1999), its effects on the affective responses of infants and children prenatally-exposed to cocaine are unknown. However, several important studies have shown differences in children’s temperament as a consequence of early cocaine exposure (Alessandri, Sullivan, Bendersky, & Lewis, 1995; Alessandri, Sullivan, Imaizumi, & Lewis, 1993; Bendersky, Alessandri, & Lewis, 1996; Bendersky et al., 1995; Eisen et al., 1991; Field, 1995; Ukeje, Bendersky, & Lewis, 1999; Zuckerman & Bresnahan, 1991). The capacity to respond empathetically and non-aggressively to emotion-eliciting situations is fundamental to the development of satisfying interpersonal relationships and the ability to learn from situations and people in the environment (Eisenberg, 1989; Saarni, 1999). When frustrated during a learning task, infants exposed to cocaine have demonstrated less arousal, expressed less interest, fewer positive emotions, and more anger (Alessandri et al., 1993). Magnano, Garder, and Karmel (1992) found that during mildly stressful situations, cocaine-exposed infants showed lower cortisol levels, suggesting the presence of regulatory problems even under normally stressful events. However, these studies did not examine the longterm consequences for these children’s physiological and behavioral functioning. Moreover, studies examining older children have been somewhat inconsistent (Chasnoff et al., 1992; Griffith, Azuma, Chasnoff, 1994; Schneider & Chasnoff, 1987). Brain electrical patterns (as measured by an electroencephalograph, EEG) have been shown to relate to variations in temperament, specifically, individual differences in emotional reactivity and regulation during childhood (Fox, 1994). For example, one study revealed that childhood social withdrawal is related to greater right

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frontal EEG activity (Fox, Rubin, Calkins, Marshall, Coplan, Long, & Stewart, 1995). In addition, our own studies have shown that 3to 6-year-old children of depressed mothers show right frontal EEG asymmetry, a pattern which may relate to greater negative affect (Jones, Field, & Davalos, 2000) and remains stable among children of depressed mothers (Jones, Field, Davalos, & Pickens, 1997). Yet no studies have examined the association between brain electrical activity and temperament in children prenatally exposed to cocaine. Of the relatively few longitudinal studies of prenatally exposed infants, Rodning, Beckwith, and Howard (1989b) found that by toddlerhood, cocaine-exposed children did not show typical distress responses when separated from attachment figures. Beckwith and colleagues (Beckwith, Rodning, Norris, Phillipsen, Khandabi, & Howard, 1994) demonstrated altered play patterns among toddlers of drugusing mothers, including less mature play, more deviant behaviors, and fewer positive social interactions. Taken together, these data suggest that lack of emotional responsiveness, overreactivity to stimulation, and limited resources for emotional regulation may be risk factors associated with prenatal cocaine exposure (Chasnoff et al., 1992). The present study compared cocaine-exposed children to control children on tasks designed to elicit emotional responses. The cocaine-exposed children were expected to show fewer empathic responses to the crying of an infant and to the simulated distress of their mothers, difficulty completing a frustrating task, and greater right frontal asymmetric EEG patterns.

METHOD Participants Children and their biological mothers were recruited from the hospital’s substance abuse clinic or the prenatal care clinic during infancy. These children were a part of a larger longitudinal study on cocaine-exposure and infant and child development. The present study reports on the 54 families (27 prenatally exposed to cocaine and 27 non-exposed controls) that participated in the 3- to 6-year


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follow-up. Table 1 reports the demographic characteristics of the sample for this study. The children ranged in ages between 3 and 6 years (M = 4.0, SD = 1.1), and their mothers were of low socioeconomic status (Hollingshead, 1975; M = 4.5, SD = 0.7) and were distributed 66.7% African American and 33.3% Hispanic. At the time of testing, the groups did not differ on demographic factors. Since there are reports that polydrug use is common among cocaine users (Day & Richardson, 1994; Matera, Warren, Moomjy, Fink, & Fox, 1990) and since we had no reason to believe that the cocaine-using mothers in the present sample differ from others, we considered them polydrug users (cocaine, alcohol, nicotine, and caffeine). Information collected during infancy and during the 3–6 year follow-up showed that the cocaine group used more alcohol than controls, χ 2 (1, N = 54) = 7.34, p < .05, but no differences were reported in caffeine, nicotine, and marijuana. Because mothers differed in alcohol use, this variable was included as an additional grouping factor, however, all analyses using alcohol alone as a grouping variable were not significant and are not reported here. Mothers also provided information about their child’s birth and delivery characteristics. Only healthy full-term infants were chosen

TABLE 1. Demographic data

Mother’s age (in years) Marital status (% Single) SES: Hollingshead Ethnicity African American White, Hispanic Drug use (% yes) Caffeine Nicotine Alcohol Marijuana Education (in years) BDI Child’s age (in years) WPPSI total score

Cocainea

Controlb

28.4 (3.4) 66.7% 4.6 (0.4)

26.6 (4.4) 72.0% 4.4 (0.9)

52.8% 47.2%

44.4% 55.6%

92.3% 69.2% 65.4% 19.2% 12.1 (1.7) 7.3 (7.4) 4.2 (1.0) 97.9 (1.1)

78.6% 60.7% 28.6%* 10.7% 11.8 (1.4) 4.6 (3.0) 3.8 (1.0) 97.0 (1.0)

Note. Values represent mean scores. Standard deviations are in parentheses. a n = 27. bn = 27. *p < .01.

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for the original sample; thus, records and maternal reports obtained during the infant assessment indicated no serious peri- or postnatal complications (e.g., prematurity, low birth weight, small head circumference, etc.). At the 3–6 year assessment, families who were invited to participate did not have serious health problems, and based on the Wechsler Preschool and Primary Scale of Intelligence (WPPSI, Wechsler, 1967), children did not differ in overall cognitive functioning, F < 1. Thus, risk factors associated with health and cognitive development were experimentally controlled for in this study. The groups also were similar in their socioeconomic status, and both groups of children were exposed to similar impoverished environments during development. Laboratory Procedures Mothers who had reported prenatal cocaine use and whose medical records confirmed that use (based on maternal urine and infant meconium samples) were assigned to the cocaine group. Mothers who reported no history of substance abuse and whose tests were negative during pregnancy were assigned to the control group. During the laboratory session, mothers were asked to complete the Beck Depression Inventory (BDI, Beck, Ward, Mendelson, Mach, & Erbaugh 1961), a demographic questionnaire, and a drug checklist. They were also asked to rate their child’s behavior on Conners Parent Rating Scale (Conners, 1985). This scale is designed to assess maternal perceptions of anxiety, hyperactivity, impulsive behaviors, learning problems, psychosomatic symptoms, and conduct problems. The children’s EEG activity was recorded prior to their responses to the emotion-inducing situations, including two empathy tasks and a mildly frustrating task. EEG was recorded during a non-stimulus session (i.e., a baseline session) to obtain an index of tonic EEG activation asymmetries, because the tasks chosen involved significant movement, which would have created a significant degree of artifact in the EEG recordings (Field et al., 1995; Fox et al., 1995; Jones et al., 2000; Schmidt, Fox, Schulkin, & Gold, 1999). For the empathy tasks, children’s behaviors were examined in response to a crying infant (modeled after Zahn-Waxler, Friedman, & Cummings, 1983) in response to simulated maternal distress (modeled


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after Radke-Yarrow, Zahn-Waxler, Richardson, Susman, & Martinez, 1994). For the frustration task, children and their mothers were examined during the process of opening a Chinese magic box, a task that requires mutual cooperation to complete. EEG Recordings Children were asked to sit still with their eyes open during a 3 min EEG recording. A stretch lycra cap (Electro-Cap, Inc.) with the international 10–20 system was positioned on the participant’s head. Omni-prep gel (to abrade the scalp gently) and electrode gel (to provide good conductance) were inserted into the mid-frontal (F3 & F4), temporal, (T3 & T4), parietal (P3 & P4), and occipital (O1 & O2) sites and referenced to the vertex site (Cz). Although there have been questions concerning the appropriate reference location (Davidson, 1988; Hagemann, Naumann, & Thayer, 2001), in the present study, the vertex reference was used to record on-line, and then data were re-referenced offline to a computer-generated average reference (James Long Inc., 1991). Similar methods of EEG data collection have been used for examining the association between EEG activity and temperament in children (Schmidt et al., 1999). Data were displayed on a computer monitor. EOG was also obtained using two Beckman electrodes, one placed at the outer canthus and the second placed at the supra orbit position of the right eye. All electrode impedances were required to be less than 5K ohms, or the site was re-abraded with the blunt end of a Q-tip. The signal was passed through a Grass Model 12 Neurodata Acquisition System. The output from each amplifier was directed to a Dell 325D PC fitted with an Analog Devices RTI-815 AID board. The data were bandpassed from 1 to 100 Hz. The sampling rate was 512 samples per second, and the data were streamed across the computer screen and saved on a hard disk using data acquisition software (Snapstream, v. 3.21, HEM Data Corp., 1991). EEG Analysis Artifact in the EEG was underscored by using the EOG channel as a cue for eye movement and motor artifact using visual displays

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and manual elimination of artifact. The data containing eye or muscle artifact were eliminated from each channel by technicians trained to identify the artifact. The reliability of the artifact scorers was >.90. The data were submitted to a discrete Fourier Transform using a Hanning Window with 50% overlap. This analysis produced power for each single hertz frequency bin in picowatt ohms (equal to 1 microvolt2) for each channel. After spectral plots were made on a subsample of the children, we determined that the 6–9 Hz band would be used. Previous research has shown that children have a shift in alpha band frequencies across development (Bell, 2002; Pivik, Broughton, Coppola, Davidson, Fox, & Nuwer, 1993), and that the 6–9 Hz frequency band in children of this age is similar to the characteristics of the alpha band in adults (Schmidt et al., 1999). Thus, we used this frequency band for the analyses. Frontal, temporal, parietal, and occipital alpha EEG asymmetry scores were computed using the natural log power of the scores in each region. The asymmetry score is a difference score, reflecting the power in one hemisphere relative to the power in the contralateral hemisphere (ln (Right) minus (ln (Left)). Power scores and activation scores are reciprocal. Therefore, this computation produces values in which greater scores indicate greater relative left hemisphere EEG activation asymmetries. Infant Crying Situation In a modified version of the task described by Zahn-Waxler and colleagues (Zahn-Waxler et al., 1983), a mother was asked to leave the room, and her child was asked to remain in the room, sitting in a chair. The children were told that the experimenter was just outside the room if they needed anything. After each mother left the room, children heard an audiotape of an infant crying. This cry was played for 60 s, after which a confederate examiner, pretending to be a “mother,” entered the room and asked the child if she or he had seen her baby’s bottle. The baby bottle was in plain view of the child. This situation lasted for 60 s or until the child pointed to the bottle. Children’s responses were scored from videotapes by two coders who were blind to the group status of the child.


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Coding of infant crying situation. The child’s responses were coded for both the “infant crying” and the “mother searching” for the bottle segment. First, latency to respond was scored for each child. Second, the child was also scored on the degree of prosocial behavior towards the “mother” on the following scale: no response (either verbally or by gesture) was scored as 0; recognition was scored as 1; verbal non-helping (e.g., saying “I don’t know” or “No”) was scored as 2; gesture/non-helping (e.g., shrugging) was scored as 3; verbal-only helping (e.g., saying “right over there,” but not pointing) was scored as 4; verbal and by gesture helping (e.g. saying “over there on the table” and pointing to the bottle) was scored as 5. If two responses were noted during the session, the child was given the highest score. Third, negative affect (facial expressions of distress or anxiety) was coded as present (score of 1) or absent (score of 0) during the infant crying and during the mother searching conditions (time-sampled in 2, 30-s scores). Two coders scored 25% of the videotapes, and agreements versus disagreements were computed. inter-observer reliability was computed by Cohen’s Kappas (M = .86, range .79 to .91). Magic Box Task The mother was provided a Chinese magic puzzle box that requires several maneuvers to open. This task has been used previously to examine differences between depressed and conduct disorder children (Field, Sandberg, Goldstein, Garcia, Vega-Lahr, Porter, & Dowling, 1987). Each mother was shown how to open the box prior to the task initiation. She was then instructed to show the child how to open the box through a physical demonstration followed by verbal instructions. The child was promised a reward upon completion of the task. This mutual cooperation task lasted 5 min or until the child opened the box. Coding of magic box task. The child’s behavior was coded from the videotapes by observers who were blind to the child’s group status. Data were on a second-by-second basis and then converted to percentages. The behaviors coded for the child during this task included on-task activity (versus off-task), asking the mother for help,

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and affect. The latter affect was rated on a Likert scale, from 1 to 3, with 1 for positive affect, 2 for neutral affect, and 3 for negative affect. The child’s success at opening the box and the number of time sampling units (TSUs) to open the box (a maximum of ten, 30-s time-sampling units) were also recorded. The behaviors coded for the mother included requesting attention, helping (versus not helping) the child verbally, and the number of remarks of approval/ disapproval, with the latter scores designed as tallies of positive and negative remarks. Affect was also rated for the mother using a Likert scale, with 1 indicating positive affect, 2 indicating neutral affect, and 3 indicating negative affect. This task and coding procedure were taken from a similar study on conduct disorder and depressed children (Field et al., 1987). Inter-observer reliability was calculated by determining the number of agreements and disagreements for two coders on 25% of the videotapes. Reliability was calculated by Cohen’s Kappa (M = .79, range of .73 to .89). Simulated Maternal Distress The final procedure involved an assessment of the children’s empathy toward their mothers. Mothers were asked to cover their face with their hands and simulate sobbing sounds for 2 min. If queried by the child as to the source of her distress, each mother was instructed to say she was not feeling well. The mothers also were asked not to instruct the children to perform any specific actions, but to let the children respond as they naturally would to the distress sounds. Children were debriefed after this task by the experimenter, explaining that their mothers were asked by the experimenter to pretend to be distressed. Coding of simulated maternal distress. Two observers (who were blind to the group status of the dyad) coded the child’s videotaped responses during the simulated maternal distress. Two coding systems were used. The observers coded and tallied the number of empathic and non-empathic behaviors. Empathic behaviors included asking “what’s wrong,” hugging, holding mom’s hand, patting mom’s head, touching mom affectionately, giving mom a toy, or going to get help from the experimenters. Nonempathic behaviors included walking away from mom; standing silently, looking for or playing with


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toys, wandering around room, looking out the window, sitting or lying in front of mom; physically striking their mom, and demanding her to cease crying. A second coder rated the child using an empathy scale described by Frankel and colleagues (1992). Ratings were made on a 5-point scale, with 1 indicating “very low” and 5 indicating “very high” for each child on the following 8 behaviors: denial (looking or backing away); caring (verbal or nonverbal solutions to alleviate the distress); empathy (level of concern or worry); hypothesis testing (asking questions); latency (time before a response); freezing (remaining motionless); callousness (aggressive or insensitive responses); and inappropriate affect (pleasure or laughing). As a validity check, mothers were also rated on their degree of credibility/ drama during their simulated distress on a similar 5 point scale. Interobserver reliability was calculated on 25% of the videotapes by Cohen’s Kappa (M = .91, range .86 to .96). RESULTS Maternal Report Multivariate analyses of variance (MANOVAs) were conducted on the mothers’ ratings of their children using drug status (cocaine versus control) as the grouping variable and six composite scores of the Conner’s Parent Rating Scores as the dependent variables. The results are presented in Table 2. Analyses of the scores on the Conner’s scale revealed that in comparison with controls, the cocaine-exposed mothers reported more overall problems in their children’s behaviors, Wilks’ Λ = .72, F(5,48) = 3.56, p < .05 and overall between-subjects effect for group, F(1‚52) = 14.66, p < .05. Follow-up ANOVAs showed that mothers in the cocaine group reported more conduct problems, F(1,54) = 7.66, p < .05, anxiety, F(1,54) = 5.12, p < .05, impulsive behaviors, F(1,54) = 19.49, p < .05, and hyperactivity, F(1,54) = 17.10, p < .05, than the control mothers on the Conner’s scale. EEG Analyses Group (cocaine-exposed versus control) × Region (frontal, temporal, parietal, occipital) repeated measures MANOVAs were conducted

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N. A. Jones et al. TABLE 2. Maternal ratings of cocaine-exposed versus control children Cocainea Conners Conduct problems Learning problems Psychosomatic Impulsive behaviors Anxiety Hyperactivity

72.8 52.7 74.3 54.2 52.1 56.4

(27.6) (14.6) (41.6) (12.8) (12.7) (13.5)

Controlb

50.8 45.6 53.0 45.8 46.4 43.0

(8.7)* (13.7) (20.0) (7.9)* (5.7)* (6.7)**

Note. Values represent mean scores. Standard deviations are in parentheses. a n = 27. bn = 27. *p < .05; **p < .01.

using the children’s EEG asymmetry score as the dependent variable. This analysis yielded a significant multivariate within-subjects Group × Region interaction effect, Wilks’ Λ = .83, F(3,49) = 3.30, p < .05. Subsequent ANOVAs, separately for each region, revealed that the group differences were in the frontal region, with greater relative right frontal asymmetry in the cocaine-exposed group than in the control group, F(1,51) = 4.23, p < .05 (Figure 1). To examine hemispheric differences between cocaine-exposed and control children, a Group (cocaine versus control) × Region (frontal, temporal, parietal, occipital) × Hemisphere (right versus left) repeated-measures MANOVA was conducted using the EEG power scores as the dependent variable. This analysis yielded a significant between-subjects main effect for Group, F(1, 51) = 5.84, p < .05, and a marginally significant within-subjects main effect for Region, F(3,49) = 2.71, p = .06, but no significant interaction effects. An examination of the means and follow-up ANOVAS, separately for each region, showed that the cocaine-exposed group showed less right and left hemisphere power (greater right and left hemisphere activation) in each region than the control group. Infant Crying Situation A MANOVA was also conducted on the children’s behavioral responses during the infant crying situation. The results demonstrated that the children in the cocaine group had a different overall response to this situation than children in the control group, F(4,48) = 9.92, p < .05. Follow-up ANOVAs showed that the children in the


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FIGURE 1. Frontal, temporal, parietal, and occipital EEG asymmetry scores in cocaineexposed and control children.

control group had higher ratings on their prosocial responses, F(1,51) = 10.03, p < .05, i.e., were more likely to use verbal responses and gestures to help the “searching mother” find the bottle than the children in the cocaine group. Moreover, an ANOVA demonstrated that the children in the cocaine-exposed group had lower affect scores during the sound of the crying infant, F(1,51) = 30.05, p < .05, suggesting that the cocaine-exposed group were less negatively expressive during this sound (Table 3). Simulated Maternal Distress During the situation designed to examine empathic responses to their mother’s distress, children in the cocaine-exposed group also

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showed fewer empathic responses. Chi square analyses were performed comparing the cocaine versus control children and the overall judgments of their empathic or nonempathic responses. This analysis yielded a significant effect, χ 2 (1, N = 54) = 13.17, p < .05, suggesting that more children in the control group were judged as empathic during the mothers’ simulated distress (88%) than were children in the cocaine group (37%) (Table 3). ANOVAs comparing the tallied number of empathic versus nonempathic responses demonstrated that the cocaine-exposed group demonstrated fewer empathic behaviors, F(1, 51) = 4.16, p .05. There were also no differences between groups for maternal credibility in displaying the simulated cry, p > .05. Magic Box Task To examine whether dyads differed in their ability to complete the magic box task, an ANOVA was conducted on the time sampling units needed to complete the task, and an overall Chi Square analy-

TABLE 3. Empathy behaviors during infant crying and simulated maternal distress conditions Cocainea Infant crying condition Latency to response Prosocial response (1–5) Affect during crying Affect during “Mother searching” Simulated distress condition Global rating of empathy Yes No Empathic behaviors (N) Nonempathic behaviors (N) Mother credibility

46.2 3.0 0.9 0.6

(14.3) (1.4) (0.6) (1.5)

37.0% 63.0% 1.8 (1.8) 2.6 (1.6) 3.5 (1.2)

Note. Values represent mean scores. Standard deviations are in parentheses. a n = 27. bn = 27. *p < .05; **p < .01.

Controlb

35.0 4.2 2.0 0.3

(19.5) (0.7)*** (0.4)*** (0.4)

88.0% 12.0%* 3.7 (1.7)* 1.9 (1.0)* 3.7 (0.9)


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sis was conducted examining the number of cocaine-exposed versus control group participants who completed versus those who did not complete the task. Results showed that the control group children required less time to complete the magic box task (5.60 versus 6.90 TSUs) than the cocaine group, F(1,51) = 3.80, p < .01, and more children in the control group completed the task than the children in the cocaine group, χ 2 (1, N = 54) = 6.17, p < .05. An additional MANOVA compared the children’s behavior during the magic box task. This analysis revealed no significant differences between the behaviors of the control and cocaine-exposed groups during the task, p > .05. A MANOVA comparing the mothers’ behavior during the magic box task, however, was significant, F(3,49) = 3.94, p < .05. Specifically, mothers in the cocaine group used fewer approval statements than the mothers in the control group, F(1,51) = 11.64, p < .05 (Table 4).

DISCUSSION The greater relative right frontal EEG asymmetry in the cocaine children was predictable inasmuch as the right frontal EEG has been associated with greater negative affect. Although right frontal EEG asymmetry previously has been reported for infants and children of depressed mothers (Field, Fox, Pickens, & Nawrocki, 1995; Jones et al., 2000; Jones et al., 1997; Jones, Field, Fox, Lundy, & Davalos, 1997) and for shy children (Schmidt et al., 1999), this report is the first to demonstrate EEG asymmetry patterns in cocaine-exposed children. When examining the hemisphere differences, greater EEG activation scores were noted in both the right and the left hemispheres for children prenatally exposed to cocaine. This result is consistent with Dawson’s (1994) suggestion that greater activation is associated with higher intensity emotions during stressful situations, and Mayes’ (1999) suggestion that cocaine exposed groups may be hypersensitive to mildly stressful environmental events. In the present study, the greater activation was noted during a resting baseline, suggesting that cocaine-exposed children may have altered biobehavioral regulation patterns and may, in fact, have a lower threshold

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N. A. Jones et al. TABLE 4. Percentage behaviors during magic box task

Child behaviors Asks for help On task #TSU to completion Completion of task (%) Yes No Mother behaviors Requests attention Helping/nonhelping Approval (#) Disapproval (#)

Cocainea

Controlb

2.2 (3.8) 55.0 (23.4) 6.9 (2.8)

1.7 (3.0) 47.4 (18.6) 5.6 (2.3)**

61.5% 38.5%

87.0% 13.0%*

33.6 19.2 2.3 2.3

30.3 18.3 9.1 2.8

(22.6) (24.0) (4.8) (4.4)

(13.7) (19.2) (9.2)** (5.2)

Note. Values represent mean scores. Standard deviations are in parentheses. n = 27. bn = 27. *p < .05; **p < .01.

a

for responding physiologically to environmental situations. This suggestion would be consistent with the data showing that cocaineexposed infants are poor modulators of their reactivity (Magnano et al., 1992), although it counters findings that these infants demonstrate under-arousal of their behavioral and physiological systems (Alessandri, et al., 1993; Lester et al., 1991). The reasons for these inconsistencies need to be further explored, although one possible explanation for the different findings could be related to the developmental level of the participants. Alternatively, the children in the cocaine-exposed groups could have perceived the EEG recording as more stressful than the control group. The elevated scores on maternal-reported anxiety, hyperactivity, impulsive behaviors, and conduct problems among the cocaine-exposed children were not unexpected, as other studies have suggested that cocaine-exposed children are more temperamentally difficult (Alessandri et al., 1995; Lester et al., 1991). Other researchers also have found links between higher internalizing scores (Tsoubris, 1998) and higher externalizing scores in cocaine-exposed children (Azuma & Chasnoff, 1993; Field, 1995; Griffith et al., 1994). Although some of the maternal-reported differences in childhood behaviors may be due to altered maternal perceptions, nonetheless, these data highlight the importance of documenting the variability in childhood


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temperament. Ultimately, individual differences in emotional responses, whether they are real or a merely individual variation in maternal perceptions, effect caregiver-infant relationships. An improved understanding could lead to a better planning of intervention programs. In documenting the important factors that should be considered in intervention program design, Mayes (1999) has suggested that future research and interventions should focus on the following 3 areas: (1) the changes in neural development between 3 to 4 years of age that provide the opportunity for change; (2) the regulatory difficulties in cocaine exposed children that could influence social functioning; and (3) the mental health needs of the children and their families. In addition, we would emphasize a focus on the individual variation of emotional reactivity and regulation that may result from altered physiological and behavioral reactions to the environment. Cocaine-exposed children also were less empathic toward their mothers’ distress and toward that of others (the crying infant and the confederate “mother”) than children in the control group. During the “mother looking for bottle” task, the cocaine-exposed children showed a longer latency to gesture as well as fewer prosocial responses. Most children in the cocaine-exposed group merely shrugged or said they could not find the bottle. Children in the control group were more likely to help verbally or both verbally and with gestures. Theories of prosocial and moral reasoning suggest that empathy increases with age and that the internalization of values and norms also increases as children mature (Eisenberg, 1989; Saarni, 1999). The present data suggest that children prenatally exposed to cocaine may lack this form of emotional progress or may lag in their capacity to empathize. This also is demonstrated in their responses to simulated maternal distress. These are the first data to show that children in the cocaine group were less empathic to their mother’s distress, whereas other studies have not shown a relationship between empathy and cocaine exposure (Field, 1995). However, these data complement other studies that have shown that cocaine-exposed children are less cooperative and show poorer social skills (Edmondson & Smith, 1994). Finally, children in the cocaine group were also less proficient at solving the magic box task (a mildly frustrating task). They did not

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solve the puzzle as quickly as the control children and were less likely to solve the puzzle. These results are similar to those obtained by Field and colleagues (1987) who showed that conduct disorder children were more likely to spend more time off task than control children. Other studies have shown that cocaine-exposed children interact less adaptively with their mothers and with peers (Burns, Chethik, Burns, & Clark, 1997; Field, 1995; Metoksy & Vondra, 1995) than nondrug exposed children. Moreover, infants with difficult temperaments are more likely to show cognitive delays (Sostek & Anders, 1977; Thomas & Chess, 1977), especially in tasks that require attention and persistence (Mayes, Feldman, Granger, Haynes, Bornstein, & Schottenfeld, 1997). Although children in this study showed little evidence of overall cognitive delays, and some studies find no differences in interactive play for cocaine-exposed children (Hagan & Myers, 1997), the children in this study demonstrated subtle differences in their behaviors that had an overriding effect on their ability to finish the task. Another explanation for the inability to complete this task was evident in the coding of the mothers’ behaviors. Mothers in the cocaine-exposed group were less likely to motivate their children by expressing approval statements, whereas the control group significantly showed more approval statements. Studies have demonstrated that caregivers’ responses, especially the contingent responsiveness, are important for the child’s cognitive and emotional development. A caregiver who is able to tune into the child’s temperamental characteristics will positively influence dyadic interaction (Bornstein, 1989). Although the results of this study are intriguing, several limitations of this study must be noted. First, the cocaine-exposed children in this study were all healthy and showed no serious cognitive delays during infancy or childhood. Thus, the present study provides data on a select sample of children, because in some cases cocaine-exposed infants may experience prematurity and other health problems (Scafidi et al., 1996). Secondly, environmental factors, such as family instability, neglect, poor nutrition, poor parenting, a history of child abuse, and family violence were not specifically controlled for in the present sample. However, both groups were from similar environments, which may have helped to reconcile many of these potential confounds. Thirdly, the determination of cigarette, alcohol, marijuana and other


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illicit drug use is imperfect in our study, with documentation based on self-report and limited documentation of dosage levels. Nevertheless, it is widely accepted that substance-abusing adults rarely use cocaine in isolation. Differences in alcohol consumption could have also contributed to the findings. Fourthly, maternal report incidences could have been supported by reports from other adults. However, only some of the participants were in consistent preschools or grade schools, making this assessment impractical for this study. Ultimately, our results are more conservative, because the findings underestimate possibly even larger behavioral differences between groups. In sum, the results of this study are in the predicted direction, with cocaine-exposed children showing less empathic behavior, more maternal-perceived behavior problems, and an inability to complete mildly frustrating tasks. These children also showed greater relative right frontal EEG asymmetry and greater overall EEG activation, which may indicate that they respond more negatively and may have higher intensity responses even during nonstressful conditions. Future studies should further delve into the association between the brain activity patterns noted here and neurochemical findings reported by Mayes and colleagues (1996, 1999), as a window for developing intervention programs. REFERENCES Alessandri, S. M., Sullivan, M. W., Bendersky, M., & Lewis, M. (1995). Temperament in cocaine-exposed infants. In M. Lewis & M. Bendersky (eds.,) Mothers, babies, and cocaine: The role of toxins in development (pp. 273–285). Hillsdale, NJ: Lawrence Erlbaum Associates. Alessandri, S. M., Sullivan, M. W., Imaizumi, S., & Lewis, M. (1993). Learning and emotional responsivity in cocaine-exposed infants. Developmental Psychology, 29, 989–997. Alper, K. R., Chabot, R. J., Kin A. H., & Prichep, L. S. (1990). Quantitative EEG correlates of crack cocaine dependence. Psychiatry Research: Neuroimaging, 35, 95–105. Azuma, S. D., & Chasnoff, I. J. (1993). Outcome of children prenatally exposed to cocaine and other drugs: A path analysis of three-year data. Pediatrics, 92, 396–402. Beck, A. T., Ward, C. H., Mendelson, M., Mach, J. E., & Erbaugh, J. (1961). An inventory for measuring depression. Archives of General Psychiatry, 4, 561–571. Beckwith, L., Rodning, C., Norris, D., Phillipsen, L., Khandabi, P., & Howard, J. (1994). Spontaneous play in two-year-olds born to substance-abusing mothers. Infant Mental Health Journal, 15, 189–201. Bell, M. A. (2002). Power changes in infant EEG frequency bands during a spatial working memory task. Psychophysiology, 39, 1–9. Bendersky, M., Alessandri, S. A., & Lewis, M. (1996). Emotions in cocaine-exposed

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