The Neurobiology of Parenting Disturbance —
the Study of Early Interactional Disturbance in High-risk Parents

Louise Newman, MD, Monash University Centre for Developmental Psychiatry & Psychology

Parenting is a complex phenomenon including inter-related behaviors, beliefs, attitudes and interpretation of infant cues and communication. The human infant has a range of communicative capacities and the neural programming to enter into social relationships from birth. The response of the caretaking environment directly shapes infant neurobiological and psychological development. Disturbances of early parenting, including 'misreading' infant cues are highly significant indicators of potential risks and may result from parental neurobiological factors. The study of parenting at a neurobiological level may help in the understanding of parenting disturbance and lead to the development of more specific interventions for high-risk groups.
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Introduction

Experiences in infancy, particularly the quality of caregiving relationships and socio-emotional interaction, are increasingly recognized as 'foundational' – that is, forming the basis of development in neurological, psychological and social domains (Schore 1994, Siegal 1999). From a neurodevelopmental viewpoint, infancy (0-3 years) represents the period of most rapid brain growth across the lifespan with the establishment of neural pathways and networks underlying basic neuropsychological functions such as learning, memory, attention and the processing and regulation of emotional states. These capacities are central to later psychological and emotional health.

Neurodevelopmental and infant research over the last 20 years has been examining the interpersonal context of infant brain development — the way in which experience influences neuronal functioning and brain architecture. The quality of emotional interaction and input the infant brain receives is held to directly affect neural activation and synaptogenesis, a process described as the 'experience–dependent' nature of brain development (Siegel, 2000). Parenting, a constellation of caregiving behaviors, interactions, affects and beliefs is a complex, multiply- determined phenomenon of fundamental importance to early development. It involves biological, psychosocial and cultural components and there are diverse accounts of its evolution.

There is also increasing interest in the integration of neurodevelopmental, biological and psychosocial developmental models. The genetic programming of human development is seen as being shaped by social experience. Infants also interact with and shape environmental responses. Sameroff (1993) describes a 'transactional model' of development in which the development of the infant is seen as the product of an ongoing interaction between the child and social experience. The child has the capacity to influence environmental responses, and both child and the social environment employ complex regulatory mechanisms.

Attachment theory stresses the importance of early relationships and the need for security and comfort. Early work by Harlow (1958) in non-human primates, for example, demonstrated very clearly the significance of infants' need for comfort, overriding even the need for food. Both Bowlby and Harlow noted the implications of early deprivation of care and separation from caretakers on adult functioning, and subsequently on later parenting behaviour, challenging the notion that parenting behavior is 'instinctual' and stressing the role of early experience in providing models for behavior within relationships.

Attachment Theory, which initially focused on the delineation of patterns of normal development, has moved to the examination of attachment dynamics in clinical groups and in disturbed early infant-parent interactions. In this way, it reflects current concerns within developmental neurobiology about the effects of early stress on brain development (Heim, Meinlscmidt & Nemeroff, 2003; Perry, 1995) and the contribution of infant research to the understanding of normal and disturbed infant-parent relationships. These developments raise the importance of the concept of 'trauma' in the infant period and in particular, the mechanisms by which early trauma may contribute to broad disruptions of developmental processes such as those presumably involved in such complex forms of psychopathology as the personality disorders.

Recent infant research has focused on the influence of caregiving quality on neuropsychological development with the overarching hypothesis that optimal brain development is promoted by sensitive and responsive care (Schore, 2000).

Attachment Theory has also moved to examine populations at risk of developmental and mental disorder. Research has focussed on a model of 'transgenerational transmission' of attachment insecurity (Holmes, 1999) in which the parental 'state of mind' with respect to attachment and unresolved traumatic attachment issues are seen to impact on parental cognitions, affects and interaction with the infant. Infant experience and attachment to the parent will reflect the quality of interaction, which in turn reflects the parents own early experiences. In this way, observable parental emotional interaction with the infant is said to in part reflect the adults' memories and history of being parented (Winnicott, 1960; Stern, 1985). In situations of disturbed infant-parent interaction, traumatic themes from the past of the parent are hypothesized to negatively impact on the parents thinking about, and interaction with the infant. Issues from the attachment history of the parent are the 'ghosts in the nursery' which disrupt the emerging attachment relationship with the infant (Fraiberg et al., 1975).

This framework has been significant in thinking about the repetition of dysfunctional relationship patterns (such as child abuse and disturbances of attachment) across generations and has broadened the understanding of early difficulties in parenting and influenced approaches to intervention (Baradon et al., 2005). At the present time there is little research looking specifically at 'high risk' parents and their interactions with their infants or experiences as parents which relates these to attachment history. In many ways this appears to be the next necessary step in broadening the understanding of issues for vulnerable parents and of early risk factors for infant development.

The ongoing work outlined here aims to study mothers with histories of early trauma from the perspective of their attachment status, parenting self-concept, and interaction with their infants. Mothers with a clinical diagnosis of Borderline Personality Disorder (BPD) have been chosen as a group experiencing long-term difficulties related to childhood adversity such as abuse and neglect. Further this work is now moving to examine the neurobiological underpinning of observed difficulties in emotional interaction between this group of mothers and their infants.

Borderline Personality Disorder is a significant mental disorder characterized by disturbances of identity, emotional dysregulation and impaired interpersonal functioning. Emotional dysregulation is seen as a core dimension of BPD and is characterised by emotional reactivity and inability to modulate emotional responses (Wagner & Linehan, 1999). Similarly, BPD is seen as characterized by difficulties in sustaining attachment relationships and maintaining appropriate boundaries in close relationships. The majority of etiological models focus on the role of early disturbances in the caretaking environment and maltreatment as key impact on cognitive and emotional development (Judd & McGloshan, 2003), although there is increasing interest in examining the neurodevelopmental implications of early trauma.

BPD is a high prevalence condition with estimated community prevalence of 2% (Swartz et al. 1990). This is a group known to be over represented in studies of abusive, depressed and poorly functioning parents (Levy, 2005) yet there are minimal data available on their specific experiences and interaction with their children. Studies of the interactions between mothers with BPD and their infants find high rates of infant attachment disorganization, which is of significance to overall development (Newman, et al. papers).

From the perspective of Attachment Theory, disorganization represents a state of breakdown or failure to develop a coherent strategy to regulate anxiety and emotional behavior with the caretaker. This will have potential significant effects on the emerging capacity to understand emotions in the self and other and on self-organization and representation (Fonagy, Gergely, Jurist & Target, 2000).

Looking at disorganized infants overall, Lyons-Ruth has described communication errors related to infant disorganization. Mothers of infants with disorganized-insecure classifications showed a contradictory mix of intrusive and role confused interactions with their infants. A second group of mothers of disorganized-secure infants were more withdrawn and fearful and were termed 'helpless-fearful regarding attachment' (Lyons-Ruth and Spielman, 2004). The 'hostile' and 'helpless' profiles are seen as alternate reflections of the mothers' own history of attachment-related trauma.

Main and Hesse (1990) argued that unresolved loss or trauma influences the parent's interaction with and thinking about the infant and results in frightening or frightened behaviors. The infant experiences unresolvable fear and confusion leading to disorganization of the attachment strategy. 'Unresolved' trauma in this model refers to memories and experiences that have not been integrated into consciousness or self narrative, and which continue to exert a dysregulating effect on mental life.

Disorganization in infancy is associated with a range of developmental problems in the pre-school period and school years including aggressive behavior, poor peer-relations, internalizing problems and cognitive immaturity.

Early Parenting Disturbances
Infants have complex inborn capacities for social interaction and social learning. Infant researchers have described the infant as 'primed' for social interaction from birth and described the ways in which the infant seeks social contact — such as making eye contact, mimicry of facial expressions, signalling of affective states — which elicit responses in potential caregivers. These 'signalling' behaviors result in communicative and emotional interactions which form the 'building blocks' of the attachment relationship. In healthy relationships the carer has the capacity to recognize and respond to the infant's communication and can respond in such a way that the infant's affective state is modulated and contained.

The primary caretaker and infant develop coordinated interactional patterns in which the caretaker functions to regulate or modulate infant arousal and affective state. The caregiver acts as an 'external psychobiological regulator' of the infants' level of arousal and the emerging attachment relationship functions to regulate affect (Sroufe, 1995, Trevarthen 1984). Both partners in the relationship influence the other and continually 'restructure' the quality of and intensity of interaction.

In early parenting, caregiver capacity to respond in a sensitive position to infant signals has been recognized as central in mediating infant cognitive and linguistic development and sociability. More recently studies of interactive processes between infant and caregiver have examined the organization of dyadic interaction and the possible significance of these early patterns for ongoing development (Beebe et al., 2005). Interaction patterns are defined as the characteristic ways in which caregiver and infant influence each other during an interaction. These patterns include both, how the infant 'self-regulates' or attempts to modulate arousal, and interactive regulation.

A body of research supports the overall hypothesis that the quality of early interaction between infant and caregiver (in the first year of life) provides the basis for patterns of interaction as the child develops representation of expected interactional sequences (Stern, 1977; 1985).

From birth, the infant can discriminate his/her mother's voice and shows preference for it, compared to a stranger's, and prefers the mother's face (Field & Fogle, 1982). There is also empirical evidence that infants have the capacity to perceive contingencies (associations between infant behavior and outcome), and that infants as young as 3-5 months of age develop expectations and have the memory capacity to recall these for around 24 hours.

Infant research suggests that infants are particularly sensitive to the affective state of the caregiver and have early and accurate capacities to both signal and 'read' emotional states (Tronick et al., 1986). The emotional state of the infant is influenced in a direct way by the caregivers' emotional displays. Infants show preference for a 'joy' face as opposed to an 'anger' face and tend to 'match' or mimic the emotional expression of the caregiver (Field et al., 1982). Tronick and colleagues (1978) developed the 'Still Face' paradigm as a way of investigating the infants' response to maternal level of responsivity. After a two-minute period of face-to-face play, mothers were instructed to maintain a non-responsive, affectless face. Infants initially signal the desire to communicate and receive a response, are surprised and perturbed, and eventually disengage from the mother. Trevarthen (1984) found a similar infant response of distressed disengagement when using videotape feedback to the infant, maternal response was mistimed. Tronick (1989) found that infants exposed to aberrant maternal emotional expression showed a negative mood and avoided eye contact for several minutes after resumption of normal interaction. It also appears that infants develop characteristic styles of managing the stress of the still-face experience, which are linked to attachment status at 12 months. Those infants who persist in attempts to elicit a response from the mother are more likely to be secure, while those who do not attempt to engage the mother are more likely to be insecurely attached. This suggests that secure infants have learned from experience that signalling to the mother generally elicits a response, and this becomes incorporated into the infant's representation of the relationship.

The intense study of face-to-face interactions between infant and caregiver has been the focus of most recent work attempting to describe early relational disturbance and has allowed hypotheses to develop about the pathogenic nature of these disturbances. Initial work by Field (1984) found that depressed mothers were poorly interactive in both normal and still-face interactions. While a large number of studies have used the Still Face paradigm to study maternal disorders that may affect interaction with infants, it is not clear that the main feature of maternal lack of response to infant affect characterizes maternal disorders other than depressive withdrawal.

Overall, maternal depression has been related to higher rates of insecure attachment in several studies (Radke-Yarrow et al., 1985) with strongest effects found in mothers with Bipolar Disorder, with up to 50% of infants found to be disorganized (DeMulder & Radke-Yarrow, 1991). Early studies also highlighted the possible mediating role of parenting perceptions and beliefs, finding that depressed mothers are more likely to perceive the infant's behavior as problematic or negative (Rickard et al,. 1981). There is unlikely to be a simple linear relationship between parental mental state, parenting beliefs and interactional behavior, as again demographic and contextual factors are significant.

Beebe & Lachmann (2002) describe the use of split-screen videotaping and microanalysis of face-to-face interactional sequences with infants three to four months of age. Time-series analysis, a statistical method for assessing bidirectional regulation, provides a model of the way in which interactions are 'co-constructed'. The infant and caregiver monitor both their own behavior, and that of the partner. This method provides an estimate of the caregiver's effect on the infant, and the infant's effect on the mother during the sequence. This approach has been useful in allowing close tracking of the processes of normative, sensitive parenting and particularly, the way in which affective states are 'shared' and amplified in the dyad. Similarly, vocal rhythms between caregiver and infant have been found to be coordinated, with rapid tracking and response to vocalizations by both parties. Beebe and Lachmann suggest that in well-functioning dyads, there is a balance of self and interactive regulation, with an optimal or 'midrange' degree of tracking of the partner. Insecure attachment is likely to be associated with both extremes of low and high tracking, representing either self-preoccupation, or preoccupation with the interaction, respectively.

This work follows from and builds on Stern's (1985) description of 'affect attunement' between infant and caregiver and the central role of parental sensitivity to the fluctuations in the infant's states of arousal. Attunement for Stern involves parental matching of the infant's feeling state, and the parents' capacity to interpret, respond and convey emotional resonance with the infant. Stern suggests that the parent who misinterprets or responds unempathically towards the infant, disrupts the infant's experience and risks the infant experiencing a breakdown of communication and self-monitoring. This notion of early communicative disturbance is seen as significant in several accounts of the development of infant psychological disorders, particularly later attachment disorders and relationship difficulties (Beebe et al. 2005), as well as adult personality and relationship dysfunction (Stolorow, Brandschaft & Atwood 1987; Meares, 2005). It is not clear however what degree of misattunement might be associated with later disturbance, or if misattunement per se is related to attachment disorganization.

Schore (2003) argues that the process of 'reattunement' is important here, and that the adequate caregiver is able to contain or regulate infant stress by re-establishing interactive synchrony. In healthy early relationships the caregiver has the capacity to recognize and respond to lapses in attunement. Psychopathology may arise in situations of chronic misattunement and interactive disruption, where the infant is unable to regulate high stress levels or negative affective states. Early 'relational trauma' — that is, the failure of the caregiving relationship to regulate infant stress — disrupts the development of the infants self-regulatory capacities and neurologically based capacities for affect regulation and the processing of socioemotional information. It is clear, however, that all infants will experience episodes of misattuned interactions and have the ability to recover from these. Little evidence is available as to the 'threshold' level of impaired interaction beyond which developmental harm occurs.

While interactional disturbances associated with maternal depression are well known and there is information as to their long-term developmental significance, little attention has been paid to other high-risk situations or other types of maternal disorder. Again, other than in maternal depression, little data is available on the developmental outcome of infants exposed to relational trauma. While there is likely to be a spectrum of development risk, and a variety of interactional disturbances in high-risk parenting, there is as yet no clear modelling of the pathways to attachment disturbances and psychopathology.

Osofsky & Eberhart-Wright (1988) present a typology of negative affective exchanges between adolescent mothers and infants. These mothers experienced multiple psychological risk factors in their own histories including child abuse, loss of attachment figures and ongoing relationship difficulties. No formal psychiatric diagnoses were provided.

Three negative patterns were described:

1. Blandness or Dullness — little communication between infant and caregiver ask infants sharing restricted range of affect by six months of age.
2. Angry and Negative — mother expresses frustration and anger towards the infant and the infant in turn may be angry and aggressive. This pattern is particularly evident at 20-30 months of age.
3. Mixed negative affective exchanges — mother may give contradictory communications, for example, conflict between words and facial expression. Mother and infant express conflicting emotions.

The authors comment that infants repeatedly subjected to non-reciprocal inconsistent responses from caregivers may have adverse outcomes and develop maladaptive ways of dealing with these conflicts, affecting the development of self-identity and understanding of relationships. While their work is descriptively useful and theoretically cogent, there is no further evidence as to the validity of the proposed classification.

Looking at the broad domain of parental personality functioning and infant interaction, little observational research is available, despite the fact that all major psychodynamic developmental models and Attachment Theory see parental personality as a significant variable and likely to influence parenting behaviors.

With respect to BPD, mother — infant interaction has as yet received minimal attention. Crandell, Patrick and Hobson (2003), using the Still Face Procedure, found that mothers with BPD interact with their children in an intrusively-insensitive manner and that their infants respond with 'dazed' facial expressions.

Functional MRI studies have recently been used to further investigate the involvement of several inter-related mechanisms in maternal responses to infant cues: reward-motivation pathways (Lenzi et al. 2009; Swain, et al. 2007); the processing of infant affective information (Strathearn, L. Et al. 2009, Niriuchi, et al. 2008), and the influence of mothers own attachment system and related processing capacities (Lenzi, D. Et al. 2009; Strathearn, L., et al. 2009). In these studies, researchers have aimed to examine the systems underlying maternal responsivity to infant cues- whether differences in maternal responsivity are related to how mothers themselves were parented. Such research may provide evidence that on the basis of their own early parenting experiences, people with different attachment classifications have different neurobiological organization of relevant reward and affective related structures.

Several reviews of functional neuroimaging research examining the neurological basis of human parent-infant interactions have since aimed to describe a model of parenting behavior. In their review of the literature at the time, Swain and colleagues (2007), proposed that the processing of infant cues exists within a motivation and reward feedback system centered on the cingulate cortex, coupled with complex planning, memory processing (hippocampus, parahippocampus and amygdala) and contextual social response processing. Recently, Swain and colleagues (2008) suggested that parental responses to infants involve an initial detection and organization of infant cues by the sensory cortices which then interact with subcortical memory and motivational structures for cue appraisal. When sufficient motivation is achieved, these structures are said to interact with a number of corticolimbic modules related to reflexive caring behaviors, emotion, alarm, preoccupation, and cognition and memory, in order to generate a coordinated response via activation of the motor cortex and hypothalamus.

In an important initial step in the examination of the underpinnings of sub-optimal parenting, Strathearn and colleagues (2009) compared the neurological and hormonal responses to infant cues in mothers with secure and insecure/dismissing patterns of attachment, as measured by the Adult Attachment Interview. In this study mothers with secure attachment patterns displayed higher peripheral oxytocin levels following mother-infant play interactions than mothers with insecure/dismissing attachment patterns. Further, when viewing infant facial cues while undergoing fMRI, securely attached mothers displayed greater activation in the oxytocin and dopamine related hypothalamus/pituitary regions than did insecure/dismissing mothers. These results suggest maternal attachment status, a classification related to mothers own early parenting experiences, may be related to differing neurobiological responses to infant cues. They further implicate oxytocin in mediating maternal attachment-related behaviors, perhaps heightening reward and motivation to engage in parent-child interactions. Reward processing regions were also activated when securely attached mothers viewed their own infants sad facial expressions, however insecure/dismissing mothers showed increased anterior insula activation, a pattern previously associated with negative emotional states such as pain and disgust when viewing own infants sad expressions.

The existing fMRI literature largely supports Swain et al.'s (2007) model of an interaction between corticolimbic structures associated variously with affiliation and reward in the perception and assessment of infant stimuli. The role of neurohormones such as oxytocin, and dopamine in human maternal behavior have only just begun to be explored, however evidence suggests they are pivotal in the initiation and sensitivity of maternal behaviors and that their efficacy is mediated by genetic, existing stress and environmental factors. This evidence further provides us with a framework from which to explore the neurological and hormonal correlates of abnormal parenting behaviors.

Transmission of parenting disturbance
In humans, as in animals (Maestripieri, D., et al. 2006) individuals exposed to early trauma are at an increased risk of parenting disturbances with their own children, which may involve direct repetition of patterns or types of abusive behaviors (Egeland, B. et al., 1988; Maestripieri, D. & Carroll, K.A., 1998). The transgenerational transmission of parenting disturbance appears to be complex, involving social learning, poor emotional processing abilities, as well as genetic and epigenetic effects. The transgenerational effect of disruptions of early caretaking experiences on infants have been known for some time. In a series of seminal social deprivation studies, Harlow et al. (1967) observed female primates that had been isolated as infants displayed a high rate of abuse neglect and infanticide as mothers. Maestripieri and colleagues (Maestripieri, D., et al. 2006; Maestripieri, D. 1998; Maestripieri, D., et al. 1999) built on this work to provide evidence for the perpetuation of infant abuse among first-degree offspring. In a longitudinal cross-fostering observational study, Maestripieri (2005) found that over half (56%) of primates exposed to abusive parenting practices during infancy, displayed dysfunctional maternal behaviors in adulthood. In contrast, all those reared by non-abusive mothers displayed adequate or 'good enough' parenting styles. Findings from non-human primate epidemiological studies suggest that aberrant parenting is a relatively stable characteristic, with similar inconsistent interactions repeated with subsequent infants (Maestripieri, D., et al. 1999; Maestripieri, D. & Carroll 1998; Maestripieri, D., et al. 1997). Maestripieri and colleagues (2006) further observed that the transgenerational effects of maternal abuse on stress regulation may be mediated by serotonergic mechanisms and that development of these systems may be negatively affected by exposure to neglectful parenting.

Evidence suggests that early parenting experiences may influence the development of skills necessary not only for normal infant development, but also the future capacity of that infant in their own parenting. The neurobiological development underpinning these abilities continue to be illuminated, with a notable overlap between those structures most affected by early parenting experiences and those utilized in normal parenting behaviors. However, disturbances in human parenting behaviour including neglect and abuse of children are poorly understood in terms of their neurobiological underpinnings. Studies of BPD adults suggest a series of possible neurodevelopmental effects of early trauma with ongoing affective dysregulation and deficits in socioemotional processing as key features which may relate to difficulties in parenting. Early parenting in particular, involves processing of infant social and emotional communications as well as the need to regulate strong affect and these capacities' may be impaired in parents with BPD. Further, it may be hypothesized that parents who are experiencing parenting difficulties, particularly in maintaining a positive stance towards their child may be experiencing less reward during interactions and have core issues in processing affective stimuli. Parents with BPD have fundamental difficulties in understanding and regulating their child's emotional and psychological experiences and distortions of early interactions may be related to high levels of stress and the effects of stress-related hormones on brain development as well as epigenetic effects on emerging brain functioning. This work suggests that it may be important to examine the specific patterns of neurobiological parenting difficulties in parents who have experienced significant early trauma as in BPD, and to examine neurodevelopmental sequelae in infants exposed to parenting disturbance.
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For more information about this article, please email: louise.newman@med.monash.edu.au
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