SOCIAL NEUROSCIENCE, 2012, 7 (5), 525–536

Investigating the impact of parental statusand depression symptoms on the early perceptual

coding of infant faces: An event-related potential study

Laura K. Noll1,2, Linda C. Mayes1, and Helena J. V. Rutherford1

1Yale Child Study Center, New Haven, CT, USA2University College London, London, UK

Infant faces are highly salient social stimuli that appear to elicit intuitive parenting behaviors in healthy adultwomen. Behavioral and observational studies indicate that this effect may be modulated by experiences of repro-duction, caregiving, and psychiatric symptomatology that affect normative attention and reward processing ofinfant cues. However, relatively little is known about the neural correlates of these effects. Using the event-relatedpotential (ERP) technique, this study investigated the impact of parental status (mother, non-mother) and depres-sion symptoms on early visual processing of infant faces in a community sample of adult women. Specifically,the P1 and N170 ERP components elicited in response to infant face stimuli were examined. While characteristicsof the N170 were not modulated by parental status, a statistically significant positive correlation was observedbetween depression symptom severity and N170 amplitude. This relationship was not observed for the P1. Theseresults suggest that depression symptoms may modulate early neurophysiological responsiveness to infant cues,even at sub-clinical levels.

Keywords: Infant face; Parenting; Depression; ERP/EEG, N170.

Infant faces are highly salient social stimuli. Notingthat people respond to Kindchenschema or babyschema (i.e., facial features common to newbornsacross mammalian species, such as large eyes androunded cheeks) with positive emotions and increasedattention, Lorenz (1943, 1971) argued that babyschema facilitate parental care and, ultimately, repro-ductive success by way of an evolutionarily con-served innate releasing mechanism. Strong supportfor this hypothesis comes from observational stud-ies of human–infant interaction. For example, in theiraudiovisual microanalysis of parent–infant exchanges,Papousek and Papousek (1975, 1979, 1983) observedthat parents consistently modified their speech, facialexpressions, and other movements in simple and

Correspondence should be addressed to: Helena J. V. Rutherford, Yale Child Study Center, Yale University, 230 South Frontage Road, NewHaven, CT 06520, USA. E-mail: helena.rutherford@yale.edu

The authors would like to acknowledge the contributions of Alice Proverbio, who provided the infant stimuli used in this project, and MaxGreger-Moser for his assistance with collection of EEG data. This work was submitted in partial fulfillment of the requirement of the degree ofMSc in Psychodynamic Developmental Neuroscience by L.K.N., and it was funded by the Anna Freud Centre (UK).

repetitive patterns “as if they were unconditionedresponses to specific eliciting stimuli” (Papousek &Papousek, 1983, p. 121). These intuitive parentingbehaviors were found to operate over temporal inter-vals of 200–800 ms, indicating that they are slowerthan reflexes but faster than conscious responses(Papousek & Papousek, 1987).

The contingency between a parent’s perceptualcoding of infant cues and their intuitive behavior isthought to be crucial for learning, allowing the infantto perceive causal relationships between their commu-nication and parental response (Beeghly, Fuertes, Liu,Delonis, & Tronick, 2011). Likewise, visual feedbackenables caregivers to contingently regulate the amountof stimulation they direct toward the infant according

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526 NOLL, MAYES, RUTHERFORD

to the child’s communicated needs (Beebe et al., 2008,2010). Not surprisingly, then, the temporal dynamicsof parent–infant interactions appear to have long-termconsequences for development, and play a determina-tive role in the development of secure attachment andemotional regulation abilities in the infant (Fonagy,Gergely, Jurist, & Target, 2002).

Emerging functional imaging studies have sug-gested that neurobiological changes occurring as aconsequence of reproduction may facilitate the emer-gence of intuitive parenting in humans. For exam-ple, recent short-term longitudinal work suggests thatthe postpartum period is accompanied by signifi-cant maternal brain changes (i.e., significant increasesin gray matter volume) that are associated withmaternal perception of her baby (Kim et al., 2010).Moreover, parents as compared to non-parents showheightened sensitivity to infant crying than infantlaughter in limbic emotion processing regions of thebrain (Seiftriz et al., 2003). In addition, reproduction-induced changes in neuroendocrine systems, suchas the dopamine-reward processing and oxytociner-gic systems, are thought to help regulate maternalbehaviors that foster mother–infant bonding, such asincreased responsivity to infant distress communica-tions (Strathearn, Fonagy, Amico, & Montague, 2009).

Complementing these neuroimaging studies, theevent-related potential (ERP) technique provides ameans of investigating the functional course of per-ceptual processing (i.e., encoding) at the neural level,with high temporal resolution in the millisecondrange (Luck, 2005). Accordingly, this technique isparticularly well suited to the study of intuitive ornon-conscious aspects of parenting, such as sen-sory processing, which occur within time frames toonarrow to be captured by functional neuroimaging,self-report measures, or behavioral observation alone(Rutherford & Mayes, 2011). While relatively fewstudies have capitalized on the high temporal resolu-tion of the ERP method to investigate the temporalcourse of visual encoding of infant faces, the abun-dance of ERP studies using adult face stimuli providesa methodological foundation upon which such studiesmay be grounded.

In experiments presenting adult face stimuli, alarge negative potential is observed at lateral occipital-temporal electrode sites in the low alpha range(7–8 Hz), peaking between 130 and 200 ms post-stimulus (Bentin, McCarthy, Perez, Puce, & Allison,1996; Rossion et al., 1999). This negative deflectionhas been termed the N170, and is typically largerwhen recorded over the right, relative to the left,hemisphere (Bentin et al., 1996). Relative to non-face stimuli, the N170 peaks later and with larger

amplitude for inverted faces relative to upright faces(Rossion et al., 2000). This inversion effect convergeswith behavioral data indicating that it takes longerto recognize inverted faces than inverted objects inhumans (Yin, 1969), and even in some conspecifics,such as certain primates, an inversion effect is seen(Adachi, Chou, & Hampton, 2009). In keeping withdistributed models of face processing (e.g., Bruce &Young, 1986; Haxby, Hoffman, & Gobbini, 2000),many argue that the N170 may be regarded as a face-specific marker of visual processing that reflects thestructural encoding of facial stimuli preceding higher-order processing (e.g., Eimer 2000a, 2000b; Eimer &Holmes, 2007). However, this remains an area ofongoing investigation and debate, as other studiesindicate modulation of the N170 by variable facial fea-tures such as emotional expression (e.g., Blau, Mauer,Tottenham, & McCandliss, 2007).

Following the seminal work of Purhonen andcolleagues (2001), who first applied the ERP tech-nique to the study of maternal sensitivity to auditorystimuli (infant cry), Proverbio, Brignone, Matarazzo,Del Zotto, and Zani (2006) investigated the impactof parental status (parent, non-parent) and gender(male, female) on the amplitude of visual corti-cal response to infant facial expressions of variedvalence and intensity. In their experiment, participantsviewed infant faces varying in affective expression,categorizing the emotion in the face on a trial-by-trial basis. N170 amplitude was modulated by infantfacial expression, with strongly negative expressions(i.e., distress) eliciting larger negative amplitudes thanweakly negative expressions (i.e., discomfort); no sig-nificant differences were observed between positiveexpressions (i.e., comfort or pleasure). While no dif-ference in N170 amplitude was found between non-parents of both genders, N170 amplitude in moth-ers was significantly larger than N170 amplitude infathers, suggesting that parental status may modulatethe structural encoding of infant faces more stronglyin women than in men. Notably, the amplitude of theP1 (an index of early visual processing in the extrastri-ate cortex) was observed to be larger for women thanmen, irrespective of parental status, suggesting thatgender may moderate the cortical response to infantfaces during early visual processing.

A recent study also explored whether ERPs elicitedin response to infant and child face stimuli weremodulated by face familiarity and the biological relat-edness of the child to the mother (Grasso, Moser,Dozier, & Simons, 2009). Here, birth mothers (n = 14)and foster or adoptive mothers (n = 14) of childrenaged 1.6–4.7 years (M = 2.7 years, SD = .9) viewedphotographs of their own child, a familiar child, a

PERCEPTUAL CODING OF INFANT FACES 527

familiar adult, and an unfamiliar child and adult.Across the stimulus conditions, all mothers showed anincreased positive deflection for their own children’sfaces, beginning at 100–150 ms post-stimulus onset.The authors interpret these findings as evidence thatthere was an increase in attention allocated to pho-tographs containing faces of the mother’s own chil-dren. Notably, consistent with the view that theN170 reflects pre-categorical perceptual coding ofstructural information (see Eimer, 2000a, 2000b;Eimer & Holmes, 2007), the N170 was not modulatedby face familiarity or age (infant or adult face).

Behavioral and observational studies suggest thatdepression symptoms reliably correlate with maternalinsensitivity to infant cues and, therefore, represent arisk factor for parental dysfunction (Davis & Logsdon,2010). While the mechanism by which depressionsymptoms attenuate maternal sensitivity to infant cuesremains largely unknown, Pearson, Cooper, Penton-Voak, Lightman, and Evans (2010a) found that thepresence of depression symptoms during pregnancycorrelated with disrupted attentional processing ofinfant cues. Using a task adapted from Bindermann,Burton, Hooge, Jenkins, and de Haan (2005) thatwas designed to assess the ability of a stimulus toretain attention under conditions of go/no-go taskdemands, the authors demonstrated that healthy con-trols took longer to disengage from images of dis-tressed (versus non-distressed) infant faces and com-plete the go/no-go task. By contrast, no attentionalbias was seen in women who endorsed at least oneof the “entry criteria” for depressive symptoms on theClinical Interview Schedule (Lewis, Pelosi, Araya, &Dunn, 1992), a self-administered computerized clin-ical interview. Importantly, this disruption predictedthe quality of mother-infant attachment after birth(Pearson, Lightman, & Evans, 2010b). Although byno means conclusive, these results suggest that depres-sion may attenuate the inherent salience of infant facesthat under normal circumstances facilitates caretak-ing responses (via increased attention allocation) whenexposed to distressed infant stimuli. As these studiesdid not include depressed non-mothers, it is unclearwhether or not parental status modulates the relation-ship between depression symptoms and an attenuationof salience for infant visual cues.

Despite its utility for the study of sensory pro-cessing, no ERP studies to date have investigated therelationship between maternal depression symptoma-tology and perceptual encoding by measuring earlyvisual processing of infant face stimuli. However,Rodrigo and colleagues (2011) recently demon-strated the relevance of this approach to researchon maternal insensitivity in a study that investigated

the neural correlates of infant face perception dur-ing an emotion-recognition task in mothers withsubstantiated neglect of a child under 5 years old(n = 14). Whereas the control group of non-neglectingmothers (n = 14) exhibited increased N170 amplitudein response to viewing crying (versus laughing andneutral) infant facial expressions, neglecting mothersdid not show a significant difference in N170 ampli-tude across conditions. This finding suggests thatattenuated N170 amplitude may index reduced mater-nal sensitivity to infant facial expressions of distress.

STUDY AIMS

The aims of this study are two fold: first, to repli-cate existing research on the impact of parental status(mother, non-mother) on the early visual processingof emotional infant faces; and, second, to offer a newexploration of the relationship between early visualprocessing of infant faces and individual differencesin depression symptoms, which may attenuate thesalience of infant stimuli. We included both ampli-tude and latency measures of the N170 to understandwhether infant affect and depression symptoms modu-lated the intensity and efficiency of infant face process-ing. We also examined the amplitude and latency of theP1, as a general marker of visual processing, to ascer-tain whether any modulation of the N170 would reflectmore general modulation in the temporal dynamics ofearly visual processing of infant faces. Given evidencesupporting the notion that biological changes associ-ated with reproduction facilitate the emergence of sen-sitive maternal behavior, we hypothesized that motherswould exhibit larger N170 amplitudes when viewinginfant faces than non-mothers. By contrast, an inverserelationship was expected between depression symp-tom severity and N170 amplitude, with greater depres-sion scores predicting an attenuated neural responseto infant faces. Due to contradictions in the literature,no predictions were made about the impact of infantemotional expressions on attributes of the N170.

METHODS

Participants

Prior to recruitment, the Human InvestigationsCommittee at Yale School of Medicine approvedall procedures. Thirty right-handed adult women(17 mothers, 13 non-mothers) aged 21–45 years(M = 31.53 years, SD = 6.84) were recruited from theNew Haven community. All mothers had at least one

528 NOLL, MAYES, RUTHERFORD

TABLE 1Participant demographics

Mother (n = 17) Non-Mother (n = 13) All (N = 30)

Mean SD Range Mean SD Range Mean SD Range

Age (years) 34.76 5.96 23–45 27.31 5.60 21–37 31.53 6.84 21–45BDI-II Score 6.00 4.56 0–17 3.46 3.53 0–9 4.90 4.27 0–17

Ethnicity n % n % n %C 12 70% 7 53% 19 63%AA/B 1 6% 1 8% 2 7%AA/A 2 12% 1 8% 3 10%O 2 12% 1 8% 3 10%DNR 0 0% 3 23% 3 10%

Note: C = Caucasian, AA/B = African American/Black, AA/A African American/Asian, O = Other, DNR = Did not report.

child under 5 years of age and non-mothers had nochildren or stepchildren, young nieces, nephews orcousins; the age of the mothers’ youngest child var-ied from 1.5 to 48 months (M = 21.64, SD = 16.14).Participants received a neuropsychological and neu-rological screening form, and were excluded fromparticipation if they endorsed items indicating any cur-rent or historical trauma, disease, or medication knownto influence brain activity, including but not limited toa lifetime history of substance use or any substanceuse during pregnancy. Participant demographics aredisplayed in Table 1.

Mothers and non-mothers differed significantly byage, with mothers (M = 34.76 years, SD = 5.96) beingolder than non-mothers (M = 27.31 years, SD =5.60), t(28) = 3.48, p < .01. Mothers and non-mothersdid not statistically differ by ethnicity, Cramer’sV(27) = .08, p = .98.

Apparatus and stimuli

A 128 Ag/AgCl electrode sensor net (ElectricalGeodesics, Inc; Tucker, 1993) was placed on the par-ticipant’s head and fitted according to manufacturerspecifications. All electrodes were spaced evenly andsymmetrically to cover the scalp from nasion to inionand from left to right ear. Impedances were kept below40 k�. Continuous EEG was recorded, using NetStation 4.2.1, with a sampling rate of 250 Hz and highimpedance amplifiers (0.1 Hz high-pass, 100 Hz low-pass). Electrodes were referenced to Cz during EEGrecording.

Infant face stimuli were drawn from Proverbioet al. (2006) and were presented to participants ona Pentium-IV computer controlling a 51-cm colormonitor (75 Hz, 1024 × 768 resolution) runningE-Prime 1.2 software (Schneider, Eschman, &

Zuccolotto, 2002). Images were viewed at a distanceof 91.4 cm in a sound-attenuated room, with lowambient illumination. Infant face stimuli consistedof 75 high-resolution, grayscale digital images sized18.3 cm (2.16◦) wide and 11.5 cm (1.81◦) tall ofunique Caucasian infant faces, each expressing oneof three emotions: pleasure, comfort, or distress(25 exemplars for each expression). Representativeexamples of these images are shown in Figure 1 (panelA). Each face was clearly in the foreground of itsimage, rotated no more than 45◦ from a frontal orinclined position. Approximately 90% of the infantsfaces were judged to be 15 months or younger and allimages were standardized for facial expression by apanel of experts (see Proverbio et al., 2006). Visualoffset of the stimuli was 19 ms.

Measures

The Beck Depression Inventory, Second Edition (BDI-II) (Beck, Steer, & Garbin, 1996) is a 21-item, self-report measure designed to assess the severity ofdepression symptoms, as described in the AmericanPsychiatric Association’s Diagnostic and statisticalmanual of mental disorders, 4th edition (DSM-IV)(APA, 1994). Each item on the BDI-II is scored ona four-point scale ranging from 0 to 3, with zeroindicating a complete absence of the symptom andthree representing its maximum presence; all itemsare summed to yield a total score. Respondents areinstructed to circle the answer that best describes theirexperience of the preceding two weeks. A total scoreof 0–13 is considered minimal depression, 14–19 mild,20–28 moderate, and 29–63 severe.

The psychometric properties of the BDI-II are wellestablished (Weiner & Craighead, 2010). Excellenttest-retest reliability (reliability co-efficient = .93) is

PERCEPTUAL CODING OF INFANT FACES 529

Figure 1. Panel A. Representative examples of infant face stimuli from each of three conditions: comfort, distress, and pleasure. Reprintedfrom Proverbio et al. (2006). Gender and parental status affect the visual cortical response to infant facial expression. Neuropsychologia, 44,2987–2999, with permission from Elsevier. Panel B. Sensor layout for the Geodesic Hydrocel GSN 128 1.0 (Electrical Geodesics, Inc.) (Tucker,1993). Electrodes used in the analysis of P1 and N170 ERP components are highlighted in green in the boxed regions.

reported in the BDI-II test manual (Beck et al., 1996).Likewise, independent groups report that the BDI-IIhas high internal consistency (α = .91), which is com-parable to the original version of the metric (α = .93)(e.g., Dozois, Dobson, & Ahnberg, 1998). Convergentvalidity for the BDI-II is indicated by its significantcorrelation with other measures of depression symp-toms, such as the Revised Hamilton Psychiatric RatingScale for Depression (r = .71) (Riskind, Beck, Brown,& Steer, 1987). The BDI-II also shows a low correla-tion with demographic variables such as age, sex, andethnicity (Segal, Coolidge, Cahill, & O’Riley, 2008),indicating adequate divergent validity. Two main fac-tors consistently emerge in factor analyses of the BDI-II (e.g., Beck et al., 1996; Storch, Roberti, & Roth,2004; Whisman, Perez, & Ramel, 2000). These are thecognitive-affective factor (items 1–14, 20, 21) and thesomatic factor (items 15–19).

Procedure

EEG was recorded continuously throughout each trial.At the beginning of a trial, a central fixation cross waspresented for 2000 ms followed by a 500 ms blankscreen. A randomly selected infant face was then pre-sented for 1500 ms followed by another blank screen,which varied in duration between 500 and 700 ms.There were 75 trials in total and the procedure tookapproximately 10 minutes to complete.

Data analysis

EEG data was pre-processed and prepared for statisti-cal analysis using NetStation 4.2.1. Prior to segmen-tation, each file was digitally filtered with a 30 Hzlow-pass filter to reduce environmental noise artifacts.EEG signal was segmented into epochs of 1 s, begin-ning 100 ms before and ending 900 ms after stimulusonset. The data were transformed to correct for base-line shifts. NetStation artifact detection was set to 200μV for bad channels, 150 μV for eye blinks, and150 μV for eye movements. Channels with artifacts inmore than 50% of trials were marked as bad channelsand replaced through spline interpolation. Segmentsthat contained eye blinks or eye movement and thosewith more than 10 bad channels were marked as badand excluded from the analysis. At completion of pre-processing, all participants had at least 60% of trials(M = 88%, SD = 11%, equating to an average of21.96 trials per condition). Following artifact detec-tion procedures, data were re-referenced to the averagereference of all electrodes.

Electrodes of interest were selected by maxi-mal observed N170 amplitude to the infant faces.These conformed to those used in previous research(McPartland, Dawson, Webb, Panagiotides, & Carver,2004) and the scalp regions characteristically elicitingthe N170 (Bentin et al., 1996). ERP data were averagedacross six electrodes over the left lateral posterior scalp(58, 59, 64, 65, 68, and 69) and six electrodes over the

530 NOLL, MAYES, RUTHERFORD

right lateral posterior scalp (89, 90, 91, 94, 95, and 96).The position of these electrodes is shown in Figure 1(panel B).

The time windows for analysis of the P1 andN170 components were chosen by visual inspectionof the grand averaged data. The resultant time win-dows for the P1 (27–195 ms post-stimulus onset) andN170 (99–235 ms post-stimulus onset) were examinedfor each participant’s average to confirm that the com-ponents of interest were captured at each electrodefor each subject. Peak amplitude and latency to peakmeasures were averaged across each electrode groupwithin the specified time window and were statisticallyextracted for each participant. One non-mother wasexcluded from the analysis of amplitude and anothernon-mother from the analysis of latency, because theirvalues were more than 2 SDs from the mean for allparticipants.

P1 and N170 amplitudes and latencies for each par-ticipant were analyzed separately with a 3 × 2 repeatedmeasures ANOVA, with infant facial expression (plea-sure, comfort, distress) and hemisphere (right, left) asthe within-subject factors and parental status (mother,non-mother) as the between-subject factor. Age wasentered into the model as a covariate to account for thesignificant difference in age between mothers and non-mothers. Greenhouse–Geisser corrections were usedwhere applicable. Effect sizes are presented as partialeta-squared (η2

p), where .01 represents a small effectsize, .06 represents a medium effect size, and .14 rep-resents a large effect size (Cohen, 1988). Relationshipsbetween BDI-II scores and ERP data were analyzed byPearson correlations.

RESULTS

Impact of parental status

The average ERP waveform for mothers and non-mothers is shown in Figure 2. After controlling for ageas a covariate, the analyses of variance for P1 ampli-tude, P1 latency, N170 amplitude, and N170 latencyyielded null results (F’s < 3.24, p’s > .05) for allvariables of interest (see Supplemental Materials)with one exception. A significant interaction wasobserved between hemisphere and parental status,F(1,26) = 6.07, p = .02, η2

p = 0.19. Post-hoc t-testsindicated that N170 amplitudes (μV) differed signif-icantly between right (M = –3.87; SD = 2.53) and left(M = –2.21; SD = 1.44) hemispheres in non-mothers,t(11) = 2.85, p = 0.2, whereas N170 amplitudesdid not differ significantly between right (M =–3.78; SD = 1.82) and left (M = –3.42; SD = 1.81)

–1

–100

–2

–3

–4

Figure 2. Grand average ERP waveforms for mothers (n = 17) andnon-mothers (n = 12) averaged across electrodes of interest in bothhemispheres and conditions. Amplitude (microvolts) is displayed asa function of latency (milliseconds).

hemispheres in mothers, t(16) = .72, p = .48. Notably,N170 amplitude in mothers and non-mothers didnot differ in either the right, t(27) = .11, p = .92,or left, t(27) = –1.92, p = .07, hemisphere. Thispost-hoc analysis suggests that the amplitude of theN170 elicited by infant faces does not differentiatehemispheric face processing between mothers andnon-mothers, but does suggest that, within non-mothers, there is an asymmetry in face perceptionconsistent with studies using adult faces (e.g., Bentinet al., 1996).

Impact of individual differences indepression symptoms

In the absence of emotional expression modulatingP1 and N170, ERP amplitudes and latencies wereaveraged across emotional expressions to yield amean value, and these values were assessed sep-arately for each hemisphere. The absence of aparental status group effect modulating P1 andN170 meant that data from mothers and non-motherswere included together for the individual differenceanalysis. Importantly, BDI-II scores for depressionsymptoms did not differ significantly between moth-ers (M = 6.00, SD = 4.56) and non-mothers (M = 3.75,SD = 3.52), t(27) = 1.43, p = .16 in the sampleincluded in this analysis.

BDI-II scores indicated that individuals in thisstudy experienced minimal to mild depression symp-toms (range = 0–17), according to the cut-offs recom-mended by Beck et al. (1996). No statistically signifi-cant relationships were found between BDI-II scoresand right P1 amplitude, r(29) = –.08, p = .69; leftP1 amplitude, r(29) = –.08, p = .67; right P1 latency,

PERCEPTUAL CODING OF INFANT FACES 531

0

5

10

15

20

–12 –10 –8 –6 –4 –2 0 2

BD

I-II

Sco

re

Right N170 Amplitude (microvolts)

r(29) = –.48, p < .01

Figure 3. Depression symptoms showed a statistically signifi-cant positive correlation with right hemisphere N170 amplitude(microvolts) in response to infant face stimuli across conditions.

r(29) = –.30, p = .12; or left P1 latency, r(29) = –.18,p = .35. However, a significant relationship wasobserved between BDI-II scores and N170 amplitudefor the right hemisphere; they were positively cor-related (Figure 3), r(29) = –.48, p < .01, indicating23.04% shared variance between the two variables.According to the guidelines established by Cohen(1988), this constitutes a medium effect size and indi-cates that, as BDI-II scores increase, N170 amplitudealso increases. A slight positive correlation was alsoobserved in the left hemisphere (Figure 4); how-ever, the relationship was not statistically significant,r(29) = –.25, p = .19, indicating only 6.25% sharedvariance between BDI-II scores and N170 ampli-tudes. By Cohen’s (1988) guidelines, this constitutesa small effect size. No significant relationships werefound between BDI-II scores and right N170 latency,r(29) = –.08, p = .69; or left N170 latency, r(29) =–.09, p = .63.

The relationship between the cognitive-affectiveand the somatic factors of the BDI-II andN170 amplitude was also examined as a function

–12 –10 –8 –6 –4 –2 0 20

5

10

15

20

BD

I-II

Sco

re

Left N170 Amplitude (microvolts)

r(29) = –.25, p = .19

Figure 4. Depression symptoms showed a statistically non-significant positive correlation with left hemisphere N170 amplitude(microvolts) in response to infant face stimuli across conditions.

of hemisphere. Notably, in the right hemisphere, thecognitive-affective factor of the BDI-II exhibiteda statistically significant positive correlation withN170 amplitude, r(29) = –.49, p < .01. However, thecorrelation between the somatic factor of the BDI-IIand N170 amplitude did not reach statistical signifi-cance, r(29) = –.32, p = .10. In the left hemisphere,the cognitive-affective factor of the BDI-II exhibiteda non-significant correlation with N170 amplitude,r(29) = –.24, p = .21; and a non-significant correla-tion between the somatic factor of the BDI-II andN170 amplitude, r(29) = –.19, p = .31.

DISCUSSION

Using the ERP technique, this study investigated theimpact of parental status (mother, non-mother), infantemotional expression (pleasure, comfort, distress), andself-reported symptoms of depression on early visualprocessing of infant faces in a community sampleof healthy adult women. Two ERP components, theP1 and N170, were used separately as dependent vari-ables to evaluate the magnitude and temporal courseof neural activity during early visual processing ofinfant faces under passive viewing conditions. In keep-ing with the extant literature on early face processing,the P1 was regarded as a general marker of earlyvisual processing and the N170 was utilized as a neuralmarker of early face processing.

Infant emotional expression did not modulate char-acteristics of the N170 in this experiment. This isconsistent with the claim that this ERP componentpredominantly reflects the structural encoding of facestimuli (Eimer & Holmes, 2007) and converges withthe results of Grasso and colleagues (2009), whoalso utilized a passive viewing paradigm but insteadmanipulated the familiarity and age (infant, adult)of their stimuli rather than emotional expression.However, our findings contradict those previouslyreported where infant emotional expression has mod-ulated N170 amplitude (e.g., Proverbio et al., 2006;Roderigo et al., 2011). Moreover, the present studyincluded stimuli that had previously been shown tomodulate the N170 (Proverbio et al., 2006); therefore,it seems unlikely that the absence of N170 modulationby infant affect is related to the stimuli employed inthe present study.

A notable difference between studies that havefound modulation of N170 amplitude by infant affectis the nature of the task participants engage in duringeach experiment. In contrast to the passive view-ing paradigm used in this experiment, Proverbioand colleagues (2006) and Roderigo and colleagues

532 NOLL, MAYES, RUTHERFORD

(2011) engaged participants in an emotion-recognitiontask, perhaps increasing attention allocation to thevisual stimuli. As increased attention is thought tomodulate early visual processing of the N170 (Holmes,Vuilleumier, & Eimer, 2003), it is possible the differ-ence in task demands could account for the discrep-ancy between study results. This notion is consistentwith the results of one fMRI study that found thatdifferential patterns of prefrontal cortical activity inmothers (compared to non-mothers) were dependentupon whether they were discriminating infant emo-tional expressions or passively viewing these stim-uli (Nishitani, Doi, Koyama, & Shinohara, 2011).Future work should explore the influence of these taskdemands on early perceptual processing of infant facestimuli, using a block design that contains both pas-sive and active viewing conditions. Such studies mayhelp clarify the conditions under which reduced orenhanced sensitivity to infant cues has the greatestimpact on parenting behavior.

Interestingly, a statistically significant interactionbetween parental status and hemisphere was observed.In keeping with behavioral studies that suggest aright hemisphere advantage for processing adult(Dutta & Mandel, 2002) and infant faces (Brosch,Sander, & Scherer, 2007), the N170 amplitudes ofnon-mothers in our sample were larger in the right (vs.left) hemisphere. This also converges with the resultsof other ERP (e.g., Bentin et al, 1996; Rossion, Joyce,Cottress, & Tarr, 2003) and fMRI (Haxby et al., 2000)studies that demonstrate a right hemisphere bias in theneural correlates of face processing. By contrast, nostatistically significant lateralization in amplitude sizewas observed in mothers for the N170 in this exper-iment. While it is important to reiterate that no maineffects were observed between groups, it is possiblethat this interaction may index the presence of norma-tive reproduction or parenting-induced cortical reorga-nization in mothers such that there is equal hemispheresensitivity to infant faces. To test this hypothesisempirically, longitudinal studies of mothers duringpregnancy and into the postpartum period would bevaluable, contrasting with neural responses measuredfrom non-mothers across the same time frame.

Supporting this interpretation, both animal andhuman studies suggest that the biological changesassociated with reproduction facilitate the emergenceof sensitive parenting (Kim et al., 2010; Strathearnet al., 2009). While the mechanisms of action for theseprocesses remain largely unknown, the results froma recent randomized, controlled trial of nulliparouswomen (n = 42) suggest that the hormone oxytocinpromotes caregiving behaviors, such as approachinga crying infant, by reducing activation in brain areas

known to modulate behavioral responses to anxi-ety and disgust (i.e., the amygdala) and increasingactivation in neural circuitry that promotes empathy(i.e., the insula and inferior frontal gyrus pars trian-gulars) (Riem et al., 2011). This is consistent withtheories from affective neuroscience that suggest thatthe balance between two distinct motivational systemsregulates human interaction (e.g., Davidson, 1992,1998; Lang, Bradley, & Cuthbert, 1997, 1998; seeRutherford & Lindell, 2011, for recent review). Thefirst may be regarded as an approach system and isthought to be involved in goal-directed behavior andthe maintenance of positive affect. The second is bestcategorized as a withdrawal system and is believed tocoordinate responses to aversive or threatening stimuliand generate negative affect. It is proposed that both ofthese systems are regulated by the forebrain: whereasthe approach system is modulated by increased neu-ral activity in the left prefrontal cortex, the withdrawalsystem is regulated by increased activity in the rightprefrontal cortex (Fowles, 1994).

Importantly for maternal behavior, the balancebetween the approach and withdrawal systems maybe disrupted by depression symptoms, which are com-mon in the postpartum period (Moses-Kolko, Meltzer,Berga, & Wisner, 2008). In our study, mothers andnon-mothers were combined into one group for theanalysis of individual differences in self-reporteddepression symptoms. To the authors’ knowledge, thisis the first ERP study to examine the influence ofdepression symptoms on early visual coding of infantfaces in a non-clinical sample of women. No rela-tionship was observed between characteristics of theP1 ERP component and participant scores on theBeck Depression Inventory II (BDI-II) (Beck et al.,1996), suggesting that visual perception in general wasnot compromised by variability in depression symp-tomatology in the current sample. There was also norelationship between BDI-II scores and N170 latency,providing preliminary evidence that depression symp-toms do not seem to impact the efficiency of process-ing of infant face stimuli during this portion of earlyvisual encoding.

Notably, a significant relationship was observedbetween participant scores on the BDI-II andN170 amplitude, but in the opposite direction thanexpected. Whereas it was predicted that depressionscores would inversely correlate with N170 ampli-tude, a positive correlation was observed with greaterlevels of self-reported depression symptoms corre-sponding to more negative (i.e., larger) deflectionsof the N170 for infant face stimuli. This resultwas statistically significant for the right hemisphereonly. These results suggest that the infant faces used

PERCEPTUAL CODING OF INFANT FACES 533

in this experiment may be more visually salient(evidenced by increased amplitude measures) forparticipants reporting higher levels of mild depressionsymptoms—but none of whom were over the thresh-old for clinical depression. While replication withboth clinically depressed and healthy participantsis needed to make inferences about functional sig-nificance of this effect for participants experienc-ing sub-clinical depression symptoms, it is possi-ble that these results represent the lower end of amulti-modal distribution—the upper end of whichexhibits an inverse relationship between depressionsymptom severity and N170 amplitude. Specifically,where women with mild depression symptoms exhibitincreased neural responsivity for infant faces, perhapsserving an adaptive function in the context of caregiv-ing that may support increased allocation of attentionto the infant, women with clinically significant depres-sion symptoms might exhibit an attenuated neuralresponse. Alternatively, if the relationship betweenN170 amplitude and depression symptoms holds atclinically significant levels of symptom expression, thelack of normative attentional bias for infant face stim-uli that was observed in clinically depressed women(e.g., Pearson et al., 2010a, 2010b) may reflect avoid-ance of, rather than indifference to, visually salientstimuli. Consistent with this notion of avoidance andthe increased N170 amplitude reported here, Pearson,Lightman, and Evans (in press) found that symptomsof depression were associated with increased systolicblood pressure responses in women when exposed toinfant distress.

While the relationship between aberrations inperceptual processing at the neural level and insen-sitive parenting behavior remains far from clearlyestablished, some evidence suggests that depressedmothers spend less time looking at their infants’faces (e.g., Livingood & Daen, 1983). Likewise, sincedepression is reliably associated with a negativitybias in cognitive attentional processing, particularlyfor self-related stimuli (Mathews & MacLeod, 2005),when depressed women do gaze at their infant’s face,some data suggest that their subjective experience ofvisual perception differs significantly from that ofhealthy controls. For example, Stein and colleagues(2010) found that depressed mothers rated infantfaces expressing distress more negatively than controlor anxious mothers, suggesting depression-specificaberrations in the processing of emotional infantstimuli. Supporting this hypothesis, results from thecurrent study suggest that the relationship betweendepression symptoms and early encoding of infantface stimuli is independent of aberrations in sleep,appetite, energy level, or concentration, as only

the cognitive-affective (and not somatic) factor ofthe BDI-II was significantly associated with rightN170 amplitude. However, it is worthwhile beingcautious with this interpretation, as the somatic factorconsists of fewer items and we observed a trend for acomparable relationship to that observed between theN170 and cognitive-affective factor.

An alternative interpretation to the positive cor-relation between N170 amplitude and BDI-II scoresreported here is that differences in sensitivity toinfant cues across the sample may be representativeof differences in other domains relevant to depres-sion. Anhedonia is a core feature of depression thatrepresents the inability to experience pleasure orreward from affectively positive stimuli or situations.Arguably, infant stimuli are inherently rewarding, evenwhen expressing affectively neutral or negative expres-sions. Indeed, there is evidence that the rewardingvalue of infant stimuli may down-regulate the stressresponse system when mothers experience infant nega-tive affect (Strathearn et al., 2009). In depressed adults,anhedonia, not depression, symptoms positively corre-lated with brain activity in response to happy stimuli(Keedwell, Andrew, Williams, Brammer, & Phillips,2005). This increasing activity was observed in brainregions responsible for attentional control, and sug-gests that anhedonic individuals may pay more atten-tion to positive stimuli to increase their positivemood. No such effect was seen with negative stim-uli. This notion of increased attention to rewardingstimuli resonates with findings that increased atten-tion to faces enhances the N170 (Holmes et al., 2003).Therefore, variability in levels of anhedonia, ratherthan depression, may drive the positive correlationbetween N170 amplitude to infant faces and BDI-IIscores observed here. Indeed, the depression symp-toms reported by Pearson and colleagues (in press) asbeing associated with increased systolic blood pressureresponses to infant distress were anhedonic depressionsymptoms. It is the goal of our ongoing research toinvestigate this proposal, as well as disentangle therelative role of salience and visual attention to theperception of infant cues in depressed women.

It is important to note the limitations of the presentstudy. Despite finding a correlation between BDI-II scores and N170 amplitude, the present studywill need to be replicated with a larger sample.Accordingly, since the majority of women recruitedfor the study were Caucasian, with few self-identifiedminorities, replication with a racially diverse sam-ple (and correspondingly diverse infant face stim-uli) will be necessary. All infant stimuli presentedto the women were unfamiliar; therefore, it remainsunclear whether and how this effect differs from

534 NOLL, MAYES, RUTHERFORD

depression-related aberrations in the visual process-ing of other emotionally salient face and non-facevisual stimuli of varying familiarity. Indeed, famil-iarity may serve as a protective factor if there is aninherently rewarding value when perceiving one’s owninfant. Moreover, differential perception of infant cuesas measured by the N170 may not translate to mater-nal sensitivity at the behavioral level. Therefore, futurework should explore the functional significance ofthese findings for maternal sensitivity at the behaviorallevel and longitudinally across the postpartum period.While not evaluated in this study, later ERP compo-nents (underscoring cognitive as well as perceptualprocessing) could also be examined to understand theimpact of depression symptomatology on the temporaldynamics of infant face perception. Both early and lateERP components could also be examined in relationto additional individual difference variables related toparenting in mothers (e.g., postpartum bonding, attach-ment, parenting stress) as well as emotion perceptionand regulation in women more generally. Indeed, dif-ferences in depression symptomatology may emerge atthe level of higher cognitive processes as well. Finally,it is worth noting that while we included age as acovariate in the analyses, mothers were older thannon-mothers. This is an important variable to considerfor the field of experimental parenting research wheninvestigating the potential for differences between par-ents and non-parents. While age-matching is optimalin experimental design, in this study as in others, moth-ers are typically older than non-mothers. Recruitmentof older women to age match with mothers maypresent additional confounding variables, includingvariability in attitudes toward parenting and childrearing as well as medical conditions preventing preg-nancy (see also Gustafson & Harris, 1990).

In conclusion, this study extends existing researchon the impact of parental status (mother, non-mother),infant emotional expression (pleasure, comfort, dis-tress), and hemisphere, on early visual process-ing of infant faces under passive viewing condi-tions; and offers a new exploration of the relation-ship between early visual processing of infant facesand individual differences in self-reported depressionsymptoms. While the N170 was not modulated byparental status, infant emotional expression, or hemi-sphere, a statistically significant positive correlationwas observed between depression symptom severityand N170 amplitude. Although replication and futureresearch are needed to determine the exact signif-icance of this finding, it provides preliminary evi-dence that depression symptoms may modulate earlyneurological responsiveness to infant cues, even atsub-clinical levels.

Original manuscript received 1 January 2012Revised manuscript accepted 28 February 2012

First published online 21 March 2012

REFERENCES

Adachi, I., Chou, D. P., & Hampton, R. R. (2009). Thatchereffect in monkeys demonstrates conservation of faceperception across primates. Current Biology, 19(15),1270–1273.

American Psychiatric Association (APA) (1994). Diagnosticand statistical manual of mental disorders (4th ed.).Washington, DC: APA.

Beck, A. T., Steer, R. A., & Garbin, M. G. (1996). Manualfor the Beck Depression Inventory-II. San Antonio, TX:Psychological Corporation.

Beebe, B., Jaffe, J., Chen, H., Buck, K., Cohen, P., &Feldstein, S. et al. (2008). Six-week postpartum depres-sive symptoms and 4-month mother–infant self- andinteractive contingency. Infant Mental Health Journal,29, 442–471.

Beebe, B., Jaffe, J., Markese, S., Buck, K., Chen, H.,& Cohen, P., et al. (2010). The origins of 12-monthattachment: A microanalysis of 4-month mother–infantinteraction. Attachment and Human Development, 12,1–135.

Beeghly, M., Fuertes, M., Liu, C. H., Delonis, M. S., &Tronick, E. (2011). Maternal sensitivity in dyadic con-text: Mutual regulation, meaning-making, and reparation.In D. W. Davis & M. C. Logsdon (Eds.), Maternal sen-sitivity: A scientific foundation for practice (pp. 45–69).New York: Nova Science Publishers, Inc.

Bentin, S., McCarthy, G., Perez, E., Puce, A., & Allison,T. (1996). Electrophysiological studies of face percep-tion in humans. Journal of Cognitive Neuroscience, 8(6),551–565.

Bindemann, M., Burton, A. M., Hooge, I. T., Jenkins,R., & de Haan, E. H. (2005). Faces retain attention.Psychonomic Bulletin and Review, 12, 1048–1053.

Blau, V. C., Maurer, U., Tottenham, N., & McCandliss, B.D. (2007). The face-specific N170 component is mod-ulated by emotional facial expression. Behavioral andBrain Functions, 3(7).

Brosch, T. Sander, D., & Scherer, K. R. (2007). Thatbaby caught my eye: Attention capture by infant faces.Emotion, 7(3), 685–689.

Bruce, V., & Young, A. (1986). Understanding face recogni-tion. British Journal of Psychology, 77(3), 305–327.

Cohen, J. (1988). Statistical power analysis for the behav-ioral sciences (2nd ed.). Hillsdale, NJ: LawrenceErlbaum Associates, Inc.

Davidson, R. J. (1992). Anterior cerebral asymmetry and thenature of emotion. Brain and Cognition, 20(1), 125–151.

Davidson, R. J. (1998). Affective style and affective disor-ders: Perspectives from affective neuroscience. Cognitionand Emotion, 12(3), 307–330.

Davis, D. W., & Logsdon, M. C. (Eds.) (2010). Maternal sen-sitivity: A scientific foundation for practice. New York:Nova Science Publishers, Inc.

Dozois, D., Dobson, K., & Ahnberg, J. (1998). Apsychometric evaluation of the Beck DepressionInventory-II. Psychological Assessment, 10(2), 83–89.

PERCEPTUAL CODING OF INFANT FACES 535

Dutta, R., & Mandal, M. K. (2002). Visual-field superiorityas a function of stimulus type and content. InternationalJournal of Neuroscience, 112(8), 945–952.

Eimer, M. (2000a). Effects of face inversion on the struc-tural encoding and recognition of faces: Evidence fromevent-related brain potentials. Cognitive Brain Research,10(1–2), 145–158.

Eimer, M. (2000b). The face-specific N170 componentreflects late states in the structural encoding of faces.Neuroreport, 11(10), 2319–2324.

Eimer, M., & Holmes, A. (2007). Event-related brainpotential correlates of emotional face processing.Neuropsychologia, 45(1), 15–31.

Fonagy, P., Gergely, G., Jurist, E., & Target, M. (2002).Affect regulation, mentalization, and the development ofthe self . New York, NY: Other Press.

Fowles, D. C. (1994). A motivational theory ofpsychopathology. Nebraska Symposium on Motivation,41, 181–238.

Grasso, D. J., Moser, J. S., Dozier, M., & Simons, R. (2009).ERP correlates of attention allocation in mothers process-ing faces of their children. Biological Psychology, 81,95–102.

Gustafson, G. E., & Harris, K. L. (1990) Women’s responsesto young infants’ cries. Developmental Psychology, 26,144–152.

Haxby, J. V., Hoffman, E. A., & Gobbini, M. I. (2000).The distributed human neural system for face per-ception. Trends in Cognitive Neuroscience, 4(6),223–233.

Holmes, A., Vuilleumier, P., & Eimer, M. (2003). The pro-cessing of emotional face expression is gated by spatialattention: Evidence from event-related potentials. BrainResearch. Cognitive Brain Research, 16(2), 174–184.

Keedwell, P. A., Andrew, C., Williams, S. C. R., Brammer,M. J., & Phillips, M. L. (2005). The neural correlatesof anhedonia in major depressive disorder. BiologicalPsychiatry, 58, 843–853.

Kim, P., Leckman, J. F., Mayes, L. C., Feldman, R., Wang,X., & Swain, J. E. (2010). The plasticity of human mater-nal brain: Longitudinal changes in brain anatomy duringthe early postpartum period. Behavioral Neuroscience,124, 695–700.

Kinsley, C. H., & Lambert, K. G. (2008). Reproduction-induced neuroplasticity: Natural behavioural alterationsassociated with the production and care of offspring.Journal of Neuroendocrinology, 20(4), 515–525.

Lang, P., Bradley, M. M., & Cuthberg, B. N. (1997).Motivated attention: Affect, activation and action. InP. Lang, R. F. Simons, & M. Balaban (Eds.), Attentionand orienting: Sensory and motivational processes(pp. 97–136). Hillsdale, NJ: Lawrence ErlbaumAssociates, Inc.

Lang, P. J., Bradley, M. M., & Cuthbert, B. N.(1998). Emotion, motivation, and anxiety: Brain mech-anisms and psychophysiology. Biological Psychiatry, 44,1248–1263.

Lewis, G., Pelosi, A. J., Araya, R., & Dunn, G. (1992).Measuring psychiatric disorder in the community: Astandardized assessment for use by lay interviewers.Psychological Medicine, 22, 465–486.

Livingood, A. B., & Daen, P. (1983). The depressed motheras a source of stimulation for her infant. Journal ofClinical Psychology, 39(3), 369–375.

Lorenz, K. (1943). Die angeborenen Formen möglicherErfahrung [The innate forms of potential experience].Zeitschrift für Tierpsychologie, 5, 233–519.

Lorenz, K. (1971). Studies in animal and human behaviourII. (R. Martin, Trans.). Cambridge, MA: HarvardUniversity Press.

Luck, S. J. (2005). An introduction to the event-relatedpotential technique. Boston, MA: MIT Press.

Mathews, A., & MacLeod, C. (2005). Cognitive vulnera-bility to emotional disorders. Annual Review of ClinicalPsychology, 1, 167–195.

McPartland, J., Dawson, G., Webb, S. J., Panagiotides,H., & Carver, L. J. (2004). Event-related brain poten-tials reveal anomalies in temporal processing of faces inautism spectrum disorder. Journal of Child Psychologyand Psychiatry, 45(7), 1235–1245.

Moses-Kolko, E. L., Fraser, D., Wisner, K. L., James, J. A.,Saul, A. T., & Fiez, J. A., et al. (in press). Rapid habitu-ation of striatal response to reward receipt in postpartumdepression. Biological Psychiatry.

Moses-Kolko, E. L., Meltzer, C. C., Berga, S. L., & Wisner,K. L. (2008). Postpartum depression: The clinical disor-der and application of PET imaging research methods. InR. S. Bridge (Ed.), Neurobiology of the parental brain(pp. 175–199). London, UK: Elsevier.

Nishitani, S., Doi, H., Koyama, A., & Shinohara, K. (2011).Differential prefrontal response to infant facial emotionsin mothers compared with non-mothers. NeuroscienceResearch, 70(2), 183–188.

Papousek, H., & Papousek, M. (1975). Cognitive aspects ofpreverbal social interaction between human infants andadults. Ciba Foundation Symposium, 33, 241–269.

Papousek, H., & Papousek, M. (1977). Mothering and thecognitive headstart: Psychobiological considerations. InH. R. Shaffer (Ed.), Studies in mother–infant interaction(pp. 63–85). London, UK: Academic Press.

Papousek, H., & Papousek, M. (1982). Integration into thesocial world: Survey of the research. In P. Stratton (Ed.),Psychobiology of the human newborn (pp. 367–390).New York, NY: Wiley.

Papousek, H., & Papousek, M. (1983). Biological basisof social interactions: Implications of research for anunderstanding of behavioural deviance. Journal of ChildPsychology and Psychiatry and Allied Disciplines, 24,117–129.

Papousek, H., & Papousek, M. (1987). Intuitive parenting:A dialectic counterpart to the infant’s integrative com-petence. In J. D. Osofsky (Ed.), Handbook of infantdevelopment, 2nd ed. (pp. 669–720). New York, NY:Wiley.

Pearson, R. M., Cooper, R. M., Penton-Voak, I. S., Lightman,S. L., & Evans, J. (2010a). Depressive symptoms inearly pregnancy disrupt attentional processing of infantemotion. Psychological Medicine, 40, 621–631.

Pearson, R. M., Lightman, S. L., & Evans, J. (2010b).Attentional processing of infant emotion during late preg-nancy and mother–infant relations after birth. Archives ofWomen’s Mental Health, 14(1), 23–31.

Pearson, R. M., Lightman, S. L., & Evans, J. (in press).Symptoms of depression during pregnancy are associatedwith increased systolic blood pressure responses towardsinfant distress. Archives of Women’s Mental Health.

Proverbio, A. M., Brignone, V., Matarazzo, S., Del Zotto,M., & Zani, A. (2006). Gender and parental status affect

536 NOLL, MAYES, RUTHERFORD

the visual cortical response to infant facial expression.Neuropsychologia, 44, 2987–2999.

Purhonen, M., Paakkonen, A., Ypparila, H., Lehtonen, J.,& Karhu, J. (2001). Dynamic behavior of the auditoryN100 elicited by a baby’s cry. International Journal ofPsychophysiology, 41, 271–278.

Riem, M. M. E., Bakermans-Kranenburg, M. J., Pieper,S., Tops, M., Boksem, M. A. S., & van IJzendoorn,M. H. (in press). Oxytocin modulates amygdala, insula,and inferior frontal gyrus responses to infant crying: Arandomized controlled trial. Biological Psychiatry.

Riskind, J. H., Beck, A. T., Brown, G., & Steer, R. A.(1987). Taking the measure of anxiety and depres-sion: Validity of the reconstructed Hamilton scales.Journal of Nervous and Mental Disease, 1975,474–479.

Rodrigo, M. J., León, I., Quiñones, I., Lage, A., Byrne,S., & Bobes, M. A. (2011). Brain and personalitybases of insensitivity to infant cues in neglectful moth-ers: An event-related potential study. Development andPsychopathology, 23, 163–176.

Rossion, B., Campanella, S., Gomez, C. M., Delinte, A.,Debatisse, D., Liard, L., et al. (1999). Task modulation ofbrain activity related to familiar and unfamiliar face pro-cessing: An ERP study. Clinical Neurophysiology, 110,449–462.

Rossion, B., Gauthier, I., Tarr, M. J., Despland, P., Bruyer,R., Linotte, S., et al. (2000). The N170 occipito-temporalcomponent is delayed and enhanced to inverted facesbut not to inverted objects: An electrophysiologicalaccount of face-specific processes in the human brain.Neuroreport, 11(1), 69–74.

Rossion, B., Joyce, C. A., Cottrell, G. W., & Tarr, M. J.(2003). Early lateralization and orientation turning forface, word, and object processing in the visual cortex.NeuroImage, 20, 1609–1624.

Rutherford, H. J. V., & Lindell, A. K. (2011). Thrivingand surviving: Approach and avoidance motivation andlateralization. Emotion Review, 3(3), 333–343.

Rutherford, H. J. V., & Mayes, L. C. (2011). Primary mater-nal preoccupation: Using neuroimaging techniques toexplore the parental brain. Psyche, 65, 973–988.

Schneider, W., Eschman, A., & Zuccolotto, A., (2002).E-Prime user’s guide. Pittsburgh, PA: PsychologySoftware Tools.

Segal, D. L., Coolidge, F. L., Cahill, B. S., & O’Riley, A. A.(2008). Psychometric properties of the Beck DepressionInventory-II (BDI-II) among community-dwelling olderadults. Behavior Modification, 32(1), 3–20.

Seifritz, E., Esposito, F., Neuhoff, J. G., Lüthi, A.,Mustovic, H., Dammann, G., et al. (2003). Differentialsex-independent amygdala response to infant cryingand laughing in parents versus nonparents. BiologicalPsychiatry, 54, 1367–1375.

Stein, A., Arteche, A., Lehtonen, A., Craske, M., Harvey, A.,Counsell, N., et al. (2010). Interpretation of infant facialexpression in the context of maternal postnatal depres-sion. Infant Behavior & Development, 33, 273–278.

Storch, E., Roberti, J., & Roth, D. (2004). Factor struc-ture, concurrent validity, and internal consistency of theBeck Depression Inventory-Second Edition in a sam-ple of college students. Depression and Anxiety, 19(3),187–189.

Strathearn, L., Fonagy, P., Amico, J., & Montague,P. R. (2009). Adult attachment predicts mater-nal brain and oxytocin responses to infant cues.Neuropsychopharmacology, 34(13), 2655–2666.

Tucker, D. M., (1993). Spatial sampling of head electricalfields: The geodesic sensor net. Electroencephalographyand Clinical Neurophysiology, 87, 154–163.

Weiner, I. B., & Craighead, W. B. (2010). The CorsiniEncyclopedia of Psychology, vol. I. Hoboken, NJ: Wiley.

Whisman, M., Perez, J., & Ramel, W. (2000). Factorstructure of the Beck Depression Inventory SecondEdition (BDI-II) in a student sample. Journal of ClinicalPsychology, 56(4), 545–551.

Yin, R. K. (1969). Looking at upside-down faces. Journal ofExperimental Psychology, 81, 141–145.

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