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EEG during lavender and rosemary exposure in infants of depressed and non-depressed mothers
Infant Behavior & Development 27 (2004) 91–100
EEG during lavender and rosemary exposure in infants of depressed and non-depressed mothers Mercedes Fernandez, Maria Hernandez-Reif∗ , Tiffany Field, Miguel Diego, Chris Sanders, Amparo Roca Department of Pediatrics, Touch Research Institutes, University of Miami School of Medicine, P.O. Box 016820 (D-820), Miami, FL 33101, USA Received 11 November 2002; received in revised form 26 June 2003; accepted 1 July 2003
Abstract This study investigated whether exposure to lavender or rosemary would change electroencephalographic (EEG) activity and behavior in infants of depressed and non-depressed mothers. Twenty newborns were exposed to a 10% (v/v) concentration of rosemary oil or lavender oil. Their EEG and behavior (via a video camera) were simultaneously recorded for 2-min each at baseline and during odor exposure. Group inclusion (depressed versus non-depressed) was based on mothers’ CES-D scores. Although the groups did not differ at baseline and the two odors did not differentially affect the EEG, the infants of depressed mothers showed increased relative left frontal EEG asymmetry from baseline to the odor exposure phase. Infants of non-depressed mothers showed no change in frontal EEG asymmetry from baseline to the odor exposure phase. At least in adults, greater relative left frontal EEG asymmetry has been associated with an approaching pattern of behavior and response to positive stimuli, while greater relative right frontal EEG asymmetry has been associated with a withdrawing pattern of behavior and response to negative stimuli. Among the behaviors recorded; negative affect, head turns, lip licking, and nose wrinkling, the only differences were that the infants of depressed mothers showed increased head turning during the odor exposure. These results suggest that infants of depressed and non-depressed mothers respond differently to odors. © 2004 Elsevier Inc. All rights reserved. Keywords: EEG; Infants; CES-D; Lavender; Rosemary; Aroma
∗
Corresponding author. E-mail address: [email protected] (M. Hernandez-Reif).
0163-6383/$ – see front matter © 2004 Elsevier Inc. All rights reserved. doi:10.1016/j.infbeh.2003.07.001
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1. Introduction Depressed adults show greater relative right frontal electroencephalographic (EEG) asymmetry than non-depressed adults (Davidson, 1995, 1998; Davidson & Tomarken, 1989; Schaffer, Davidson, & Saron, 1983). Moreover, this EEG pattern persists after depressive symptoms have remitted, suggesting that greater relative right frontal EEG asymmetry indexes a vulnerability for depression (Henriques & Davidson, 1990; Tomarken, Davidson, Wheeler, & Kinney, 1992). A similar pattern of greater relative right frontal EEG asymmetry has been observed in infants born to depressed mothers (Dawson et al., 1999; Field, Fox, Pickens, & Nawrocki 1995; Jones, Field, Fox, Lundy, & Davalos, 1997a) and has been shown to remain stable over time (Fox, Bell, & Jones, 1992) from 1 to 3 months of age (Jones et al., 1997a) and from 3 months to 3 years of age (Jones, Field, Davalos, & Pickens, 1997b). Frontal EEG asymmetry is also thought to reflect the processing (see Davidson, 1995, 2000) and regulation of emotion (Fox, 1991). For example, shifts towards greater relative right frontal EEG asymmetry have been observed in infants exhibiting negative affect (Fox & Davidson, 1988) and in response to negative emotion evoking situations such as maternal separation (Davidson & Fox, 1989) and when viewing negative facial expressions (Davidson & Fox, 1989; Field, Pickens, Fox, Gonzalez & Nawrocki, 1998). Similarly, shifts towards greater relative left frontal EEG asymmetry have been observed in infants exhibiting positive affect (Fox & Davidson, 1988) and in response to positive emotion evoking situations such as playful interactions (Dawson et al., 1999) and when viewing positive facial expressions (Davidson & Fox, 1989; Field et al., 1998). The studies discussed above measured EEG asymmetry at rest or employed positive or negative affect-eliciting stimuli or situations, such as play or maternal separation. No studies were found in our literature review that investigated frontal EEG asymmetry responses to olfactory stimuli in newborns. However, a number of studies indicate that odors can elicit behavioral and physiological responses in infants. For example, shortly after birth, neonates show a preference for their mothers’ scent (Cernoch & Porter, 1985; Mennella & Beauchamp, 1993; Shaal, 1986) and when exposed to their mother’s odor, they exhibit less head and arm movements and suck more (Shaal, 1986). Shortly after birth newborns prefer and show positive affect when exposed to pleasant smells like banana and vanilla odors and show frowning when exposed to unpleasant smells including rotten eggs and fish (Steiner, 1977). Similarly both Japanese Macaque infants (Kawakami, Tomonaga, & Suzuki, 2002) and human infants (Kawakami et al., 1997) exposed to lavender exhibit lower saliva cortisol levels after a heel lance than controls who received no odor, suggesting that lavender has calming effects on infants. In a study on adults, exposure to lavender and rosemary altered EEG patterns in a positive direction and improved mood (Diego et al., 1998). If aromas like lavender and rosemary are perceived by young infants as positive stimuli, then this might be reflected in their EEG pattern as has been shown for other sensory stimuli and their facial expressions as has been shown for other pleasant odors. The purpose of the present study was to investigate infant affective and frontal EEG responses to rosemary and lavender aromas. Based on adult findings, we expected that exposure to both lavender and rosemary aromas would cause a shift towards greater relative left frontal EEG asymmetry in both newborns of depressed and non-depressed mothers. Both groups of infants were also expected to exhibit greater positive affect in response to the aromas.
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Table 1 Means on background variables (and standard deviations in parentheses) for the depressed and non-depressed groups Variables
Infant variables Gestational age (weeks) Birthweight (g) Age at study (days) Gender Male Female
Groups
t-test
Depressed (n = 7)
Non-depressed (n = 13)
37 (1.2) 3120 (380) 18 (6)
39 (1.5) 3464 (516) 21 (9)
4 3
7 6
χ2 -test
<0.01 N.S. N.S. N.S. N.S.
2. Methods 2.1. Participants Forty-five mothers without prenatal or postnatal complications who had infants with Apgar scores ≥7 at 1 and 5 min were recruited for this study from an ongoing longitudinal study on the effects of maternal depression on infants. Infants were randomly assigned to receive either a lavender (n = 23) or a rosemary (n = 22) aroma. Of the 45 infants who participated in this study, the data for 19 subjects were excluded from further analyses due to excessive movement. Two subjects whose extreme scores were greater than 3 S.D. from the mean were also excluded from further analysis. Group inclusion was based on mothers’ scores on the Center for Epidemiological Studies Depression Scale (CES-D) (Radloff, 1977), with the depressed group (n = 7) scoring ≥ 16 on the CES-D and the non-depressed group (n = 11) scoring ≤ 12. Data for six babies whose mothers’ CES-D scores fell in the borderline range (13–15) were not included in the depression group comparisons. A greater proportion of infants exposed to lavender (66% lavender versus 38% rosemary), but a comparable proportion of infants of depressed and non-depressed mothers (66% versus 50%), were excluded from the study. Mothers were on average 26 years old (S.D. = 4.54) came from predominantly lower SES families (M = 4 on the Hollingshead, 1975), and were ethnically distributed 50% Hispanic, 25% AfricanAmerican, 20% Haitian, and 5% Asian. Infants were on average 19 days old (S.D. = 8.1) and were 55% male. The depressed and non-depressed groups differed on gestational age, with the non-depressed group being born 2-weeks later (M = 39 weeks, S.D. = 1.5) than the depressed group (M = 37 weeks, S.D. = 1.2), t(15) = 3.26, P < 0.01. The groups did not differ on any of the other demographic variables (see Table 1). None of the depressed mothers were receiving treatment or medication for their depression, and none were assessed for co-morbidity such as anxiety disorders. The mothers were compensated for their travel expenses. 2.2. Procedure and design Upon arrival at the EEG laboratory, mothers read and signed a consent form approved by the university’s human subjects committee. The newborns were fed and changed prior to testing. Subsequently, the infants were reclined in an infant seat and EEG and EOG electrodes were attached. The EEG and video recording
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began when the newborn was quiet and alert and were recorded continuously during a 2-min baseline phase, followed by a 2-min odor-exposure phase. 2.3. Stimulus The essential oils of rosemary and lavender (donated by Aromatherapy Associates, Miami, FL) were diluted in odorless grapeseed oil to form a 10% (v/v) solution. Three drops of the solution were poured on a sterile dental swab and placed in a pierced metal container that measured approximately 6 cm wide×6 cm long. The odor emanated for 2 min from the metal container, which was manually suspended at the beginning of the odor trial approximately 15 cm above the infant’s head and out of view from the infant. To contain the aroma, the metal container was stored in a sealed jar before and after the exposure phase. 2.4. Measures 2.4.1. Depression scale Depression was assessed with the CES-D, a 20-item self-report scale that assesses depressive symptoms over the past week, including today. Respondents rate the frequency of symptoms on a Likert scale from 0 (rarely, <1 day) to 1 (sometimes, 1–2 days) to 2 (often, 3–4 days) to 3 (most of the time, 5 or more days). Characteristic items include “I felt sad”, “I could not shake the blues even with the help of family and friends”, “I had crying spells” and “I felt hopeful about the future”. CES-D scores range from 0 to 60. A score of 16 or greater differentiates clinically depressed and non-depressed participants with only a 6% false positive and a 36% false negative rate (Myers & Weissman, 1980). A score under 12 indicates no depressive symptoms. The CES-D scale has been highly correlated with structured depression interviews, such as the Diagnostic Interview Schedule (DIS) (Weissman, Prusoff, & Newberry, 1975; Wilcox, Field, Promodromis, & Scafidi, 1998) and the Beck Depression Inventory (BDI) (Wilcox et al., 1998). The CES-D has also been validated with diverse demographic groups (Radloff, 1977) and correlated with frontal EEG asymmetry (Diego, Field, & Hernandez-Reif, 2001). 2.4.2. Facial expressions (video) Infants’ facial expressions were videotaped using a Panasonic S-VHS color video camera (Model AG 455) that was placed in front of the infant, but shielded by a black curtain that allowed only the camera lens to protrude for recording. The video was later coded for negative affect, head turns, lip licking, and nose wrinkling as these measures have been coded by researchers who study infant smell perception (Mennella & Beauchamp, 1993). Negative affect was defined as a furrowed brow and down-turned mouth as described in the Affex (Izard, Dougherty, & Hembree, 1980) infant facial coding system. Head turns were defined as a 45◦ shift. Lip licking was defined as a visible protrusion of tongue to lips. Nose wrinkling was defined using the Affex coding features for disgust, such as brows sharply lowered and drawn together, vertical wrinkles or bulge between brows, and upper lip raised but without the down-turned mouth as coded in negative affect. Behaviors were coded as they occurred during sequential 10-s blocks of time. The total number of time sample units that a behavior occurred was divided by the total number of time sample units (12 10-s units for 2 min of baseline and 12 for odor exposure) to yield percentage time that behavior occurred. The percentage time for baseline was subtracted from the “during odor” percentage to yield difference scores for each behavior. Interobserver reliability was assessed on 30% of the videotaped interactions (κ = 0.84).
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2.4.3. EEG Prior to videotape recording, 9-mm gold-cup electrodes were placed on the infants’ scalp at two mid-frontal sites (F3 and F4) and referenced to the vertex (Cz). This reference site has been shown to produce comparable EEG asymmetry results to other sites (Tomarken et al., 1992) and it is less bothersome for infants. These sites were identified with a soft measuring tape using the International 10–20 system. Prior to the electrode attachment, the area of the scalp where electrodes were to be placed was wiped with alcohol. Omni-prep, a skin prepping cream, was used to gently abrade the skin, and Ten20 EEG paste (D.O. Weaver & Co., Aurora, CO) was used as the conductive medium. The impedance (i.e. the resistance to both constant and changing electrical current flow) between the reference electrode (Cz) and each of the other two electrodes (F3 and F4) did not exceed 10 k and most were under 5 k . After the electrodes were attached, a gauze band was wrapped around the infant’s head to secure the electrodes. EOG was also obtained from the outer canthus and the supra-orbit position of the right eye using Beckman mini-electrodes. The EEG signal was recorded using a Grass Model 12 Neurodata Acquisition System with a bandpass filter set to 0.1 and 100 Hz. The output was directed to a computer equipped with an A/D converter (RT1-815). Data were sampled at 512 Hz, and were saved to a hard disk using data acquisition software (Snapstream, HEM Data Corp.). The EEG data were then visually displayed and manually scored for eye and motor movement artifact using the EOG channels as cues, and the data containing artifact were underscored and eliminated from each channel. The percent of artifact free data did not differ for infants of depressed (41%) and non-depressed (43%) mothers. 2.5. EEG analyses A minimum of 20 1-s windows of artifact-free EEG data per phase (baseline and exposure), were required for the newborn data to be included in the analyses. This criterion was met for 26 of the 45 participants tested. However, for the analyses comparing infants of depressed and non-depressed mothers, we only report data for the 20 subjects whose mothers could be classified as depressed or not depressed. The data for the 26 subjects were reanalyzed based on baseline EEG asymmetry and are reported in another paper (Sanders et al., 2002). The artifact-free data were Fast Fourier Transformed (FFT), which yields a power spectrum, in microvolts squared, at each electrode site. Spectral plots revealed that the majority of activity fell below the 10 Hz band. Power within the 6–9 Hz frequency band was used to compute frontal EEG asymmetry scores, consistent with previous studies examining frontal EEG asymmetry responses in infants of depressed mothers (Dawson, Klinger, Panagiotides, Hill, & Spieker, 1992; Dawson et al., 1999; Field, Pickens, Fox, Gonzales, et al., 1998). Asymmetry scores were then computed using natural log scores. The asymmetry score is a difference score reflecting power in one hemisphere relative to power in the homologous site in the contralateral hemisphere [ln(Right) − ln(left)] with negative scores reflecting greater relative right frontal EEG asymmetry and positive scores reflecting greater relative left frontal EEG asymmetry. Two outlier scores (>3 S.D.) from the non-depressed group were omitted from the analyses.
3. Results The purpose of the present study was to investigate the affective and frontal EEG responses to rosemary and lavender aromas by infants of depressed versus non-depressed mothers. Due to our limited sample
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size and violation of assumptions of normality, a hierarchical approach utilizing non-parametric statistics was employed to analyze the EEG and behavioral data. 3.1. Lavender versus rosemary comparisons Mann–Whitney U tests conducted to compare change scores for infants exposed to the lavender versus rosemary irrespective of depression grouping revealed that there were no differences in either frontal EEG asymmetry responses (U(25) = 66, N.S.), or behavioral responses, including head turning (U(25) = 36.5, N.S.), lip licking (U = 39.0, N.S.), nose wrinkling (U(25) = 46.5, N.S.) and negative affect (U(25) = 60.5, N.S.) for the two different odor groups. 3.2. Depressed–non-depressed comparisons Because the two odors did not have differential effects, we then compared the EEG asymmetry scores and the behavioral data for the depressed and non-depressed groups. Mann–Whitney U tests on the change scores revealed that newborns of depressed mothers were more likely to show a shift towards greater relative left frontal EEG asymmetry from baseline to the exposure phase than newborns of non-depressed mothers (U(18) = 11.0, P < 0.01) (see Fig. 1). The analyses on the behavioral change scores revealed that head turning increased in the depressed group versus the non-depressed group (U(18) = 17.5, P < 0.05) (see Fig. 2) and that the groups did not differ on change scores for lip licking (U(18) = 35.0, N.S.), nose wrinkling (U(18) = 38.5, N.S.) and negative affect (U(18) = 32.0, N.S.).
Fig. 1. Frontal EEG asymmetry [ln(Right) − ln(Left) = 6–9 Hz power] change scores for infants of depressed and non-depressed mothers. Triangles indicate individual subject scores, error bars indicate means and 2 ± S.E. of the mean.
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Fig. 2. Head turning change scores for infants of depressed and non-depressed mothers. Triangles indicate individual subject scores, error bars indicate means and 2 ± S.E. of the mean.
3.3. Relations between frontal EEG asymmetry and behavior Correlations were computed to examine the relationship between frontal EEG asymmetry and behavioral responses to the aromas. These analyses revealed that the shift in frontal EEG asymmetry changes was related to head turning (r = 0.50, P < 0.05) and head turning in turn was related to lip licking (r = 0.42, P < 0.05), suggesting that greater head turning was related to both a shift toward greater relative left frontal EEG asymmetry and greater lip licking. No other significant relations were noted between infant behaviors or between infant behaviors and frontal EEG asymmetry.
4. Discussion The shift toward greater relative left frontal EEG asymmetry by newborns of depressed mothers when exposed to rosemary and lavender aromas is a pattern associated with positive affect and response to positive stimuli. In contrast, newborns of non-depressed mothers did not show a shift in frontal EEG asymmetry. Why these odors only elicited differential EEG patterns for newborns of depressed mothers is not known. Perhaps newborns of depressed mothers have higher sensory thresholds. If the odors were strong and the infants of depressed mothers had a higher olfactory threshold than those of non-depressed mothers, then the odors might not have been aversive to the depressed group but aversive to the non-depressed group. Cocaine-exposed newborns have been noted to have elevated sensory thresholds that, in turn, have been linked to dopamine depletion (Karmel & Gardner, 1996). Interestingly, newborns of depressed
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mothers show lower dopamine levels and more depressive-like symptoms (Lundy et al., 1999). And studies on depressed adults suggest that they have odor identification deficits, possibly because of their higher thresholds (see Harrison & Pearson, 1989). Thus, strong odors may be perceived as pleasant by newborns of depressed mothers who have higher olfactory thresholds than newborns of non-depressed mothers. To test this hypothesis, a future study might examine the effects of rosemary and lavender at different concentrations on the EEG of infants of depressed and non-depressed mothers. Another possible alternative is that newborns of non-depressed mothers may be more hesitant about approaching novel odors. The absence of a shift towards left frontal EEG asymmetry, a pattern associated with behavioral approach, supports this interpretation for the newborns of non-depressed mothers. These newborns may be more precocious and less approaching of novel stimuli. Future studies might examine EEG responses of newborns of depressed and non-depressed mothers when presented with familiar versus novel olfactory stimuli to see if this pattern persists. Less negative affect during odor exposure might be expected in the newborns of depressed mothers because of their EEG shift toward greater relative left frontal asymmetry. However, the only significant behavioral finding was that the newborns of depressed mothers had greater head turning during the odor exposure. Olko and Turkewitz (2001) noted that pleasant odors (as determined by adults), but not unpleasant odors, elicited head turns toward the scent when inhaled through the left nostril. The olfactory bulbs connect ipsilaterally with the frontal lobes, so that the pleasant odor seemed to have an effect on the left frontal lobe but not the right. The authors’ conclusions were that approach behaviors (related to greater relative left frontal EEG asymmetry) might develop earlier than withdrawal behaviors. Although the authors’ conclusions were related to emotional development, these findings suggest a relationship between head turning and left frontal EEG asymmetry and are consistent with the significant relationship found between head turning and frontal EEG asymmetry in the infant study. This might explain why the group with increased relative left frontal EEG asymmetry (the newborns of depressed mothers) showed an increased number of head turns during the odor exposure. Future studies should examine the direction of head turning to test this hypothesis, perhaps by presenting the odor to the infants right or left side to see if the infant turns toward or away from the odor. Surprisingly, infants of depressed mothers did not exhibit the expected baseline pattern of greater relative right frontal EEG asymmetry observed in previous studies. The differences between frontal EEG asymmetry responses for infants of depressed and non-depressed mothers may also be attributed to gestational age differences, as infants of depressed mothers, who have shown greater relative right frontal EEG asymmetry, are also more likely to be born preterm (Field et al., 1998). However, whereas infant age has been related to the development of the spectral properties of the EEG, frontal EEG asymmetry patterns in infants of depressed and non-depressed mothers remain stable across infancy (Jones et al., 1997a, 1997b). In addition, the greater relative left frontal EEG asymmetry pattern exhibited by the infants of depressed mothers might have been attributed to the gender distribution of our sample. Whereas 66% female infants in the depressed group exhibited greater relative right frontal EEG asymmetry, 100% of the male infants of depressed mothers exhibited greater relative left frontal EEG asymmetry. This is consistent with recent findings indicating that depressed and non-depressed males and females exhibit opposite resting frontal EEG asymmetry patterns (Diego, Jones, & Field, 2003; Miller et al., 2002). Due to our small sample size we were unable to take gender into account. Future studies examining frontal EEG asymmetry responses to odors should address this issue by having sample sizes large enough to conduct gender analyses. Taken together, these results suggest that olfactory stimuli differentially affect frontal EEG asymmetry and behavior of newborns born to depressed versus newborns to non-depressed mothers. However, caution
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must be taken when interpreting these results as they are based on a small sample size. The greater proportion of infants excluded from the lavender group may have influenced our results as it is possible that these infants exhibited a differential response to the aroma. Further research is needed to replicate these findings with a larger sample size. Additional regions might be recorded to determine whether these findings are limited to the frontal region. Threshold testing and other odorants and stimuli might also be used to help determine potential underlying mechanisms for these findings.
Acknowledgements We thank the mothers and newborns who participated in this study. This research was supported by an NIMH Research Scientist Award (#MH00331) and an NIMH Research Grant (#MH46586) to Tiffany Field, and by funds from Johnson & Johnson to the Touch Research Institutes.
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EEG during lavender and rosemary exposure in infants of depressed and non-depressed mothers Mercedes Fernandez, Maria Hernandez-Reif∗ , Tiffany Field, Miguel Diego, Chris Sanders, Amparo Roca Department of Pediatrics, Touch Research Institutes, University of Miami School of Medicine, P.O. Box 016820 (D-820), Miami, FL 33101, USA Received 11 November 2002; received in revised form 26 June 2003; accepted 1 July 2003
Abstract This study investigated whether exposure to lavender or rosemary would change electroencephalographic (EEG) activity and behavior in infants of depressed and non-depressed mothers. Twenty newborns were exposed to a 10% (v/v) concentration of rosemary oil or lavender oil. Their EEG and behavior (via a video camera) were simultaneously recorded for 2-min each at baseline and during odor exposure. Group inclusion (depressed versus non-depressed) was based on mothers’ CES-D scores. Although the groups did not differ at baseline and the two odors did not differentially affect the EEG, the infants of depressed mothers showed increased relative left frontal EEG asymmetry from baseline to the odor exposure phase. Infants of non-depressed mothers showed no change in frontal EEG asymmetry from baseline to the odor exposure phase. At least in adults, greater relative left frontal EEG asymmetry has been associated with an approaching pattern of behavior and response to positive stimuli, while greater relative right frontal EEG asymmetry has been associated with a withdrawing pattern of behavior and response to negative stimuli. Among the behaviors recorded; negative affect, head turns, lip licking, and nose wrinkling, the only differences were that the infants of depressed mothers showed increased head turning during the odor exposure. These results suggest that infants of depressed and non-depressed mothers respond differently to odors. © 2004 Elsevier Inc. All rights reserved. Keywords: EEG; Infants; CES-D; Lavender; Rosemary; Aroma
∗
Corresponding author. E-mail address: [email protected] (M. Hernandez-Reif).
0163-6383/$ – see front matter © 2004 Elsevier Inc. All rights reserved. doi:10.1016/j.infbeh.2003.07.001
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1. Introduction Depressed adults show greater relative right frontal electroencephalographic (EEG) asymmetry than non-depressed adults (Davidson, 1995, 1998; Davidson & Tomarken, 1989; Schaffer, Davidson, & Saron, 1983). Moreover, this EEG pattern persists after depressive symptoms have remitted, suggesting that greater relative right frontal EEG asymmetry indexes a vulnerability for depression (Henriques & Davidson, 1990; Tomarken, Davidson, Wheeler, & Kinney, 1992). A similar pattern of greater relative right frontal EEG asymmetry has been observed in infants born to depressed mothers (Dawson et al., 1999; Field, Fox, Pickens, & Nawrocki 1995; Jones, Field, Fox, Lundy, & Davalos, 1997a) and has been shown to remain stable over time (Fox, Bell, & Jones, 1992) from 1 to 3 months of age (Jones et al., 1997a) and from 3 months to 3 years of age (Jones, Field, Davalos, & Pickens, 1997b). Frontal EEG asymmetry is also thought to reflect the processing (see Davidson, 1995, 2000) and regulation of emotion (Fox, 1991). For example, shifts towards greater relative right frontal EEG asymmetry have been observed in infants exhibiting negative affect (Fox & Davidson, 1988) and in response to negative emotion evoking situations such as maternal separation (Davidson & Fox, 1989) and when viewing negative facial expressions (Davidson & Fox, 1989; Field, Pickens, Fox, Gonzalez & Nawrocki, 1998). Similarly, shifts towards greater relative left frontal EEG asymmetry have been observed in infants exhibiting positive affect (Fox & Davidson, 1988) and in response to positive emotion evoking situations such as playful interactions (Dawson et al., 1999) and when viewing positive facial expressions (Davidson & Fox, 1989; Field et al., 1998). The studies discussed above measured EEG asymmetry at rest or employed positive or negative affect-eliciting stimuli or situations, such as play or maternal separation. No studies were found in our literature review that investigated frontal EEG asymmetry responses to olfactory stimuli in newborns. However, a number of studies indicate that odors can elicit behavioral and physiological responses in infants. For example, shortly after birth, neonates show a preference for their mothers’ scent (Cernoch & Porter, 1985; Mennella & Beauchamp, 1993; Shaal, 1986) and when exposed to their mother’s odor, they exhibit less head and arm movements and suck more (Shaal, 1986). Shortly after birth newborns prefer and show positive affect when exposed to pleasant smells like banana and vanilla odors and show frowning when exposed to unpleasant smells including rotten eggs and fish (Steiner, 1977). Similarly both Japanese Macaque infants (Kawakami, Tomonaga, & Suzuki, 2002) and human infants (Kawakami et al., 1997) exposed to lavender exhibit lower saliva cortisol levels after a heel lance than controls who received no odor, suggesting that lavender has calming effects on infants. In a study on adults, exposure to lavender and rosemary altered EEG patterns in a positive direction and improved mood (Diego et al., 1998). If aromas like lavender and rosemary are perceived by young infants as positive stimuli, then this might be reflected in their EEG pattern as has been shown for other sensory stimuli and their facial expressions as has been shown for other pleasant odors. The purpose of the present study was to investigate infant affective and frontal EEG responses to rosemary and lavender aromas. Based on adult findings, we expected that exposure to both lavender and rosemary aromas would cause a shift towards greater relative left frontal EEG asymmetry in both newborns of depressed and non-depressed mothers. Both groups of infants were also expected to exhibit greater positive affect in response to the aromas.
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Table 1 Means on background variables (and standard deviations in parentheses) for the depressed and non-depressed groups Variables
Infant variables Gestational age (weeks) Birthweight (g) Age at study (days) Gender Male Female
Groups
t-test
Depressed (n = 7)
Non-depressed (n = 13)
37 (1.2) 3120 (380) 18 (6)
39 (1.5) 3464 (516) 21 (9)
4 3
7 6
χ2 -test
<0.01 N.S. N.S. N.S. N.S.
2. Methods 2.1. Participants Forty-five mothers without prenatal or postnatal complications who had infants with Apgar scores ≥7 at 1 and 5 min were recruited for this study from an ongoing longitudinal study on the effects of maternal depression on infants. Infants were randomly assigned to receive either a lavender (n = 23) or a rosemary (n = 22) aroma. Of the 45 infants who participated in this study, the data for 19 subjects were excluded from further analyses due to excessive movement. Two subjects whose extreme scores were greater than 3 S.D. from the mean were also excluded from further analysis. Group inclusion was based on mothers’ scores on the Center for Epidemiological Studies Depression Scale (CES-D) (Radloff, 1977), with the depressed group (n = 7) scoring ≥ 16 on the CES-D and the non-depressed group (n = 11) scoring ≤ 12. Data for six babies whose mothers’ CES-D scores fell in the borderline range (13–15) were not included in the depression group comparisons. A greater proportion of infants exposed to lavender (66% lavender versus 38% rosemary), but a comparable proportion of infants of depressed and non-depressed mothers (66% versus 50%), were excluded from the study. Mothers were on average 26 years old (S.D. = 4.54) came from predominantly lower SES families (M = 4 on the Hollingshead, 1975), and were ethnically distributed 50% Hispanic, 25% AfricanAmerican, 20% Haitian, and 5% Asian. Infants were on average 19 days old (S.D. = 8.1) and were 55% male. The depressed and non-depressed groups differed on gestational age, with the non-depressed group being born 2-weeks later (M = 39 weeks, S.D. = 1.5) than the depressed group (M = 37 weeks, S.D. = 1.2), t(15) = 3.26, P < 0.01. The groups did not differ on any of the other demographic variables (see Table 1). None of the depressed mothers were receiving treatment or medication for their depression, and none were assessed for co-morbidity such as anxiety disorders. The mothers were compensated for their travel expenses. 2.2. Procedure and design Upon arrival at the EEG laboratory, mothers read and signed a consent form approved by the university’s human subjects committee. The newborns were fed and changed prior to testing. Subsequently, the infants were reclined in an infant seat and EEG and EOG electrodes were attached. The EEG and video recording
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began when the newborn was quiet and alert and were recorded continuously during a 2-min baseline phase, followed by a 2-min odor-exposure phase. 2.3. Stimulus The essential oils of rosemary and lavender (donated by Aromatherapy Associates, Miami, FL) were diluted in odorless grapeseed oil to form a 10% (v/v) solution. Three drops of the solution were poured on a sterile dental swab and placed in a pierced metal container that measured approximately 6 cm wide×6 cm long. The odor emanated for 2 min from the metal container, which was manually suspended at the beginning of the odor trial approximately 15 cm above the infant’s head and out of view from the infant. To contain the aroma, the metal container was stored in a sealed jar before and after the exposure phase. 2.4. Measures 2.4.1. Depression scale Depression was assessed with the CES-D, a 20-item self-report scale that assesses depressive symptoms over the past week, including today. Respondents rate the frequency of symptoms on a Likert scale from 0 (rarely, <1 day) to 1 (sometimes, 1–2 days) to 2 (often, 3–4 days) to 3 (most of the time, 5 or more days). Characteristic items include “I felt sad”, “I could not shake the blues even with the help of family and friends”, “I had crying spells” and “I felt hopeful about the future”. CES-D scores range from 0 to 60. A score of 16 or greater differentiates clinically depressed and non-depressed participants with only a 6% false positive and a 36% false negative rate (Myers & Weissman, 1980). A score under 12 indicates no depressive symptoms. The CES-D scale has been highly correlated with structured depression interviews, such as the Diagnostic Interview Schedule (DIS) (Weissman, Prusoff, & Newberry, 1975; Wilcox, Field, Promodromis, & Scafidi, 1998) and the Beck Depression Inventory (BDI) (Wilcox et al., 1998). The CES-D has also been validated with diverse demographic groups (Radloff, 1977) and correlated with frontal EEG asymmetry (Diego, Field, & Hernandez-Reif, 2001). 2.4.2. Facial expressions (video) Infants’ facial expressions were videotaped using a Panasonic S-VHS color video camera (Model AG 455) that was placed in front of the infant, but shielded by a black curtain that allowed only the camera lens to protrude for recording. The video was later coded for negative affect, head turns, lip licking, and nose wrinkling as these measures have been coded by researchers who study infant smell perception (Mennella & Beauchamp, 1993). Negative affect was defined as a furrowed brow and down-turned mouth as described in the Affex (Izard, Dougherty, & Hembree, 1980) infant facial coding system. Head turns were defined as a 45◦ shift. Lip licking was defined as a visible protrusion of tongue to lips. Nose wrinkling was defined using the Affex coding features for disgust, such as brows sharply lowered and drawn together, vertical wrinkles or bulge between brows, and upper lip raised but without the down-turned mouth as coded in negative affect. Behaviors were coded as they occurred during sequential 10-s blocks of time. The total number of time sample units that a behavior occurred was divided by the total number of time sample units (12 10-s units for 2 min of baseline and 12 for odor exposure) to yield percentage time that behavior occurred. The percentage time for baseline was subtracted from the “during odor” percentage to yield difference scores for each behavior. Interobserver reliability was assessed on 30% of the videotaped interactions (κ = 0.84).
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2.4.3. EEG Prior to videotape recording, 9-mm gold-cup electrodes were placed on the infants’ scalp at two mid-frontal sites (F3 and F4) and referenced to the vertex (Cz). This reference site has been shown to produce comparable EEG asymmetry results to other sites (Tomarken et al., 1992) and it is less bothersome for infants. These sites were identified with a soft measuring tape using the International 10–20 system. Prior to the electrode attachment, the area of the scalp where electrodes were to be placed was wiped with alcohol. Omni-prep, a skin prepping cream, was used to gently abrade the skin, and Ten20 EEG paste (D.O. Weaver & Co., Aurora, CO) was used as the conductive medium. The impedance (i.e. the resistance to both constant and changing electrical current flow) between the reference electrode (Cz) and each of the other two electrodes (F3 and F4) did not exceed 10 k and most were under 5 k . After the electrodes were attached, a gauze band was wrapped around the infant’s head to secure the electrodes. EOG was also obtained from the outer canthus and the supra-orbit position of the right eye using Beckman mini-electrodes. The EEG signal was recorded using a Grass Model 12 Neurodata Acquisition System with a bandpass filter set to 0.1 and 100 Hz. The output was directed to a computer equipped with an A/D converter (RT1-815). Data were sampled at 512 Hz, and were saved to a hard disk using data acquisition software (Snapstream, HEM Data Corp.). The EEG data were then visually displayed and manually scored for eye and motor movement artifact using the EOG channels as cues, and the data containing artifact were underscored and eliminated from each channel. The percent of artifact free data did not differ for infants of depressed (41%) and non-depressed (43%) mothers. 2.5. EEG analyses A minimum of 20 1-s windows of artifact-free EEG data per phase (baseline and exposure), were required for the newborn data to be included in the analyses. This criterion was met for 26 of the 45 participants tested. However, for the analyses comparing infants of depressed and non-depressed mothers, we only report data for the 20 subjects whose mothers could be classified as depressed or not depressed. The data for the 26 subjects were reanalyzed based on baseline EEG asymmetry and are reported in another paper (Sanders et al., 2002). The artifact-free data were Fast Fourier Transformed (FFT), which yields a power spectrum, in microvolts squared, at each electrode site. Spectral plots revealed that the majority of activity fell below the 10 Hz band. Power within the 6–9 Hz frequency band was used to compute frontal EEG asymmetry scores, consistent with previous studies examining frontal EEG asymmetry responses in infants of depressed mothers (Dawson, Klinger, Panagiotides, Hill, & Spieker, 1992; Dawson et al., 1999; Field, Pickens, Fox, Gonzales, et al., 1998). Asymmetry scores were then computed using natural log scores. The asymmetry score is a difference score reflecting power in one hemisphere relative to power in the homologous site in the contralateral hemisphere [ln(Right) − ln(left)] with negative scores reflecting greater relative right frontal EEG asymmetry and positive scores reflecting greater relative left frontal EEG asymmetry. Two outlier scores (>3 S.D.) from the non-depressed group were omitted from the analyses.
3. Results The purpose of the present study was to investigate the affective and frontal EEG responses to rosemary and lavender aromas by infants of depressed versus non-depressed mothers. Due to our limited sample
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size and violation of assumptions of normality, a hierarchical approach utilizing non-parametric statistics was employed to analyze the EEG and behavioral data. 3.1. Lavender versus rosemary comparisons Mann–Whitney U tests conducted to compare change scores for infants exposed to the lavender versus rosemary irrespective of depression grouping revealed that there were no differences in either frontal EEG asymmetry responses (U(25) = 66, N.S.), or behavioral responses, including head turning (U(25) = 36.5, N.S.), lip licking (U = 39.0, N.S.), nose wrinkling (U(25) = 46.5, N.S.) and negative affect (U(25) = 60.5, N.S.) for the two different odor groups. 3.2. Depressed–non-depressed comparisons Because the two odors did not have differential effects, we then compared the EEG asymmetry scores and the behavioral data for the depressed and non-depressed groups. Mann–Whitney U tests on the change scores revealed that newborns of depressed mothers were more likely to show a shift towards greater relative left frontal EEG asymmetry from baseline to the exposure phase than newborns of non-depressed mothers (U(18) = 11.0, P < 0.01) (see Fig. 1). The analyses on the behavioral change scores revealed that head turning increased in the depressed group versus the non-depressed group (U(18) = 17.5, P < 0.05) (see Fig. 2) and that the groups did not differ on change scores for lip licking (U(18) = 35.0, N.S.), nose wrinkling (U(18) = 38.5, N.S.) and negative affect (U(18) = 32.0, N.S.).
Fig. 1. Frontal EEG asymmetry [ln(Right) − ln(Left) = 6–9 Hz power] change scores for infants of depressed and non-depressed mothers. Triangles indicate individual subject scores, error bars indicate means and 2 ± S.E. of the mean.
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Fig. 2. Head turning change scores for infants of depressed and non-depressed mothers. Triangles indicate individual subject scores, error bars indicate means and 2 ± S.E. of the mean.
3.3. Relations between frontal EEG asymmetry and behavior Correlations were computed to examine the relationship between frontal EEG asymmetry and behavioral responses to the aromas. These analyses revealed that the shift in frontal EEG asymmetry changes was related to head turning (r = 0.50, P < 0.05) and head turning in turn was related to lip licking (r = 0.42, P < 0.05), suggesting that greater head turning was related to both a shift toward greater relative left frontal EEG asymmetry and greater lip licking. No other significant relations were noted between infant behaviors or between infant behaviors and frontal EEG asymmetry.
4. Discussion The shift toward greater relative left frontal EEG asymmetry by newborns of depressed mothers when exposed to rosemary and lavender aromas is a pattern associated with positive affect and response to positive stimuli. In contrast, newborns of non-depressed mothers did not show a shift in frontal EEG asymmetry. Why these odors only elicited differential EEG patterns for newborns of depressed mothers is not known. Perhaps newborns of depressed mothers have higher sensory thresholds. If the odors were strong and the infants of depressed mothers had a higher olfactory threshold than those of non-depressed mothers, then the odors might not have been aversive to the depressed group but aversive to the non-depressed group. Cocaine-exposed newborns have been noted to have elevated sensory thresholds that, in turn, have been linked to dopamine depletion (Karmel & Gardner, 1996). Interestingly, newborns of depressed
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mothers show lower dopamine levels and more depressive-like symptoms (Lundy et al., 1999). And studies on depressed adults suggest that they have odor identification deficits, possibly because of their higher thresholds (see Harrison & Pearson, 1989). Thus, strong odors may be perceived as pleasant by newborns of depressed mothers who have higher olfactory thresholds than newborns of non-depressed mothers. To test this hypothesis, a future study might examine the effects of rosemary and lavender at different concentrations on the EEG of infants of depressed and non-depressed mothers. Another possible alternative is that newborns of non-depressed mothers may be more hesitant about approaching novel odors. The absence of a shift towards left frontal EEG asymmetry, a pattern associated with behavioral approach, supports this interpretation for the newborns of non-depressed mothers. These newborns may be more precocious and less approaching of novel stimuli. Future studies might examine EEG responses of newborns of depressed and non-depressed mothers when presented with familiar versus novel olfactory stimuli to see if this pattern persists. Less negative affect during odor exposure might be expected in the newborns of depressed mothers because of their EEG shift toward greater relative left frontal asymmetry. However, the only significant behavioral finding was that the newborns of depressed mothers had greater head turning during the odor exposure. Olko and Turkewitz (2001) noted that pleasant odors (as determined by adults), but not unpleasant odors, elicited head turns toward the scent when inhaled through the left nostril. The olfactory bulbs connect ipsilaterally with the frontal lobes, so that the pleasant odor seemed to have an effect on the left frontal lobe but not the right. The authors’ conclusions were that approach behaviors (related to greater relative left frontal EEG asymmetry) might develop earlier than withdrawal behaviors. Although the authors’ conclusions were related to emotional development, these findings suggest a relationship between head turning and left frontal EEG asymmetry and are consistent with the significant relationship found between head turning and frontal EEG asymmetry in the infant study. This might explain why the group with increased relative left frontal EEG asymmetry (the newborns of depressed mothers) showed an increased number of head turns during the odor exposure. Future studies should examine the direction of head turning to test this hypothesis, perhaps by presenting the odor to the infants right or left side to see if the infant turns toward or away from the odor. Surprisingly, infants of depressed mothers did not exhibit the expected baseline pattern of greater relative right frontal EEG asymmetry observed in previous studies. The differences between frontal EEG asymmetry responses for infants of depressed and non-depressed mothers may also be attributed to gestational age differences, as infants of depressed mothers, who have shown greater relative right frontal EEG asymmetry, are also more likely to be born preterm (Field et al., 1998). However, whereas infant age has been related to the development of the spectral properties of the EEG, frontal EEG asymmetry patterns in infants of depressed and non-depressed mothers remain stable across infancy (Jones et al., 1997a, 1997b). In addition, the greater relative left frontal EEG asymmetry pattern exhibited by the infants of depressed mothers might have been attributed to the gender distribution of our sample. Whereas 66% female infants in the depressed group exhibited greater relative right frontal EEG asymmetry, 100% of the male infants of depressed mothers exhibited greater relative left frontal EEG asymmetry. This is consistent with recent findings indicating that depressed and non-depressed males and females exhibit opposite resting frontal EEG asymmetry patterns (Diego, Jones, & Field, 2003; Miller et al., 2002). Due to our small sample size we were unable to take gender into account. Future studies examining frontal EEG asymmetry responses to odors should address this issue by having sample sizes large enough to conduct gender analyses. Taken together, these results suggest that olfactory stimuli differentially affect frontal EEG asymmetry and behavior of newborns born to depressed versus newborns to non-depressed mothers. However, caution
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must be taken when interpreting these results as they are based on a small sample size. The greater proportion of infants excluded from the lavender group may have influenced our results as it is possible that these infants exhibited a differential response to the aroma. Further research is needed to replicate these findings with a larger sample size. Additional regions might be recorded to determine whether these findings are limited to the frontal region. Threshold testing and other odorants and stimuli might also be used to help determine potential underlying mechanisms for these findings.
Acknowledgements We thank the mothers and newborns who participated in this study. This research was supported by an NIMH Research Scientist Award (#MH00331) and an NIMH Research Grant (#MH46586) to Tiffany Field, and by funds from Johnson & Johnson to the Touch Research Institutes.
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