Attachment and early brain development – neuroprotective interventions in infant–caregiver therapy

REVIEW ARTICLE

Attachment and early brain development – neuroprotective interventions in infant–caregiver therapy

Louise Newman1,2*, Carmel Sivaratnam1,2 and Angela Komiti1,2

1Department of Psychiatry, The University of Melbourne, Parkville, VIC, Australia, and 2Centre for Women’s Mental Health, The Royal Women’s Hospital, Parkville, VIC, Australia

Abstract

Infancy is a critical developmental period involving establishment of the neurological underpinnings of psychological, affective and relational functioning. The integration of findings from developmental and attachment theories and neurodevelopment has contributed to greater understanding of the significance of early relationships and the developmental impact of interactional disturbance. This paper provides an overview of this framework and the implications for infant–caregiver interventions in high-risk dyads.

Keywords: Attachment; Neurodevelopment; Infancy; Early Intervention

Citation: Translational Developmental Psychiatry 2015, 3: 28647 - http://dx.doi.org/10.3402/tdp.v3.28647

Copyright: © 2015 Louise Newman et al. This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International License, permitting all non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Received: 25 May 2015; Revised: 1 November 2015; Accepted: 2 November 2015; Published: 21 December 2015

Competing interests and funding: There is no conflict of interest in the present study for any of the authors.

*Correspondence to: Louise Newman, Department of Psychiatry, The University of Melbourne, Parkville, VIC 3052, Australia;
Centre for Women’s Mental Health, The Royal Women’s Hospital, Locked Bag 300, Cnr Grattan St & Flemington Rd, Parkville, VIC 3052, Australia, Email: Louise.Newman@thewomens.org.au

 

Infancy, specifically the period between 0 and 3 years of age, is increasingly being conceptualised as a time of rapid and significant brain growth, facilitating the development of core neurodevelopmental capacities underlying later psychological and emotional wellbeing (1). Environmental influences in infancy, particularly the quality of the caregiver–infant relationship and emotional interactions within this context, have been purported to shape neurological, psychological and social development and have potential long-term effects on psychological and emotional functioning (2).

The infant brain develops within an interpersonal context, where structural and functional networks are shaped by the nature and quality of early caregiver–infant interactions. This ‘experience-dependent’ nature of brain development has consistently been illustrated in studies of groups of children who were exposed to early aberrant, caregiving environments. For instance, early disruptions to early caregiver–child relationships have been found to result in alterations of particular brain regions implicated in emotional regulation (3, 4).

Psychoanalytic developmental theories and attachment theory as described initially by Bowlby (57) have long stressed the significance of the infant’s relationship with the primary caregiver for ongoing development. Some accounts indeed argue that experiences in infancy are determinant of adult personality and psychosocial functioning, minimising both the role of biological disposition and that of later experience. The question of infant determinacy has been widely debated without resolution with some authors (8) arguing that innate factors, such as temperament, are much more influential than environmental factors in shaping adult personality. Polarised views, ranging from the social determinist to the biological determinist, have presented simplistic models of infant development.

Recent models have moved towards the incorporation of neurodevelopmental, biological and psychosocial approaches to human development. Consequently, there has been a significant conceptual shift, where social experience is currently seen to play a role in shaping the biology and genetic programming of human development, rather than the simple ‘unfolding’ of a predetermined sequence of developmental stages. In the case of human infants, developmental models need to account for the increasingly recognised contribution of the infant to the social environment and their capacity to interact with and shape environmental responses. The ‘transactional model’ of development (9) proposes an ongoing interactional process between the child and social experience which consequently shapes development, where the child is able to influence environmental responses, and both child and the social environment use regulatory mechanisms (10).

Attachment theory proposes an integrative framework of human development, where development occurs in the context of early relationships, which provide security and comfort. The attachment system is seen to be an innate, homeostatic system which regulates proximity-seeking and contact-maintaining behaviours beginning in infancy (5, 7, 11). The infant’s need for comfort has consistently been found to be a central need in both human and animal research. Early deprivation of comfort and security has been found to have adverse sequelae on a broad range of domains, including neurological, psychological, emotional and physical development and functioning (1215). Early disruptions to the attachment system have been found to influence subsequent caregiving behaviour in adulthood, highlighting the salient role of early experience in informing relational functioning across development (7).

According to Bowlby, repeated and consistent interactional patterns between the infant and caregiver result in the formation of ‘internal working models’ or representations of relationships. Conceptually, this is a similar notion to the ‘internal object’ of psychoanalysis and the ‘schema’ of cognitive psychology. It describes the development of patterns of ideas, feelings, and expectations about close relationships and the self, in addition to the individual’s characteristic ways of managing anxiety in relationships. In this way, Bowlby can be seen as providing an account of development of the personality and a model of the way in which early relationship experiences influence adult relationship functioning (16). At the time of this formulation, however, little was understood about the central role of early interaction in contributing to affect the regulation or the neurological basis of relational functioning.

The development of approaches to the measurement of individual differences in attachment behaviour in infants, and later in adults, has prompted the development of a body of research looking at continuities between infant and adult attachment status, and at factors contributing to both secure and insecure attachment in infancy and their developmental significance. In light of findings of the effects of early stress on brain development, the exploration of attachment theory has moved from an initial focus on patterns of typical development to attachment in groups with disrupted or poor early caregiver–child interactions (17, 18). Given the empirical and theoretical notion that attuned and responsive care promotes optimal brain development, there is an increasing body of research exploring links between early caregiving and subsequent neurological development.

The infant is dependent on the carer for stress and emotional regulation, and to modulate their overall level of neurophysiological arousal. The impact of lack of early regulation and high levels of stress is potentially widespread and includes epigenetic effects, with impacts on emerging stress regulatory mechanisms as well as on attachment organisation (4, 19). Current studies suggest that stressful early environments contribute to physiological dysregulation of an individual’s stress regulation systems, particularly the hypothalamus–pituitary–adrenal (HPA) axis (4, 20). Further investigations on the role of caregiver–child interactions on neurophysiological systems will enable more holistic assessment and intervention in clinical settings of children with disrupted or poor early care.

Main (21) pointed to the emerging interest in distortions of early experiences (such as insecure attachment relationships, insensitive interactions, neglect and trauma) and their potential impact on development. Attachment Theory, which remains the ‘dominant theory of human contingency in international developmental psychology’ (22), has been extended since Bowlby’s (7) initial formulation to produce a more integrative model of the impact of early care on development including neuroscience data on the development of affective responses and regulation in dyadic relationships (23).

The emergence of the field of developmental psychopathology in the 1990s represents the expansion of both attachment theory and neurodevelopmental models into more complex modelling of mental disorders taking into consideration risk and protective factors influencing the onset and trajectory of psychopathology. The field focuses on both the impact of disorder on development and the way in which disorder is related to developmental stage or processes. It has prompted significant theoretical literature examining the antecedents and developmental factors contributing to a range of mental disorders including schizophrenia, mood disorders, neuropsychiatric disorders and personality disorders. In addition, it underscores the need for research on early risk factors and close examination of the infant’s caregiving context. The existing empirical data examining the risk for developmental psychopathology have, to date, focussed on the effects of broad developmental processes (e.g. self-regulation, memory functioning, social interaction) and caregiver mental disorder (e.g. maternal depression) on infant development.

Attachment Theory has more recently moved to develop models of risk and vulnerability in early relationships. It has examined transgenerational transmission of attachment difficulties, specifically, associations between caregiver mental disorder and unresolved traumatic attachment issues, as well as the quality of interaction with the infant (24). Unresolved traumatic attachment issues are seen to impact on caregiver cognitions, affects, and emotional interaction with the infant. Caregiver reflective capacity, or the caregiver’s ability to understand the mental states communicated by the infant, has been found to be influenced by their own early attachment experiences. Aberrant infant–caregiver emotional interactions, such as unempathetic or insensitive responses to the infant’s mental states, may reflect traumatic caregiving histories of the caregivers themselves (25, 26). The neurobiology of caregiving disturbance may also reflect the impact of early maltreatment and distorted interaction on brain systems involved in care and interaction with the infant (27).

Despite the significance of this framework in highlighting the pattern of repetition of dysfunctional relational interactions and caregiving difficulties, there has been little investigation on the influence of attachment histories of ‘high-risk’ caregivers, on their experiences of caregiving, and on their interactions with their infants. Further, there is little research examining caregiver–child emotional interactions in this group of caregivers and the impact of distorted interactions on neurological and psychological development. Available studies describing insensitive and non-contingent interactions between high-risk caregivers and infants are largely descriptive and cross-sectional. Consequently, there is a need for longitudinal studies to further delineate caregiving difficulties faced by vulnerable caregivers and consequently to extend the current understanding of the predictors of infant development. This understanding will be vital in developing specific neuroprotective interventions focusing on emotional interaction and regulation.

In clinical practice, it is common to see intergenerational transmission of disturbed interactions and patterns of relationships, where many vulnerable caregivers have had a history of past trauma. The re-enactment of the caregiver’s own trauma in the relationship with their child is a crucial dynamic to identify and, importantly, presents a potential window of opportunity for intervention and prevention. Early identification of caregivers at risk of traumatising interactions with their children is a core strategy in the prevention of emotional and psychological difficulties in children. This phenomenon also raises issues as to the ‘brain programming’ of caregiving behaviour and the neurological basis of caregiving disturbance.

Study of the neurodevelopmental trajectory of individuals with histories of maltreatment and trauma has described both structural and functional brain differences from groups who have not experienced trauma. Studies have looked at both children who have experienced adversity and adult populations reporting abuse and/or neglect as children. De Bellis et al. (28) first described brain changes in abused children including decreased intracranial and cerebral volumes and smaller corpus callosum. Dysregulation of stress-response systems, specifically the HPA axis, has been a consistent finding across child and adult populations reporting early maltreatment, comprising abuse and/or neglect (29, 30). These findings overall suggest that impaired caregiving and trauma, particularly during crucial early brain development, may have long-term consequences on neurodevelopment and increase the risk of psychopathology (31). Interventions aimed at improving the quality of early emotional regulation and attachment, while taking into consideration trauma resolution, are arguably neuroprotective and a high priority in terms of modifying the potential negative impact of early stress.

Attachment and early caregiving relationships

The quality of early care of the infant has long been seen as central to infant development and later socio-emotional functioning. Freud described the infant’s relationship with the mother (primary caregiver) as the first love relationship and prototype for later relationships. Similarly, Bowlby (7) elaborated the notion of the primary caregiver as a ‘secure base’ – a secure position from which the infant explores the world – and described this relationship as influencing the development of ‘inner working models’, or representations, of the self, other, and relationships. The inner working model in turn influences perception, cognition, and affect about relationships, and forms the basis for ongoing patterns of relating or attachment. Attachment Theory has developed a classification of attachment status in adults, which emphasises the organisation of thinking, feeling, and memory around attachment issues and the way in which different attachment styles represent adaptational or defensive strategies to manage anxieties about significant attachment relationships. Within this framework, caregiving style and the quality of interaction between caregiver and infant will also reflect the caregiver’s attachment status and attachment history. Caregivers will recapitulate or re-enact early attachment experiences with their own infants. In this way, Attachment Theory has focussed on the ‘transgenerational transmission’ of attachment styles. A body of research provides support for the overall hypothesis that the caregiver’s state of mind with respect to attachment and representation or model of the relationship with the infant is predictive of infant attachment status (32, 33).

Research in the field of Attachment Theory gained impetus with the development of the Ainsworth Strange Situation Procedure (SSP), a structured laboratory assessment and classification method which allows classification of infant attachment at 12 months of age (11). The development of attachment classification systems and the Adult Attachment Interview (AAI) (34), a semi-structured clinical interview for attachment assessment, prompted a body of research looking at caregiver influences on infant attachment and the transmission of attachment patterns from caregiver to child. Early studies by Ainsworth and Wittig (11, 35) examined the relationship between infant attachment behaviour observed during the SSP and home-based observations of infant and caregiver.

Ainsworth described patterns of secure and insecure attachment and related these to patterns of emotional interaction between infant and carer. Observable categories of infant attachment behaviour (secure, avoidant, and ambivalent) represent strategies developed by the infant for managing anxiety about the availability of the primary carer, and for regulating their own emotional state. As described by Ainsworth et al. securely attached infants use the mother as a secure base for exploration and, although distressed by separation, are comforted by the mother’s return. In home observation, the mothers of secure infants were described as sensitively responsive to the infant’s signals and consistently psychologically available.

Ainsworth stressed the role of maternal sensitivity to the infant’s signals in determining the quality of the early attachment relationship and saw ‘sensitivity’ as a dyadic concept (35) involving maternal behavioural response to infant initiative. A study of maternal responsiveness to infant crying (36) found that responsive mothers who consistently interacted with their crying infants in the first 6 months of life tended to be overall more responsive to infant communication and to have more settled infants later in the first year. Maternal sensitivity, acceptance, and accessibility were related to infant attachment classifications in the strange situation. Whilst the concept of ‘sensitivity’ is broad, it may be seen as involving capacity to attend to and interpret infant affective communication as well as responding to this in a way which modulates the infants state of anxiety or overall arousal. In this model, caregiver functioning impacts the infant overall affective and stress regulation with implications for emerging neurological capacity.

The clinical importance of early disturbances of interaction emerged with the finding of ‘disorganised’ attachment defined over 20 years after Ainsworth’s initial classification. Main and Solomon (37) described a group of infants, previously thought to be secure in relationship to the carer, as exhibiting confused, frightened, and contradictory behaviours in relation to the caregiver. It was hypothesised that these infants experienced contradictory feelings towards the attachment figure, both fear and the desire to approach, resulting in high stress and a state of unresolvable conflict.

Disorganised attachment has become the category of attachment behaviours of most interest to clinicians due to its clear association with ongoing developmental and psychological disorders. Unlike the broad category of attachment insecurity, disorganisation is said to represent a ‘collapse’ or failure to develop coherent strategies for the management of stress relating to caregivers and for emotional regulation overall. Disorganisation in infancy is associated with a range of developmental problems in the pre-school period and school years including aggressive behaviour, poor peer relations, internalising problems, and cognitive immaturity (38). Disorganised attachment strategies in infancy are found in up to 24% of disadvantaged, low socio-economic status samples with significant stability over time (39). Disorganisation increases with family risk factors including child abuse, caregiver major depression, and caregiver alcohol abuse. In maltreatment samples comprising individuals with documented abuse, rates of disorganisation range from 55 to 82% (40, 41).

Individuals with disorganised attachments tend to possess difficulties with self-organisation and representation in the context of interpersonal relationships, and in understanding the emotions of themselves and others (42). On a neurobiological level, disorganisation is seen as a state of dysregulating anxiety and limited ability to modulate affective experience in the absence of an organised relationship with a carer who functions to organise the infant’s experience. Disorganised relationships and resultant, unresolvable anxiety for the infant are arguably important targets for clinical intervention with a focus on improving affective regulation. Van Ijzendoorn et al. (39) stress the unresolvable nature of the dilemma for the disorganised child:

Disorganised behaviours are considered to be indicative of an experience of stress and anxiety which the child cannot resolve because the caregiver is at the same time the source of fright as well as the only potential haven of safety. In the face of this paradoxical situation the infants’ organised strategy is expected to fall apart.

Lyons-Ruth et al. (43) have examined Main and Solomon’s (37) hypothesis and argue that factors in addition to frightening/frightened behaviours may be involved in caregiver disorganising behaviours. Firstly, they argue that caregivers themselves may display contradictory caregiving strategies and secondly, that caregiver failure to regulate the infant’s overall level of fear may be more important than specific behaviours in the prediction of infant disorganisation.

Main and Hesse (41) described caregiver behaviour in disorganised attachment relationships as either frightening for the infant or showing signs of fear in the caregiver, where the caregiver’s unresolved loss or trauma is seen to influence their interaction with and perceptions of the infant (44). Unresolved trauma refers to experiences and memories that have yet to be integrated into the individual’s consciousness, and which have an ongoing dysregulating effect on the individual’s mental states. In the AAI (34), the presence of unresolved trauma is identified by ‘lapses’ in the monitoring of reasoning or discourse when discussing trauma (also known as metacognitive monitoring) (21). The caregiver with anxiety about the infant may be avoidant or poorly interactive or seek comfort from the infant. These behaviours are related to the caregivers’ own early fearful experiences in close relationships and are confusing and inexplicable to the infant. Hesse and Main (44) suggest that the infant experiences high levels of anxiety in these situations where the primary carer is confusing and does not provide feelings of security. The carer is at once an attachment figure and also a figure of fear. This may result in ongoing high levels of stress which is essentially unresolvable, with potential impacts on neurodevelopmental processes, for instance, HPA axis dysregulation (29). There is little available research in human infants, however, that examines relationships between specific patterns of disturbed infant–caregiver communication, stress reactivity and later disorganisation of attachment. There may be differential effects, for example, of caregiver avoidance or neglect and caregiver intrusion, on HPA axis development (45).

Maternal behaviours indicating insensitivity and misattunement to the specific content of the infant’s attachment-related communications predict infant disorganisation (21). These include disturbances in affective communication between caregiver and infant, negative and intrusive caregiver behaviour, caregiver disorientation and withdrawal. Lyons-Ruth et al. (43) noted that while caregiver affective communication errors were strongly related to infant disorganisation, mothers of babies showing predominantly approach behaviours (disorganised–secure) tended to demonstrate a contradictory mix of intrusive and role confused interactions with their infants, while mothers of infants showing an avoidant/resistant pattern (disorganised–insecure) were seen to be more withdrawn and fearful. The mothers’ interactional styles were termed ‘hostile’ and ‘helpless’, respectively, and have been conceptualised as alternate reflections of the mothers’ own early attachment trauma. Lyons-Ruth et al. in this way provides an elaboration of Main and Hesse’s (41) ‘frightened/frightening’ model of caregiving implicated in attachment disorganisation.

In a meta-analysis of 12 studies, Van Ijzendoorn et al. (39) found an average effect size of r=.29 looking at the relationship between disorganisation and externalising disorders (such as conduct disorder), suggesting that more than one developmental pathway is likely to be involved. There are likely to be differences between subtypes of disorganised attachments and complex mediating variables involved. Green and Goldwyn (38, p. 840) correctly comment that ‘there is insufficient research as to whether the disorganisation seen in infancy behaviours may reflect more general behavioural disorganisation, and in later years it is uncertain how much the disorganisation and “bizarreness” in children’s mental states may relate to more general behavioural and cognitive disorganisation’. Despite the lack of clarity surrounding the concept of disorganisation in later childhood and the overlap with established attachment disorders during this period (38), the consensus regarding early attachment disorganisation in infancy is that it represents a state of unresolvable high stress and may have an immediate negative impact on the development of affect regulation, control of stress responses, and overall socioemotional development. The significance of these findings for later development, let alone for the development of specific forms of psychopathology, remains unclear.

From the perspective of the study of early disturbances of caregiving behaviour and experiences, the prevailing theoretical model of the ‘disorganising’ caregiver proposed by Hesse and Main (44) remains where the caregiver with unresolved loss or trauma ‘transmits’ this to the infant via specific interactional patterns. As noted above, this is likely to be a complex association and is not accounted for solely by ‘frightening/frightened’ caregiver behaviour. Factors such as the social context of early caregiving, the caregiver’s experience of the self in the caregiving role, and variations in emotional availability to the infant are all likely to be contributory to the overall quality of interaction between caregiver and infant. The caregiver’s representation of the child (46) is also important. This concept includes the caregiver’s thinking about the child as an individual with an evolving personality, desires, intentions, and capacity to experience and communicate affective experiences.

Overall, there is a strong association between caregiver ‘state of mind’ with respect to attachment, as measured on the AAI, and corresponding infant attachment status. Van Ijzendoorn et al.’s (47) meta-analysis of 14 studies found a large average effect size (>1). Overall, 77% of autonomous adult had secure infants, 57% of dismissing adults had avoidant infants, and 21% of preoccupied adults had resistant infants. A major difficulty for attachment research is to account for the ‘transmission’ of attachment status from caregiver to child and to describe the way in which caregiver attachment status presumably influences caregiving behaviour. Van Ijzendoorn et al. examined those studies which provided data on caregiving behaviour. Only 23% of the association between caregiver and infant attachment was attributed to maternal sensitivity, seen as a major mediating variable. In other words, the link between caregiver state of mind with respect to attachment and infant attachment status is stronger than the links for the hypothesised processes that are said to connect them. This has become known as the ‘transmission gap’, and contemporary attachment theorists are concerned to describe the complex processes involved. Current research suggests that caregiver’s experience of the child, self-perception as caregiver, and representation of the child are all likely to influence caregiving behaviour and quality of emotional interaction.

Early caregiving disturbances

Infants, from birth, are neurologically primed for social communication and interaction within the context of the primary caregiving relationship (4, 22). Infants engage in a range of ‘signalling’ behaviours in order to seek and maintain social contact with caregivers, including making eye contact, mimicking facial expressions, and signalling affective states (e.g. crying), which serve to elicit responses from the caregiver (7, 36). Within healthy caregiver–child relationships, it is known that the caregiver is able to recognise and appropriately respond to the infant’s communicative signals in order to regulate or modulate their emotional states. The caregiver is seen as an ‘external psychobiological regulator’ of the infant’s state of arousal (48). The caregiver’s capacity to respond to the infant’s signals in an attuned and sensitive manner has been found to play an integral role in mediating broader infant development across a wide range of domains, including cognitive development and sociability. Organisation of behaviour in infancy is seen by contemporary infant research as primarily the property of the caregiver–infant system (49).

Interactional patterns within the caregiver–infant relationship include both how the infant ‘self-regulates’ or attempts to modulate arousal and interactive regulation (50). These patterns are known to form the basis of the attachment relationship and subsequent patterns of interaction, where the dynamics of both the child’s and the caregiver’s interactions influence the other’s responses to continuously shape the formation of the attachment relationship, as the infant develops representations of expected interactional sequences (51). This notion is in line with the ‘transactional’ model of development (9), which purports that infant development is shaped by the ongoing, continuous interaction between the infant and social environment. The infant has innate social capacities and thereby influences caregiver behaviour. Infant research has more recently begun to explore the organisation of dyadic interactive processes between infant and caregiver, alongside explorations of the link between these early patterns and subsequent development.

From birth, an infant is able to recognise and show a preference for the mother’s voice compared to a stranger’s, distinguishes his/her own mother’s smell, and prefers the mother’s face (48). ‘Preference’ in these studies refers to a statistically significant bias in response to stimulus presentation. These innate capacities shape social communication and the development of early understanding of relationships with the responsive social environment.

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 (52). The caregiver’s apparent emotional state influences that of the infant, whereby the infant tends to mimic the emotional expression of the caregiver. Infants have been found to show a preference for a ‘happy’ facial expression as compared to one of anger. The ‘Still Face’ paradigm (53) is an experimental paradigm used to investigate the infants’ response to maternal level of engagement and responsivity. As part of this paradigm, mothers were instructed to maintain an affectless facial expression after a 2-min period of face-to-face play with their infants. Infants were found to exhibit signs of distress and confusion when there was a lack of maternal response and eventually disengaged from the interaction. Similarly, Tronick and Cohn (52) 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. Manipulation of maternal responsiveness has demonstrated infant sensitivity to both the timing and quality of interaction (14).

Current knowledge on the subsequent effects of early relational disturbances have largely stemmed from the study of face-to-face interactions between caregivers with psychiatric conditions and their infants. Murray (14) initially found that depressed mothers were poorly interactive across normal and still-face interactions on the Still-Face paradigm. Infants of withdrawn, depressed mothers have been found to demonstrate protest and distress, while infants of intrusive, depressed mothers tend to be avoidant and often gaze-averting (54). While the Still-Face paradigm is widely used to study the influence of maternal mental health on interactions with infants, it remains unclear whether a lack of maternal responsiveness is pervasive in mother–infant interactions across disorders, or whether this is specifically characteristic of depressive withdrawal.

Depressed mothers tend to be more likely to perceive the infant’s behaviour as problematic or negative (55), suggesting that caregiving perceptions and beliefs may mediate the nature of the developing attachment relationship. Accordingly, maternal depression has been found to be a factor influencing increased rates of attachment insecurity (56). The strongest effects have been found in mothers with Bipolar Disorder (18), with up to 50% of infants found to be disorganised (57).

Stern’s (51) concept of ‘affect attunement’ highlights the salient role of caregiver sensitivity to fluctuations in the infant’s arousal and mental states, encompassing caregiver matching of the infant’s emotional states, as well as the caregivers’ capacity to accurately interpret and respond to the infant’s emotional states. Early communicative disturbances such as misinterpretations or unempathetic responses to the infant’s signals have been found to disrupt the infant’s experience of self-monitoring and communication and linked to the subsequent development of infant psychological disorders, specifically attachment disorders and relationship difficulties, as well as adult personality and interpersonal dysfunction.

In extending the work of Stern, based on their work with split-screen videotaping and microanalysis of face-to-face interactional sequences with 3- to 4-month-old infants, Beebe and Lachmann (50) propose that interactions between the infant and caregiver are ‘co-constructed’, where both parties monitor their own behaviour and that of the other party. Time-series analysis, which is a statistical method used to measure bidirectional regulation, has been used as a method of tracking interactional processes involved in caregiving, including the sharing of affective states. Using this method, Beebe and Lachmann (50) found that vocal rhythms between caregiver and infant are coordinated, with rapid tracking and response to vocalisations by both parties. While there tends to be a balance of self and interactive regulation in secure dyads, with an optimal or ‘midrange’ degree of tracking of the partner, both extremes of high and low tracking characterise insecure attachment relationships, indicating either self-preoccupation or preoccupation with the interaction, respectively. Schore (58) argues that in functional relationships a process of ‘reattunement’ occurs in which the caregiver has the capacity to modulate the quality of interaction in a way which is responsive to the infant’s emotional communication and signals and is able to re-establish synchronous interaction.

In disturbed early interactions, the infant tends to be exposed to chronic aberrant caregiver responses with the corresponding high levels of relational stress and negative affect (22). Preliminary studies of emotional processing of infant communication in mothers with histories of early relational trauma find core difficulties in interpretation and negative attributional bias, which may be a possible mechanism involved in early relational missattunement (59). When the attachment system does not function to regulate the infant’s emotional states, it has been found that there is a subsequent disruption to the development neurological structures and networks involved in self-regulation and the processing of emotionally salient information (60).

Neurobiology of early caregiving disturbances

The increasing breadth of findings relating to the neurobiological implications of early attachment is beginning to drive a more focused exploration of the factors informing early assessments and interventions in children with disturbed early caregiving experiences (4, 61, 62).

Imaging studies suggest that structural and functional abnormalities in cortical and sub-cortical regions may contribute to subsequent deficits in affect-regulation in children and adults exposed to early relational trauma or maltreatment from abusive or neglectful caregiving (63). Children who experience abuse and/or neglect are likely to endure long periods of intense negative affect on their own, without support and scaffolding to regulate their emotional states. It has been suggested that mild-to-moderate negative affective experiences interfere with right hemisphere processing to the point where cell death occurs in the hypermetabolic right brain (64), after which the brain switches into hypoarousal to allow for cell survival (65).

A PET study investigating brain activation in post-institutionalised Romanian children found relatively lower metabolism in a network of areas involved in stress regulation, including the orbito-frontal cortex (66). Event-related potential studies such as that of Pollak and Sinha (15) have provided further support for cortical hypoactivation in maltreated children when viewing emotional facial expressions of familiar and unfamiliar individuals. It has been suggested that the hypoactivation of right-hemisphere frontal, medial temporal, and limbic structures involved in emotion regulation hinders the integration and connectivity between these regions in children with attachment-related trauma (60). Connections between the orbitofrontal cortex and the limbic system have been found to play a major role in the selection and active inhibition of emotional responses (67). Chugani et al. (66) found decreased activation in the network of areas involved in stress regulation in maltreated children, including the orbitofrontal cortex, a finding which has been supported consistently by the work of Schore looking at the relationship between attachment-related trauma and brain development (60, 65).

Another consistent finding is that of reduced overall corpus callosum volumes in children and adults with histories of abuse or neglect, particularly in the middle and posterior regions (13, 68), where aberrant inter-hemispheric interactions have also been implicated in emotional recognition, expression, and arousal impairments in other groups with emotion-processing difficulties such as schizophrenia (69). Moreover, decreased cerebellar volumes have consistently been found in children who have experienced early maltreatment (3, 70).

Dysregulation of the HPA axis has also been implicated in impaired stress regulation in maltreated populations, where feedback loops regulating glucocorticoid hormones are disrupted by consistently unpredictable or adverse attachment interactions (29), resulting in the individual becoming highly sensitive to stress (30). The consequent high allostatic load placed on the individual from prolonged periods of acute stress has been found to increase vulnerability to later psychiatric conditions, such as mood and anxiety disorders (20, 71). Furthermore, both human and animal studies have linked maternal stress during pregnancy to increased basal HPA axis activity and regulatory difficulties across the developmental trajectory of the offspring, alongside behavioural, social, and cognitive impairments (72, 73).

Further compounding notions of heightened stress sensitivity and negative attributional biases in maltreated populations, children with histories of abuse and/or neglect have been commonly found to demonstrate enhanced attention and sensitivity to negative emotions, in particular anger and sadness, over a range of both positive and negative emotions displayed (74, 75). Studies have also found that maltreated children require less sensory input than typically developing children to recognise anger (76).

In light of current knowledge on the impact of early attachment trauma on brain development across a broad range of developmental domains, the comprehensive assessment and exploration of the dynamics of attachment relationships has become especially salient in the conceptualisation of targeted and effective interventions. The next section provides an overview of existing assessment models of attachment.

Implications for assessment

Assessment of caregiving capacity and emotional interaction involves both understanding of the caregiver’s attachment history and reflective capacity and direct observation of infant–caregiver interactions and attachment behaviours. It includes exploring caregiver representations of the child and the capacity to acknowledge the psychological separateness of the child, as well as their ability to provide emotional care and support for individual development. The impaired capacity of the caregiver to think about the child’s emotional world, known as caregiver reflective capacity (77), is a key indicator of risk. Absent or low reflective capacity has been linked to aberrant caregiving behaviours including withdrawal, hostility, and intrusive interaction (33). Further, low reflective capacity has been implicated as a significant mediating factor between maternal substance abuse and poor child outcomes (78).

It is also important to assess the impact of the caregiver’s, particularly the mother’s, unevolved and unresolved early trauma and mental state with respect to attachment, and the manner in which this impacts the relationship and interaction with the infant. There are a number of tools that are useful in this regard including evaluation of caregiver attachment status, reflective capacity, and direct observational measures of caregiver–infant interaction.

The AAI (34) is useful for assessing parental unresolved trauma and attachment issues. The Working Model of the Child Interview (79), which has good face validity and is similar to the AAI, is commonly used to explore caregivers’ views of their infant. Assessing the mental status of the child is useful in providing insights into the child’s experience of possible abuse and/or neglect, and the impact of these experiences on the child’s perceptions of self, other, and relationships. Further, mental status assessments may shed light on the presence of generalised attachment difficulties, anxiety, and post-traumatic stress disorder.

The use of established coding systems such as the Emotional Availability Scales (80) with video-recordings of free-play provides valuable information about caregiver attunement. Observational measures such as the Strange Situation Paradigm (35) and the Cassidy–Marvin procedure (81) are useful in establishing attachment status. For the younger child, observational assessment of infant–caregiver intervention provides detail about affective regulation within the context of the primary attachment relationship and the capacity of the caregiver to ‘read’, monitor, and respond to the infant’s social communication in a way which is containing of infant anxiety and validates infant experience. Whilst rating of the quality of interaction is complex, several approaches focus on mutual engagement, caregiver support for interaction, and overall affective tone (82).

Implications for early intervention

Intervention for disturbed infant–caregiver relationships is a key strategy for promotion of development and prevention of longitudinal developmental disruption. The significance of early relational trauma and stress in the infant developmental period is increasingly recognised as establishing vulnerability to the range of mental disorders. There is an increasing body of research suggesting that effective early intervention for disturbed infant–caregiver relationships should operate on a range of levels, including neurobiological and psychosocial domains, with implications for broader outcomes of stress regulation capacity and resilience (4, 22, 83). Consequently, psychological interventions that function to address these domains can be conceptualised as neuroprotective. Early intervention is possible if we are able to identify and target those infants and children at high risk on the basis of caregiver vulnerability – specifically, a caregiver with a background of maltreatment, abuse, or personality difficulties should be a high priority for early intervention services. A review of animal and human brain networks underlying caregiving by Swain et al. (84) suggests that adequate caregiving involves the integration of neural circuitry underlying emotion, empathy, and motivation, as well as cognitive faculties such as attention and decision-making. Consequently, impairments across these domains in caregivers who may have experienced early adversity have tangible implications for the care of their infants. It is therefore important for interventions to take into consideration caregiver histories when addressing the quality of caregiver–child interactions, for instance, focusing on improving and promoting the caregiver’s capacity for empathic understanding of the infant.

Psychodynamic approaches are based on the basic idea that the caregiver must come to understand the particular ways in which their own past influences the current interaction with their infant (85). For the traumatised caregiver, the core clinical issue often is how to reintegrate traumatised experiences and associated feelings. Some caregivers with backgrounds of attachment-related trauma will respond to techniques aimed at controlling anger and affect, encouraging more adaptive ways of managing negative affect states, and improving tolerance of negative infant affective states. Other caregivers will need more intense individual therapy which can focus of resolving past trauma.

Caregiver reflective capacity is crucial for infant development. The reflective caregiver has the capacity to think about or reflect on the inner world of the infant and support the infant in emerging self-regulation (77). It may be argued that the majority of infant–caregiver psychotherapy approaches aim to improve caregiver reflective capacity and focus on making connections between the traumatised caregiver’s own early difficulties and the present issues in their relationship with the child. Slade (77) describes the core components of a reflective caregiving program as 1) developing a reflective stance, 2) modelling reflections – clinician represents the child to the caregiver in terms of mental states, 3) facilitating wondering – supporting the caregiver to imagine the child’s experience, and 4) using affect as a means to mentalisation – using emotional states as entry into thinking about responses.

All these processes are based around a clinician who supports the caregiver and reflects back the caregiver’s emotions, fears, and distress in a containing way. This is particularly important with traumatised mothers who have had little validation of their own experiences in childhood and may have ongoing difficulties in trust and attachment. Reflective caregiving programs may be crucial to effecting change in high-risk relationships where behavioural/cognitive approaches are ineffective. Supporting the caregiver’s capacity to understand and regulate feelings and support to ‘tell the story’ of their own trauma is central to this process.

Several clinical approaches explicitly focusing on caregiving and attachment have been reported in the literature: the Circle of Security approach (82), Watch, Wait and Wonder (WWW) (86), and Video Interaction Guidance provide a framework for improving caregivers’ understanding of the child’s attachment needs. Programs vary in the use of direct interactional work with the infant and caregiver and therefore the extent to which they may be described as ‘working at the level of emotional regulation’. In the WWW approach, caregivers are instructed to observe their children engaging in self-directed play and to participate only when this participation is initiated by the child. The therapist subsequently discusses the session with the caregiver, in order to facilitate the development of the caregiver’s awareness and understanding of relational themes emerging from the child’s play. The WWW approach has been found to assist the child in developing a more organised or secure attachment, in addition to increasing the caregiver’s sense of competence and improving both maternal and infant mental health (86).

A further issue that requires some consideration is whether individual psychotherapy for the caregiver needs to precede caregiver–infant dyadic therapy. Given that caregivers experiencing the impact of early relational trauma may have core difficulties in conceptualising the self and the other in relationships, they may be unable to reflect on the caregiving of their own infant without first resolving issues of their own caregiving. Further research is required to examine the representation of the infant in caregivers with early trauma and disturbances of early interaction (87, 88).

To date, caregiving interventions aimed at high-risk populations have primarily been behavioural in nature, with the addition of psychoeducation about attachment behaviours and the role of the attachment figure in some cases. However, emerging research has indicated that attachment-based approaches with an emphasis on improving the emotional quality of caregiver–infant relationships are not only optimal for child development but may also operate at the level of support for neurobiological organisation and for emerging systems of interpersonal functioning and regulation. Existing caregiver-based interventions aimed at improving the caregiver’s capacity to recognise and appropriately respond to infants’ and young children’s signals of distress have been found to promote improved regulation of HPA axis functioning and behavioural functioning in groups exposed to early adversity (61, 62, 89). More complex current understandings of the impact of early life stress on HPA axis functioning and risk of mental disorder further highlight the neuroprotective function of early emotion-focused attachment interventions in promoting resilience through the regulation of stress response systems (89, 90).

Conclusion and future directions

Current neurobiological evidence suggests that targeted early intervention has the potential to mitigate the long-term negative outcomes related to adverse early experiences. Nevertheless, little has been done to delineate the specific mechanisms of change in interventions aimed at improving emotional interaction, as well as in the understanding of factors influencing resilience in groups with adverse early caregiving histories. Consequently, the evaluation of targeted interventions for infants at risk of developmental psychopathology remains a key priority. While addressing the caregiver’s own attachment difficulties, providing caregiver psychoeducation, reducing caregiver stress, and enhancing mentalisation capacity appear to influence positive infant–caregiver interactions, there are as yet many aspects of therapeutic interventions that are poorly understood. There are significant challenges for both clinicians and researchers in developing methodologies that allow for a comprehensive evaluation of intervention approaches and particularly the longitudinal outcomes of intervention provided in the critical developmental period of infancy. Given current knowledge on the influence of early attachment on brain development, it is vital that the formulation of early intervention models take into account the neurobiological correlates of early interactions. The integration of attachment models and neurobiology is in many ways in the early stages of translational work, which will allow greater elaboration of interactional approaches as neuroprotective interventions.

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About The Authors

Louise Newman
Centre for Women’s Mental Health, The Royal Women’s Hospital, Parkville, VIC 3052, Australia Department of Psychiatry, The University of Melbourne, Parkville, VIC 3052, Australia
Australia

Carmel Sivaratnam
Centre for Women’s Mental Health, The Royal Women’s Hospital, Parkville, VIC 3052, Australia Department of Psychiatry, The University of Melbourne, Parkville, VIC 3052, Australia
Australia

Angela Komiti
Department of Psychiatry, The University of Melbourne, Parkville, VIC 3052, Australia Centre for Women’s Mental Health, The Royal Women’s Hospital, Parkville, VIC 3052, Australia
Australia

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