Elsevier

Neuropsychologia

Volume 50, Issue 7, June 2012, Pages 1297-1307
Neuropsychologia

Event-related potentials elicited in mothers by their own and unfamiliar infants’ faces with crying and smiling expression

https://doi.org/10.1016/j.neuropsychologia.2012.02.013Get rights and content

Abstract

Crying by an infant signals an urgent desire for care and protection. Because of the special relationship between a mother and her infant and the signal value of her crying, it is plausible to suggest that the maternal brain efficiently processes crying by infants. In the present study, we examined this hypothesis by measuring event-related potentials in mothers while they observed crying or smiling by their own or unfamiliar infants embedded within a train of neutral expressions. We found that the amplitude of the face-specific N170 component was enlarged for crying regardless of familiarity. The P300 component, which reflects a later cognitive evaluation stage of stimulus processing, was decomposed into functionally distinct components by temporal principal component analysis. The amplitude of the third temporal factor, which corresponds to the earliest portion of the P300, was larger when a mother observed her own infant crying than for the other conditions. Moreover, onset latency of P300 was shortest when mothers observed their own infant crying. These results indicate that mothers process their own infant's crying more efficiently than smiling by their own infant or crying by an unfamiliar infant.

Highlights

► Mothers viewed own and unfamiliar infant's emotional expression. ► Early portion of P300 is enlarged specifically by own infant's crying face. ► Onset of P300 effect was fastest for own infant's crying face. ► Interaction between identity and expression at evaluative stage of face perception.

Introduction

Crying is one form of attachment behavior, and the auditory and visual signals accompanying crying elicit empathy and motivation to relieve the discomfort of the infant (Hendriks and Vingerhoets, 2006, Hendriks et al., 2007, Spangler et al., 2001). Crying plays a prominent role in the relationship between mothers and infants, especially at the non-verbal stage (Acebo & Thoman, 1995). An infant's crying signals an urgent need for care and protection, which makes it of primary importance for mothers to direct their attention efficiently toward their infant's crying cues. Attentiveness to infant crying together with the ensuing care-taking and protecting behaviors ultimately increases the odds of an off-spring's survival (Hahn-Holbrook, Holbrook, & Haselton, 2011). Therefore, throughout the evolutionary history of mankind, it has been quite advantageous for humans to be endowed with mechanisms that allow for efficient response to the crying of their infants.

In the sense that an infant's crying signals discomfort, a crying face can be regarded as one type of negative expressions. On this basis, it could be predicted that the processing of crying is partly subserved by neural mechanisms that are also recruited in the processing of negative expressions. The human visual system is quite efficient at detecting negative information (Cuthbert et al., 2000, Eimer and Holmes, 2002, Olofsson et al., 2008). This negativity bias (Ito, Larsen, Smith, & Cacioppo, 1998) extends to the domain of social cognition, with negative expressions inducing stronger and more efficient behavioral and neural responses than positive ones. At the same time, previous studies on crying indicate that a crying face, especially the crying face of an infant, is distinguishable from other negative expressions by the behavioral and neural responses to this stimulus (Noriuchi et al., 2008, Strathearn et al., 2009, Spangler et al., 2001). Therefore, simple extrapolations of findings based on negative facial expressions are not sufficient to unravel the neural mechanisms of processing crying. However, there is a paucity of studies that have examined the crying-related perceptual mechanisms.

In exploring the neural mechanism of the processing of attachment-related behavior such as crying, it is important to examine the influence of identity or familiarity. Because the attachment bond between mother and child is presumably one of the most intimate and personal of human relationships (Ainsworth, Blehar, Waters, & Wall, 1978; Bowlby, 1969), mothers often deem their own child irreplaceable. Considering the special status of her own infant for a mother (Bartels and Zeki, 2004, Grasso et al., 2009, Leibenluft et al., 2004, Nitschke et al., 2004, Noriuchi et al., 2008), together with the fact that an infant's crying signals an urgent need for care and protection (Acebo & Thoman, 1995), we hypothesized that a mother's processing of her own infant's crying takes precedence over the processing of other types of facial expressions. However, few studies to date have empirically examined this hypothesis. Several previous studies using fMRI compared neural activations in mothers when viewing their own or an unfamiliar infant's expressions. However, most of these studies (Bartels and Zeki, 2004, Leibenluft et al., 2004, Nitschke et al., 2004, Ranote et al., 2004) focused on either neutral or smiling expressions.

As notable exceptions, some fMRI studies (Noriuchi et al., 2008, Strathearn et al., 2009) revealed that the presentation of expressions of social distress by a mother's own infant induces different neural activations from the presentation of similar expressions in unfamiliar infants. However, the low-temporal resolution of fMRI prevented the researchers from examining whether the processing of a mother's own infant's crying temporally precedes that of other types of infant emotional expressions. In contrast to fMRI, the event-related potential (ERP) technique is a useful tool for investigating the temporal course of neural activations in face processing because of its high temporal resolution. Nonetheless, to date there have been only a few sporadic attempts to apply ERP measurement to the study of processing crying faces (Hendriks et al., 2007, Proverbio et al., 2006, Rodrigo et al., 2011). Of particular relevance to the present study, Proverbio et al. (2006) compared the electrophysiological responses to infant's emotional expression across mothers, fathers, nulliparous women, and childless males. The results showed striking differences in the electrophysiological responses to infant's distress expressions between mothers and the other participant groups. However, they did not compare the electrophysiological responses to distress expressions of a mother's own and an unfamiliar infant.

The primary aim of the present study was to examine whether crying face of mother's own infant is processed more efficiently in mothers than other types of infant emotional expressions. To this end, we measured ERPs elicited by crying or smiling of a mother's own or an unfamiliar infant. To control for the stimulus attributes of the facial stimuli, a yoked design (Roye et al., 2007, Roye et al., 2010) was adopted. Specifically, every participant was paired with another participant and presented a picture of her counterpart's infant as the unfamiliar infant, ensuring that exactly the same set of stimuli were presented in each condition. A similar stimulus presentation design was used in previous neuroimaging studies on neural activations in mothers in response to their own and an unfamiliar infant's emotional expressions (Nitschke et al., 2004, Ranote et al., 2004).

The crying and smiling expressions were presented in an odd-ball stimulus presentation format (Olofsson et al., 2008, Polich, 2007, Polich et al., 1994, Rozenkrants and Polich, 2008). Specifically, the infants crying and smiling expressions were presented as low-frequency targets embedded within a train of high-frequency neutral expressions. In such experimental paradigms, a series of early components (P1, N170) that reflect the perceptual processing of visual stimuli and a large positivity called P300 are elicited to target-stimuli. By examining the effects of facial expressions and familiarity on these components, we aimed to clarify whether these factors exert interacting influences at each stage of face processing.

The presentation of facial stimuli induces a series of components at the occipito-temporal electrode sites. After about an 80–120 ms stimulus onset, a prominent positivity (P1) is observed at occipital electrodes. P1 purportedly reflects the processing of low-level visual features such as luminance and contrast (Taylor, 2002). However, several studies have indicated that this component is also sensitive to face-specific information (Doi et al., 2007, Doi et al., 2009, Herrmann et al., 2005, Linkenkaer-Hansen et al., 1998, Taylor, 2002). Following P1 component, a negativity called N170 is observed at the occipito-temporal region. N170 reflects the structural encoding of face processing (Bentin et al., 1996, Eimer, 2000a, Eimer, 2000b, Rossion et al., 1999), which is involved in the formation of representations of spatial relations among facial parts. Although whether N170 component is sensitive to information other than facial configurations (Eimer, 2000a) is still controversial, several recent studies have shown that both facial expression (Caharel et al., 2005, Doi et al., 2010) and familiarity information (Caharel et al., 2005, Caharel et al., 2006) modulate N170 component. Examining the effects of facial familiarity and expressions on these components should show whether the processing by mothers of their own infant's crying is different than the processing of the crying faces of other infants at the initial perceptual stages of face perception.

P300 is a long-latency positive component elicited at posterior-medial electrodes by low-frequency target stimuli (Olofsson et al., 2008, Polich, 2007, Polich et al., 1994, Rozenkrants and Polich, 2008). P300 is generally considered to reflect cognitive evaluation stages of face processing that take place after initial perceptual stages of face processing reflected in P1 and N170. Previous studies have shown that P300 reflects diverse array of cognitive functions, including attentional control (Langeslag et al., 2007, Langeslag et al., 2008), memory (Olofsson et al., 2008, Polich, 2007, Polich et al., 1994, Rozenkrants and Polich, 2008), emotional arousal (Cuthbert et al., 2000, Delplanque et al., 2005), and stimulus evaluation (Bobes et al., 2007, Kutas et al., 1977, Picton, 1992, Polich, 2007, Woodman, 2010). On the basis of these, we hypothesized that analyzing the modulation of P300 should determine whether own infant's crying expression is processed more efficiently than other facial expressions at these later cognitive evaluation stages of face processing.

Some studies indicate that the neural responses to infants’ faces are supposed to be instinctive, whereas other studies show individual differences in these responses. With regard to the former notion, it is well accepted that “baby shema”, a collection of babyish characteristics such as big eyes and round contours, instinctively triggers protective and care-taking behaviors (Glocker et al., 2009a, Glocker et al., 2009b). In support of the latter notion, a recent study by Rodrigo et al. (2011) showed that personality traits modulate the amplitudes of long-latency potentials that are elicited when viewing infants’ emotional expressions. Specifically, they showed that the amplitudes of the long-latency positivity elicited by the neutral, crying, and laughing faces of unfamiliar infants were smaller in neglectful mothers than in healthy controls. If the neural responses to crying are influenced by individual characteristics (Rodrigo et al., 2011) as well as being instinctive responses (Glocker et al., 2009a, Glocker et al., 2009b), ERP components should be sensitive to a participants’ personality traits. To examine this possibility, we measured the participant's attachment attitudes towards their infants using a self-administered questionnaire and analyzed the relationship between these measures and ERP amplitudes.

Section snippets

Participants

Sixteen mothers (M = 31.7 ± 0.5 yrs) with infants approximately 12 months old (four girls; M = 12.3 ± 0.7 months) participated in the study. They provided an informed consent for the experimental procedure that was approved by the institutional ethics committee of Nagasaki University. All mothers were right-handed and had normal or corrected-to-normal visual acuity. They had no history of mental illness and were not on any medication at the point of participation.

Material preparation

At least two weeks before the EEG

Reaction times (RTs)

The RTs in the correct trials were averaged over each condition and are summarized in Table 1 together with the accuracy rates. The averaged RTs were entered into a two-way ANOVA with within-participant factors of familiarity (own–unfamiliar) and expression (smiling–crying). The ANOVA revealed a significant main effect of expression, F(1, 15) = 36.22, p < .01, ηp2=0.71, with RTs to images depicting crying being shorter than those to images depicting smiling. No other significant results were

Discussion

The present study measured ERPs elicited in mothers while they observed crying and smiling by their own or unfamiliar infants. N170, which is supposed to reflect perceptual stage of face processing, was enlarged by presentation of crying faces regardless of kinship of infant. In contrast, the early portion of the P300 component, TF3, was modulated by both facial expression and familiarity. That is, TF3 was larger in response to a mother's own infant's crying than to the other three types of

References (101)

  • H. Doi et al.

    The effects of eye and face inversion on the early stages of gaze direction perception – An ERP study

    Brain Research

    (2007)
  • H. Doi et al.

    Neural correlates of the stare-in-the-crowd effect

    Neuropsychologia

    (2009)
  • M. Eimer

    Event-related potentials distinguish processing stages involved in face perception and recognition

    Clinical Neurophysiology

    (2000)
  • M. Eimer

    Effects of face inversion on the structural encoding and recognition of faces – Evidence from event-related brain potentials

    Cognitive Brain Research

    (2000)
  • T.C. Frank et al.

    Effect of menstrual cycle phase on corticolimbic brain activation by visual food cues

    Brain Research

    (2010)
  • I.Q. González et al.

    Person identification through faces and voices: An ERP study

    Brain Research

    (2011)
  • D.J. Grasso et al.

    ERP correlates of attention allocation in mothers processing faces of their childre

    Biological Psychology

    (2009)
  • J.V. Haxby et al.

    The distributed human neutral system for face perception

    Trends in Cognitive Sciences

    (2000)
  • J. Hahn-Holbrook et al.

    Parental precaution: Neurobiological means and adaptive ends

    Neuroscience and Biobehavioral Reviews

    (2011)
  • E. Halgren et al.

    Intracerebral potentials to rare target and distractor auditory and visual stimuli. I. Superior temporal plane and parietal lobe

    Electroencephalography and Clinical Neurophysiology

    (1995)
  • E. Halgren et al.

    Intracerebral potentials to rare target and distractor auditory and visual stimuli. II. Medial lateral and posterior temporal lobe

    Electroencephalography and Clinical Neurophysiology

    (1995)
  • B. Jemel et al.

    Is the N170 for faces cognitively penetrable? Evidence from repetition priming of Mooney faces of familiar and unfamiliar persons

    Cognitive Brain Research

    (2003)
  • C. Joyce et al.

    The face-sensitive N170 and VPP components manifest the same brain processes: The effect of reference electrode sit

    Clinical Neurophysiology

    (2005)
  • D. Kuefner et al.

    Electrophysiological correlates of the composite face illusion: Disentangling perceptual and decisional components of holistic face processing in the human brain

    Brain and Cognition

    (2010)
  • S.J.E. Langeslag et al.

    Dissociating love-related attention from task-related attention: An event-related potential oddball study

    Neuroscience Letters

    (2008)
  • S.J.E. Langeslag et al.

    Event-related potential responses to love-related facial stimuli

    Biological Psychology

    (2007)
  • E. Leibenluft et al.

    Mothers’ neural activation in response to pictures of their children and other children

    Biological Psychiatry

    (2004)
  • K. Linkenkaer-Hansen et al.

    Face-selective processing in human extrastriate cortex around 120 ms after stimulus onset revealed by magneto- and electroencephalography

    Neuroscience Letters

    (1998)
  • J.P. Lorberbaum et al.

    A potential role for thalamocingulate circuitry in human maternal behavior

    Biological Psychiatry

    (2002)
  • D.A. Minnebusch et al.

    Neuropsychological mechanisms of visual face and body perception

    Neuroscience and Biobehavioral Reviews

    (2009)
  • J.B. Nitschke et al.

    Orbitofrontal cortex tracks positive mood in mothers viewing pictures of their newborn infants

    NeuroImage

    (2004)
  • M. Noriuchi et al.

    The functional neuroanatomy of maternal love: Mother's response to infant's attachment behaviors

    Biological Psychiatry

    (2008)
  • J.K. Olofsson et al.

    Affective picture processing: An integrative review of ERP findings

    Biological Psychology

    (2008)
  • J. Polich

    Updating P300: An integrative theory of P3a and P3b

    Clinical Neurophysiology

    (2007)
  • J. Polich et al.

    P300 from a single auditory stimulus

    Electroencephalography and Clinical Neurophysiology – Evoked Potentials

    (1994)
  • A.M. Proverbio et al.

    Gender and parental status affect the visual cortical response to infant facial expression

    Neuropsychologia

    (2006)
  • S. Righi et al.

    Fearful expressions enhance recognition memory: Electrophysiological evidence

    Acta Psychologica (Amst)

    (2012)
  • B. Rossion et al.

    Spatio-temporal localization of the face inversion effect: An event-related potentials study

    Biological Psychology

    (1999)
  • B. Rossion et al.

    Early lateralization and orientation tuning for face, word and object processing in the visual cortex

    NeuroImage

    (2003)
  • B. Rozenkrants et al.

    Affective ERP processing in a visual oddball task: Arousal, valence and gender

    Clinical Neurophysiology

    (2008)
  • E. Seifritz et al.

    Differential sex-independent amygdala response to infant crying and laughing in parents versus nonparents

    Biological Psychiatry

    (2003)
  • M.E. Smith et al.

    The intracranial topography of the P3 event-related potential elicited during auditory oddball

    Electroencephalography and Clinical Neurophysiology

    (1990)
  • G. Spangler et al.

    The specificity of infant emotional expression for emotion perception

    International Journal of Psychophysiology

    (2001)
  • M.J. Taylor

    Non-spatial attentional effects on P1

    Clinical Neurophysiology

    (2002)
  • C. Vico et al.

    Affective processing of loved faces: Contributions from peripheral and central electrophysiology

    Neuropsychologia

    (2010)
  • D.G. Wastell

    On the correlated nature of evoked brain activity: Biophysical and statistical considerations

    Biological Psychology

    (1981)
  • N. Wild-Wall et al.

    Interaction of facial expressions and familiarity: ERP evidence

    Biological Psychology

    (2008)
  • E.L. Wilding

    In what way does the parietal ERP old/new effect index recollection?

    International Journal of Psychophysiology

    (2000)
  • G. Yovel et al.

    The neural basis of the butcher-on-the-bus phenomenon: When a face seems familiar but is not remembered

    NeuroImage

    (2004)
  • J.S. Abramowitz et al.

    Obsessional thoughts in postpartum females and their partners: Content, severity and relationship with depression

    Journal of Clinical Psychology in Medical Settings

    (2003)
  • Cited by (44)

    • Processing children's faces in the parental brain: A meta-analysis of ERP studies

      2022, Neuroscience and Biobehavioral Reviews
      Citation Excerpt :

      Enhanced responses at these later components could reflect increased attention allocation to these motivationally significant stimuli. Regarding the role of face familiarity, while many studies only compared own child faces to unfamiliar child faces (Bornstein et al., 2013; Doi and Shinohara, 2012a, 2012b; Weisman et al., 2012) some studies have included a familiarization process to previously unknown child pictures to obtain a control condition of familiar children’s faces, making it possible to dissociate own child and familiarity effects. The findings indicate that the enhanced LPP response to own child is not explained by a familiarity effect, since LPP responses were found to be larger to own child compared to familiar child faces (Bernard et al., 2018; Bick et al., 2013; Grasso et al., 2009; Kuzava and Bernard, 2018).

    • The maternal brain: Neural responses to infants in mothers with and without mood disorder

      2019, Neuroscience and Biobehavioral Reviews
      Citation Excerpt :

      Mothers consistently experienced more positive emotions and/or higher arousal when seeing their own vs. unknown infants (Barrett et al., 2012; Doi and Shinohara, 2012; Minagawa-Kawai et al., 2009; Noriuchi et al., 2008; Strathearn and Kim, 2013; Strathearn et al., 2008; Wonch et al., 2016). One study of facial expression recognition found no differences in accuracy of own vs. unknown infant facial emotion recognition (Doi and Shinohara, 2012). Six of the 13 studies investigated associations between ratings or task and neural response to own vs. unknown infant faces.

    • Latent profiles of maternal neural response to infant emotional stimuli: Associations with maternal sensitivity

      2019, Biological Psychology
      Citation Excerpt :

      ERP studies investigating maternal processing of infant emotional expressions commonly examine the early face-sensitive N170 component, a negative-going deflection occurring approximately 170 ms after stimulus presentation; the early positive-going P200 component, which peaks approximately 200 ms after stimulus presentation and reflects non face-specific early visual attention; and the P300 and late positive potential (LPP) components, both gradual positive deflections beginning around 300 ms, which reflect sustained attention to emotionally relevant stimuli. Several studies have documented increased N170, P200, and LPP amplitudes to negative stimuli compared to neutral/positive stimuli, broadly (Carretié, Mercado, Tapia, & Hinojosa, 2001; Eimer & Holmes, 2006; Krombholz, Schaefer, & Boucsein, 2007), and infant distress expressions compared to neutral/happy expressions, specifically (Bernard et al., 2015; Doi & Shinohara, 2012; Proverbio et al., 2006; Rodrigo et al., 2011), although effects vary across components and across studies. Together, the N170, P200, and LPP reflect structural encoding, early attention allocation, and sustained elaborative processing relevant to emotional faces.

    View all citing articles on Scopus
    View full text