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J. Child Psychol. Psychiat. Vol. 41, No. 1, pp.
Great Ormond Street Hospital for Children, London, U.K. Developmental psychology and the study of behaviour and emotion have tended to be considered in parallel to the study of neurobiological processes. This review explores the eﬀects of child abuse and neglect on the brain, excluding nonaccidental injury that causes gross physical trauma to the brain. It commences with a background summary of the nature, context, and some deleterious eﬀects of omission and commission within child maltreatment. There is no post-maltreatment syndrome, outcomes varying with many factors including nature, duration, and interpersonal context of the maltreatment as well as the nature of later intervention. There then follows a section on environmental inﬂuences on brain development, demonstrating the dependence of the orderly process of neurodevelopment on the child’s environment. Ontogenesis, or the development of the self through self-determination, proceeds in the context of the nature–nurture interaction. As a prelude to reviewing the neurobiology of child abuse and neglect, the next section is concerned with bridging the mind and the brain. Here, neurobiological processes, including cellular, biochemical, and neurophysiological processes, are examined alongside their behavioural, cognitive, and emotional equivalents and vice versa. Child maltreatment is a potent source of stress and the stress response is therefore discussed in some detail. Evidence is outlined for the buﬀering eﬀects of a secure attachment on the stress response. The section dealing with actual eﬀects on the brain of child abuse and neglect discusses manifestations of the stress response including dysregulation of the hypothalamic-pituitary-adrenal axis, and parasympathetic and catecholamine responses. Recent evidence about reduction in brain volume following child abuse and neglect is also outlined. Some biochemical, functional, and structural changes in the brain that are not reﬂections of the stress response are observed following child maltreatment. The mechanisms bringing about these changes are less clearly understood and may well be related to early and more chronic abuse and neglect aﬀecting the process of brain development. The behavioural and emotional concomitants of their neurobiological manifestations are discussed. The importance of early intervention and attention to the chronicity of environmental adversity may indicate the need for permanent alternative caregivers, in order to preserve the development of the most vulnerable children. Keywords : Attachment, brain development, child abuse, neglect, neurobiology, stress. Abbreviations : ACTH : adrenocorticotropic hormone ; ADHD : Attention Deﬁcit Hyperactivity Disorder ; CRH : corticotropin-releasing hormone ; CSF : cerebrospinal ﬂuid ; DBH : dopamine beta hydroxylase ; ERPs : event-related potentials ; HPA : hypothalamic-pituitaryadrenal ; PTSD : post-traumatic stress disorder.
excellent work being carried out in the ﬁelds of neurobiology and developmental psychology. Rather, the challenge is for those of us working in the ﬁeld of child abuse and neglect to seek out and make connections with these important and clearly relevant sources of knowledge. It is hoped that this review will go some little way towards this endeavour.
Requests for reprints to : Danya Glaser, Department of Psychological Medicine, Great Ormond Street Hospital for Children, London WC1N 3JH, U.K. (E-mail : dglaser!ich.ucl.ac.uk).
or potentially harmful to the child. In the U.K., Signiﬁcant Harm (Adcock & White, 1998) as deﬁned in the Children Act (Department of Health, 1989) has been accepted as the threshold for recognition of child abuse and neglect. Signiﬁcant Harm relies on evidence of either ill-treatment of the child that has caused or is likely to cause signiﬁcant harm to the child, and\or impairment of the child’s health and development which is attributable to ill-treatment or to the care that the child has or has not received. The deﬁnition of child abuse and neglect includes both qualitative and quantitative aspects. It includes single events, repeated events, or a pattern of interaction that is characteristic of the relationship between the abuser, in this case often a parent or primary carer(s), and the child. Whereas physical and sexual abuse are in the nature of events, neglect and emotional abuse characterise the relationship between the carers and the child (Glaser & Prior, 1997). It is possible that event-type abuse, which is more likely to be traumatic in nature, leads to diﬀerent eﬀects on the brain than do chronic emotional neglect and abuse. Diﬀerent forms of child abuse and neglect often coexist (e.g. Claussen & Crittenden, 1991 ; Ney, Fung, & Wickett, 1994). As Manly, Cicchetti, and Barnett (1994) point out, there are many diﬀerent aspects of abuse and neglect including subtype, severity, frequency, and chronicity. The child’s particular characteristics, be they age, gender, temperament, or disability, may make her more vulnerable to particular forms of abuse or neglect. An abuser or a neglectful parent are likely to have been aﬀected adversely by their own past experiences (e.g. Harmer, Sanderson, & Mertin, 1999). Moreover, the abusing or neglecting person and the child(ren) are often living in a suboptimal social and, indeed, physical context (T. Boyce et al., 1998). There are factors working in parallel at diﬀerent levels or systems (e.g. Bronfenbrenner, 1979) that contribute to the ultimate particular form of child abuse or neglect. The child’s own attributes, the child’s family context, and aspects of the maltreatment will all contribute to the later outcome for the child.
distinguished the 14 mothers who went on to abuse their own children from the 10 mothers who had been able to break the cycle of abuse. it is necessary to summarise current knowledge about the processes of neurodevelopment in infancy and early childhood. High scores on the Dissociative Experience Scale (Bernstein & Putnam. The younger the infant. Johnson. however. mothers with a selfreported history of physical abuse responded to a video of a smiling. Emotional abuse by the mother was associated with worse selfesteem and physical abuse with marital breakdown. Schmeidler. which is itself related directly to environmental input (Thoenen. the cerebral cortex’s use of glucose rises. diﬀerentiation. not an inevitable outcome (Langeland & Dijkstra.CHILD ABUSE AND NEGLECT AND THE BRAIN 99 health problems. 1993). 1993). Widom. Egeland and Susman-Stillman (1996) have found some signiﬁcant diﬀerences between mothers who had been abused and went on to abuse their own children. McEwen. Further work on the relationship between childhood abuse and later sensitivity to a child’s emotions shows that. which communicate with each other by sending out ‘‘ messages ’’ from extensions of the cell body called axons and receiving ‘‘ messages ’’ into extensions called dendrites. Mann. This is a paradoxical ﬁnding that requires further exploration but which indicates an insensitivity and lack of attunement to infants’ emotional cues in mothers who had a history of childhood physical abuse. A history of childhood maltreatment in a parent’s own past is now recognised as one important risk factor in the abuse of children (e. Questions remain. & Cohen. Thus. 1994) and hippocampal neurons in animals. rather than to the absence of maltreatment during childhood (Main. exceptions include the olfactory region (Huttenlocher. the growth spurt continuing to 24 months (Schore.g. adult eating disorders were more commonly found following reported childhood emotional and sexual abuse. infant with physiological arousal. However. 1990). the determination of which synaptic connections will "Neurons are nerve cells. A history of sexual and emotional abuse by a male caregiver was associated with sexual diﬃculties in adulthood. & Leﬀ. 1985). The remainder of this review will explore ways in which the developing brain responds to the external stimuli of the child’s environment. Brain Growth and Maturation For obvious reasons. 1994). about neurobiological mechanisms by which abuse and neglect become linked with behavioural and emotional impair- ment. in contrast to mothers who had an uneventful childhood. Southwick. associations have been shown between a history of childhood physical and sexual abuse and adult psychopathology (e. Nixon. & Charney. et al. 1997). there can be little doubt of its potential for adverse eﬀects on the developing child. although increasing knowledge is being gained about human development. 1997). Environmental Inﬂuences on Brain Development The process of early brain development is constantly modiﬁed by environmental inﬂuences. 1995). Childhood abuse as a risk factor for parenting. reaching more than twice the glucose usage of adults’ brain and continuing thus until the age of 10 years (Chugani. diﬀerent forms of childhood abuse were found to be associated with diﬀerent adult psychopathology as well as personal and social problems. found on the PSE (Present State Examination) (Wing. Swett. These latter mothers were able to talk about their past abuse in a coherent and integrated fashion. much of the work on the development of the brain has been carried out in animals. & Milner. During the ﬁrst 2 years of life. but not a crying. . dendrites. Most of the brain’s neurons are formed and migrate to their assigned position during embryonic and early postnatal life. Neurotrophins are chemicals of central importance to the regulation of the survival. in a caudal to rostral direction (Nelson & Bloom. Domanic. During this period of plasticity. Kaplan. In order to consider these eﬀects. 1994). There are clear similarities here with ﬁndings from adults’ attachment status on the Adult Attachment Interview (George. 1998). Child abuse and neglect constitute one aspect of these environmental inﬂuences. & Main. Kahana. as well as attempts at psychological ‘‘ escape ’’ including early abuse of drugs and alcohol and attempts at self-harm. The authors caution against an exclusive emphasis on sexual abuse. in particular child abuse and neglect. the more these environmental factors are mediated by the primary caregiver(s). 1989). From birth to 4 years of age. however. 1995). The human brain grows from an average weight of 400 gm at birth to 1000 gm at 12 months. However. not all the synaptic connections survive. The synthesis and secretion of neurotrophins is dependent on. in which security of attachment is positively related to the coherence of the adult’s account of their own childhood. 1990). many being subsequently ‘‘ pruned ’’ due to lack of use (Singer. The volume of the human brain increases more during the ﬁrst year of life than at any other time in life (Gilles. and maintenance of function of neurons in the brain. idealised and inconsistent accounts of their childhoods. In psychiatric patients. This process is genetically determined. and regulated by. & Fuchs. Galea. McCanne. It proceeds from lower to higher brain centres.g. and overproduction of axons. which enabled then to reﬂect on their style of parenting their own children. Similarly. Yehuda. To a limited extent. Surrey. and synapses in diﬀerent regions of the brain". Synaptogenesis is the creation of synapses. The stepwise sequence of neurodevelopment is genetically predetermined and not alterable by environmental forces. 1977) to be in the depressive and anxiety areas. 1986). including primates. as measured by increased skin conductance (Casanova. This is. from the brain stem to the cerebral cortex. there is sequential growth. The axon-dendrite point of communication is termed a synapse. Despite the methodological weaknesses in some of the research on the eﬀects of child abuse and neglect. 1995). or potential for change. which continue to be formed in adult life (Gould. and those who did not. (1995) have shown that early trauma predisposes adults to suﬀer PTSD following traumatic event experiences in adulthood. A higher incidence of post-traumatic stress disorder (PTSD) in Vietnam veterans has been shown to be associated with a history of childhood physical abuse (Bremner. which present the maturing child’s brain with experiences that will crucially—and potentially adversely—aﬀect the child’s future development and functioning. Tanapat. prodigious proliferation. Yehuda. neuronal activity.
Both groups of authors found that these experience-dependent responses in the hippocampus enhance the survival of new neurons that had already been generated. More recent work has shown that in rodents. irreversible structural and functional changes are produced in the brain’s visual cortex. (2) details of the particular body system whose structure and functioning are aﬀected during the sensitive period . 1982). & Shors. being dependent on information received by the brain. rats reared for 30 days after weaning. repetitive. and neurohormonal secretions and their receptors. development is actually reliant on environmental inﬂuences. In humans. Irreversible reduction in visual acuity (amblyopia) occurs if an eye is deprived of visual input due to. Hubel and Wiesel (1979) showed that by temporarily blocking the visual input to one eye of a cat during a critical period of development. fail to reach the appropriate brain area. the respective issues of interest here are (1) both positive and undesirable\noxious social and interpersonal interactions provided by the primary caregiving environment . sensitive periods could be conceived of as a brief opening of a window (Bateson. Descriptively. The absence of these interactions with the infant would be unusual and contributes to the elimination of synaptic connections. contribute to the varied outcomes and developmental complications of early detrimental experiences (Kandel & Jessel. 1985). profoundly deaf children do not continue to vocalise in later infancy (Scarr. of need. Greenough and Black further suggest that these early experiences have been selected through the process of evolution and are expected to occur reliably in the particular species and at a particular time in development. 1993) presumably because species-typical auditory experiences. Reeves. Tanapat. 1991). The predetermined sequences of expected experiences allow for an orderly process of synaptic connections. As far as the human infant is concerned. Here too. 1979). 1979) of vulnerability. each with their own timetable for critical periods of maturation. Although generally applied to stages of early development.g. and (3) description of the nature of the actual change. leading to permanent impairment of vision in that eye. 1998). (3) the actual changes considered include synaptic connections. In experiments now regarded as classical.100 D. To quote Courchesne. for instance. A competitive process operates. Bornstein (1989) points out that the study of sensitive periods has in the past often focused on associating an experience with an observed change. and Townsend (1994) ‘‘ neurons that ﬁre together. The complex interconnections between diﬀerent areas of the brain. Davidson (1994) raises the possibility that during an experience-dependent period of plasticity. environmental inputs actively contribute to brain structure. they can also occur later in life. GLASER persist is environmentally regulated. nurturing. In turn. which vary between individuals. responsive gaze. a cataract or a squint beyond the age of 8–10 years (Taylor & Taylor. which are required for the development of language. Applying Bornstein’s terms to child development. Kuhn. exposure of the young child to particular aﬀective interactions could lead to pre-frontal asymmetric structural and enduring changes in the brain that . & Gage. that is. Synaptic connections that are not utilised gradually disappear. Greenough and Black (1992) distinguish between two aspects of this environmentally dependent maturational process of the brain. typical and expectable environmental factors and circumstances are themselves species-speciﬁc. which is postulated to be a consequence of that experience. (2) the particular body system under consideration here is the brain . The progressive neuronal maturation and the establishment of synaptic connections are reﬂected in changes in the infant’s increasing functional maturity. Experience-expectant development has been especially well studied in animals’ visual cortex (e. Beylin. Chisum. Neglect and failure of environmental stimulation during critical periods of brain development may lead to permanent deﬁcits in cognitive abilities. For instance. each stage building and depending on the establishment of the previous one. presumably evolved to ensure the stability of development. The other aspect of brain maturation has been termed experience-dependent by Greenough and Black. In humans. This species-typical development is genetically deter- mined and its organisation is designed to buﬀer the developing brain in a regulatory and orderly development in the face of a variety of environmental inﬂuences (Bjorklund. Bornstein suggests that an understanding of sensitive periods needs also to include (1) deﬁnition of the pathway by which the experience brings about change during the sensitive period . wire together ’’. predictable. development that will not happen unless a particular experience occurs during its critical period. They describe one aspect as experience-expectant. for instance. Although certain experiences are essential for orderly brain development to proceed. for instance in animals (but not humans) at the point when maternal responsiveness needs to develop towards her young. They include the handling of young infants. 1999). 1997). Sensitive Periods During early brain development there are sensitive periods during which particular experiences aﬀect brain maturation. In this early phase. in group complex environments were found to have 20–25 % more synapses per neuron in the upper visual cortex than rats reared socially or individually in standard cages (Turner & Greenough. Similar ﬁndings have been reported in adult rats trained in hippocampus-dependent tasks (Gould. the occurrences of some noxious experiences will cause harm to the developing organism. The competition is. 1997). rather than stimulating their production. Experience-dependent processes generate new synapses in response to the environmentally determined experiences. nor are synapses anticipating the experiences at any particular stage. gradual and attuned to the infant’s or child’s developmental stage ’’ (Perry & Pollard. and talking to the infant. determining which neurons and neural connections will survive. but unlike the experience-expectant process. The overproduction of synapses tends to be found in situations in which a source of information can be relied upon to guide the elimination of unused synapses. here the experiences are not predetermined. Wiesel. and also of opportunity. for potential binding sites on the receiving neuron. Sensitive periods have been observed to exist in the development of many diﬀerent animals as well as in humans. new stimuli are expected to be presented in a way which is ‘‘ safe. neurogenesis continues throughout adult life in the dentate gyrus of the hippocampus. Mice exposed to an enriched environment were found to have more new neurones in the dentate gyrus of the hippocampus than control mice (Kempermann.
Ontogenesis Ontogenesis. with the notion of ontogenesis allowing for the modiﬁcation of the process by the contribution and adjustment of the individual child (Cicchetti & Tucker. The . 1994). a process that may be more or less adequately accomplished. Whatever the contribution of ontogenesis. it has been possible to demonstrate that in humans. and to direct and focus the infant’s attention. to later adaptation. The sensitive caregiver’s role is to modulate the infant’s arousal. at diﬀerent ages early in the child’s life (Thatcher. 1994). whereas others are insensitive. showing that the maternal regulation includes both physiological and behavioural modulation of the pups (Hofer. This is necessary in order for the caregiver to regulate the aﬀect. from the end of the ﬁrst year. and with regulating responses to emotionally arousing situations. This is related to the secure base that Bowlby. Maturation is associated with decreased structural responsivity in the brain to new information (Tucker. Development therefore constitutes more than the resultant of the interaction between nature and nurture. it equally prolongs the vulnerability for the developing child’s brain. 1997). Hofer has detailed the interactions between the pups and their mothers. the course of human development is far more protracted and includes neotony. Although the processes of plasticity enable the brain’s structure and function to continue to be modulated in response to environmental input and the organism’s needs. 1994). intrusive. described as a biologically determined ‘‘ environment of evolutionary adaptedness ’’ (Bowlby. which could also follow intense displeasure.. free of anxiety. brain stem dopaminergic ﬁbres are activated. One aspect of early child abuse and neglect is the absence of these sensitive interactions between the parent(s) and the young child. 1992) or to injury. which trigger high levels of endogenous opiates. and sometimes angry (Cohn & Tronick. In the absence of experiences of external modulation of aﬀect. With increasing age. as well as with aﬀect inhibition (de Haan et al. or at an early stage of the critical period of neural development than to attempt to alleviate the later eﬀects. there is evidence that plasticity in the adult brain is limited. critical periods are proportionally longer. 1994). 1998). While this allows for a longer period of plasticity and maximal learning capacity. Neural Plasticity The process of neural plasticity in response to learning and the acquisition of new memories continues throughout childhood and into adulthood. and McGuﬃn (1994) have written. and behaviour of the young infant. and require help in learning to plan their actions. These endorphins are biochemically responsible for the pleasurable aspects of social interaction and social aﬀect and are related to attachment (Schore. in a probabilistic way. The nature of the resolution of developmental tasks and challenges. environmental factors to human development. extending into the second year of life in the frontal lobes. or the retention of embryonic or juvenile characteristics by retardation of development (Bjorklund. fear.CHILD ABUSE AND NEGLECT AND THE BRAIN 101 would carry signiﬁcant consequences for later behaviour and aﬀect. it is far more eﬀective to address adverse risk factors or actual illtreatment before. Some depressed mothers are withdrawn and disengaged in their interactions with their infants. Synaptogenesis and pruning occur in functionally diﬀerentiated neural systems at their respective periods of maturation. Using this means. Animal studies clearly indicate that recovery may be limited if treatment for the precipitating causes of the abnormal or unanticipated neural activity is Regulation of Infants’ Aﬀect and Arousal An important aspect of the primary caregivers’ interaction with the developing infant is to respond sensitively to the infant by gauging their emotion accurately. 1969). Using rat pups in the ﬁrst days of life. The pleasurable arousal also activates the sympathetic nervous system. development of these executive functions requires the maturation of the frontal lobes. Ontogenesis is conceptually located between two other interacting inﬂuences that determine the direction of development. 1994). Young infants have not developed the capacity to regulate their own level of arousal and impulses. and more global aspects of behaviour such as the regulation of goal-directed behaviour in time. arousal. Synaptogenesis can be visualised by its active utilisation of glucose on PET (positron emission tomography) scanning (Chugani. Such deﬁcits may only become apparent later. which is deﬁned as the development of the self through self-regulation. These areas are concerned with reasoning and abstract thought. by calming the infant and restoring her or him to a tolerable emotional state (van der Kolk & Fisler. or frustration. In some areas of the brain. namely the child’s genetic endowment and the environment. object (and person) constancy are an example of what Greenough and Black (1992) term an expected experience. This orderly development is dependent on appropriate input and sensitive interaction with the primary caregivers at the sensitive period. to help the infant deal with frustration. 1989). They point out that the genetic studies of human behavioural dimensions and disorders provide the best available evidence for the importance of nonheritable. 1996). In the brain of the infant who sees the responsive mother’s face. part of the process of ontogenesis. 1987). In contrast to animals. The early mother–infant interaction is thus a biobehavioural system. Owen. when the child is expected to have matured for that particular task and these deﬁcits may then become manifest by aggression or hypervigilance. the balance between plasticity and stability is progressively weighted towards the latter. The frontal lobes are involved with the expression and self-regulation of emotion including the inhibition of automatic or habitual emotional responses. the infant brain is unable to learn self-regulation of aﬀect. are unable to obtain their own gratiﬁcation. They point to the importance of an historical analysis in understanding the complex process of the brain’s self-organising system. In this area of development. maturation occurs more slowly and later than in other areas. in his conceptualisation of attachment. will determine what is integrated into the brain’s structure and contributes. These individual experiences that contribute to brain development are an example of the nonshared environment about which Plomin. no longer leading to structural changes and operating mainly by regulating the eﬃcacy of certain connections between neurons (Singer. is an active process in development.
& Wall. positron emission tomography (PET) uses small amounts of injected radioactive-labelled glucose or oxygen to measure the degree of glucose or oxygen metabolism at speciﬁc sites in the brain. activating the latter. by the use of a variety of neurophysiological measures and brain-imaging techniques# (for the latter..102 D. from nuclei in the medulla (Aston-Jones et al. see review by Nelson & Bloom. Dopamine cell bodies are present in the substantia nigra and ventral tegmental areas of the midbrain . noradrenergic cell bodies occur in the locus coeruleus and the lateral tegmental areas of the brain stem . and Pliszka (1992). Dopamine is thus involved in approach. stimulates receptors in the vagus nerve (part of the autonomic nervous system). 1994). 1969). produced as part of the stress response.. fear. punishment. the child constructs internal working models of self and parent (Bowlby. and repeated bids for a response to their attachment needs. 1993). it is evident that the relationship between observed behaviour and measured physiological function is complex. The biogenic amine systems are hypothesised to operate in balance with each other in their regulatory functions (Rogeness. 1987). others commence from a psychological perspective. & Pliszka. since they are particularly involved in the regulation of several human behavioural systems which. There are well-validated measures of the nature of infants’ and young children’s attachment status. It is. messages are sent to the noradrenalineproducing locus coeruleus (LeDoux. in turn.. cold. The child seeks to get closer to the attachment ﬁgure (parent or primary carer) on the assumption that the parent will be able to reduce the discomfort and restore the child’s equanimity. indicating activity at those speciﬁc areas . which suggested that these behavioural systems are mediated by neurotransmitters (Gray. 1992). There are diﬀerent ways by which neurotransmitter secretions become activated. which ends in the nucleus of the solitary tract in the brain stem. 1997). On the basis of the nature of the mother’s or the primary caregiver(s)’ responses to the infant’s inevitable. 1982. and biochemical processes in the brain and the autonomic nervous system. Bridging the Mind and the Brain Until recently. Blehar. It is suggested (Rogeness et al. 1992) that noradrenaline and serotonin are involved in the mediation of behavioural inhibition in the face of lack of reward. serotogenic cell bodies are located in the midline raphe regions of the pons and upper brain stem. functional magnetic resonance imaging (fMRI) identiﬁes active areas of the brain by their use of oxygen. Attachment security is measured in infancy and early childhood by the Strange Situation Test (Ainsworth. There are some neurobiological correlates of attachment security. Of these. Javors. From there. escape. and it is likely that the biogenic amines are involved in regulating the function of higher brain centres. Attachment Attachment is considered here since it is a fundamental aspect of child development and is aﬀected by child abuse and neglect. GLASER oﬀered after the closure of the critical period when neuronal ‘‘ misconstruction ’’ is completed (Courchesne et al. in this section a variety of neurobiological equivalents of observed behaviours. Biogenic Amines There are more than 30 neurotransmitters$ in the central nervous system. which yields a secure category (B). normal. the latter is concerned with the study of cellular. Dopamine is postulated to mediate the behavioural facilitatory system. There has been further ampliﬁcation of Gray’s work on behavioural facilitatory and behavioural inhibitory systems. or hunger. While some begin from a neurobiological point of view. discreet periods of time . which are of relevance to the ﬁeld of child abuse and neglect. which leads to the conversion of oxygenated to deoxygenated haemoglobin . Whereas the former is concerned with the observation and measurement of behaviour. cognition. help to regulate the interaction between the organism and its environment. which begins to be formed in the middle of the ﬁrst year of life. 1988). including pain. Javors. when he or she senses discomfort of any sort. These two neurotransmitters are therefore involved in regulating dopamine dependent behaviour. These methods are enabling the apparent mind–brain dichotomy to be bridged. For details about the activity of neurotransmitters at a synapse see Rogeness. developmental psychology and neurobiology have been studied in parallel. and emotion. 1996). However. and it has also been shown to inﬂuence the infant’s response to stress. and psychological processes will be discussed. and active avoidance as well as in predatory aggression (Quay. Rogeness and McClure (1996) have reviewed their own and others’ empirical ﬁndings about the functions of these neurotransmitters in regulating behaviour and emotions and about possible early environmental inﬂuences on permanent changes in neurotransmitter levels. for example. Before considering the neurobiological correlates of child abuse and neglect in the following section. 1991). These models are beliefs by the child about herself or himself and predictions about how he or she will be treated by others. or by aversive stimuli when escape or avoidance are possible. 1978). It is now increasingly possible to study simultaneously the neurobiological processes accompanying or underlying observed behaviour. Projecting axons from these nuclei extend to all higher #Electroencephalogram (EEG) measures electrical brain activity generated by neuronal communication . $Neurotransmitters are chemicals in the brain which cross synaptic gaps from the axon of the transmitting neuron to the dendrite of the receiving neuron. postulated that peripheral adrenaline. event-related potentials (ERPS) are recordings of brain electrical activity over very short. Attachment behaviour is deﬁned as proximity-seeking behaviour by a dependent organism (infant or child). brain centres. the biogenic amines noradrenaline (norepinephrine) and dopamine (known collectively as the catecholamines) and serotonin (or 5HT) have been studied in greater detail. It is a biological instinct (Bowlby. Waters. The locus coeruleus is primarily activated from within the brain. The biogenic amines are synthesised in discrete nuclei in the brain stem and midbrain. emotions. neurophysiological. The child’s attachment status is assumed to be based on the child’s previous attachment experiences and thus reﬂects the child’s internal working models. activated by rewarding stimuli. or uncertainty. . orthostatic challenge means standing up suddenly after lying down.
Potent sources of stress in childhood have now been shown to include severe deprivation and neglect in early life and exposure to violence between parents. extensive animal studies have shown that brief and repeated periods of separating a mother from her newly born oﬀspring leads to a stress reaction expressed by increased glucocorticoid %Adrenal cortex is the outer shell of the adrenal gland. which would suggest that some children will be more vulnerable to the eﬀects of stress. Aitken. Bhatnagar. . Parritz. It involves the hypothalamic-pituitary-adrenal axis. For example. & Sapolsky. The HPA axis is a physiological pathway connecting the brain to the adrenal cortex. the hippocampus is a part of the temporal lobe of the brain. a projective task in which children are requested to complete beginnings of a number of stories. Neurobiological correlates of attachment. in the response to stress.. the neurotransmitter system. There is also evidence of a complex relationship between attachment status and infant cardiac reactivity (Izard et al. & Smith. 1991). Lewis (1992) describes three dimensions along which responsiveness to stress can be measured. Nachmias. The measurement of attachment status in older children using the Strange Situation Test is not applicable. most likely. Van Berkel. which will be perceived by the infant or child as stressful. Dampening refers to the child’s ability to stop responding to a particular stimulus once the threshold has been reached or passed. increased licking behaviour of their pups by mother rats leads to decreased hippocampal cell loss in old age. 1998). There are individual variations. The Stress Response The stress response is a physiological coping response. Post. Kalkoske. including fear and a sense of loss of control. The hypothalamus secretes corticotropin-releasing hormone (CRH) that in turn stimulates the anterior pituitary gland Stress Stress is deﬁned as a stimulus or experience that produces a negative emotional reaction or aﬀect. It is important to note that 1 day in the life of a new-born rat is equivalent approximately to 6 months of maternal deprivation in human infants. 1992) as well as on prior experience. Boyce. Following the addition of the D category. and Rigatuso (1996) postulate that one function of a secure attachment relationship is to buﬀer or protect the developing brain from the potential deleterious eﬀects of elevated glucocorticoids on the brain during the protracted postnatal brain development. 1997) ! Further work with rats has shown that one day of maternal deprivation was suﬃcient to decrease brain-derived neurotrophic factor in the hippocampus and bring forward preprogrammed cell death (apoptosis) (Zhang. Buss. when they are met with insensitive and punitive caregiving responses. Gunnar. 1988) . cortisol is a steroid . Prior experience can aﬀect responses to stress by sensitisation. Alongside the (D) classiﬁcation. secretion with resultant death of hippocampal cells (e. also found more commonly among maltreated children. Brodersen. More boys than girls were classiﬁed as (D). These children would also be described and perceived by their carers as temperamentally diﬃcult. The frightened or discomforted infant seeks his attachment ﬁgure. who is at the same time the source of his discomfort.CHILD ABUSE AND NEGLECT AND THE BRAIN 103 two insecure categories—anxious\avoidant (A) and anxious\insecure (C)—and a disorganised\disoriented category (D) (Main & Solomon. 1993). Interestingly. 1997). V. this ﬁnding was initially attributed to brief periods of handling of neonatal rats by humans (Meaney. 1996). the abuser and caregiver will. by determining the child’s attachment security (Nachmias. 1994). This is the more so for infants rendered vulnerable due to a fearful or inhibited temperament. have been developed using story-stems (McCrone. emotional abuse. the sympathetic nervous system. Mangelsdorf. Conversely.g. Crittenden (1988) has added the (A\C) classiﬁcation. it was subsequently found that the mother rat responded to the human smell on her pups by licking them (Liu et al. Alternative means. Main and Hesse (1990) postulated that introjection of fear into the caregiving relationship leads to the (D) category. & Buss. particularly in highly reactive babies whose response threshold to stress was low and whose dampening response was low. suggesting a central role for biogenic amines as the mediators of secure or insecure attachment. and second. be the same person. An interesting psychobiological attachment theory has been expounded by Kraemer (1992). and reactivation. Heart-rate variability (a measure of heart-rate pattern) was found to be higher in insecure infants. as well as the more obvious recognised forms of abuse. 1990).. Although in Lewis’ work. ﬁrst to their own inherent responses to stress. and the immune system. They are therefore doubly vulnerable. Cicchetti. Lewis showed that in babies there was stability over the ﬁrst 2 months of life for threshold and dampening levels. Egeland. namely threshold. Plotsky & Meaney. Barr. whereas it is far more likely that the sexual abuser will not be the primary or sole caregiver of the child. Barnett. which is situated adjacent to the kidney . which secretes cortisol%. Hypothalamic-pituitary-adrenal (HPA) axis. & Carlson. Levine. Carlson. Xing. In support of temperamental inﬂuences. measures of stress responses were behavioural rather than neurobiological. and repeated physical abuse. especially of young children. Threshold represents the amount of stressful stimulation needed to produce a response. in comparison with 19 % in the nonmaltreated group. relying on the assessment of internal working models. and Braunwald (1989b) reanalysed the attachment relationships of a sample of maltreated and nonmaltreated 12-month-old infants and found a large over-representation of this disorganised category (82 %) among the maltreated group. & Zeltzer. Much of the data on the eﬀects of early deprivation on brain development comes from animal experiments. This may be explained by the fact that in neglect. and none have examined the attachment classiﬁcation of sexually abused infants (Morton & Browne. Reactivation refers to the child’s ability to become aroused again after arousal and dampening have occurred. dampening. Most studies of attachment status in maltreated children have included physically abused and\or neglected children. Gunnar. which are based on diﬀerences in temperament (W. and by shaping the child’s perception of an experience and its meaning as stressful or not. likely to be enduring. it is likely that there are neurobiological correlates to these observed behaviours.
stress has been shown to enhance the release and metabolism of dopamine in the prefrontal cortex (Charney. or at the expense of) elevated cortisol. Serum cortisol acts in a number of diﬀerent ways and on most tissues and organs. & Davis. When faced with repeated or chronic stress. while the cortisol response to stress had fallen to a lower level than in early infancy. which includes elevation of heart rate. Cicchetti. 1992). cortisol secretion increases via messages down the HPA axis. in some circumstances. Fear messages from the amygdala and hippocampus arriving in the medulla of the brain stem (LeDoux. 1991) by down-regulating the HPA axis response. alongside (and possibly facilitated by. are secreted within seconds of the body sensing a stressor. Another example of this diﬀerential response is the ﬁnding that pacifying a young infant by. leading to elevation of ACTH and plasma cortisol as well as to increased activity of the noradrenergic sympathetic nervous system. for instance. released by stress. may become enduring and. 1998). 1993). & Cicchetti. However. Giller. for instance. & Ryan. infant–mother separation activates the HPA axis. there was a negative correlation between EEG event-related potentials . Behavioural responses to stress. response to frightening experiences. against the body’s normal and immediate responses to stress. and dampening of fear responses to the stressor. As mentioned earlier. been found that a more reactive HPA axis is associated with greater professional competence in air traﬃc controllers (Rose. Deutch. One aspect of the body’s coping response to acute stress is an elevation of serum cortisol. adrenaline probably also activates noradrenaline secretion in the brain via the vagus nerve.. The eﬀects of these hormones include raising heart rate and blood pressure.104 D. and activation of the ﬁght or ﬂight response. This means that as speciﬁc brain centres receive cortisol. Southwick. glucocorticoids are secreted during the following minutes and take several hours to exert their eﬀect (M. & Mason. demonstrating the direct links between the adrenergic and the cortisol responses to stress (Southwick et al. suppression of the stress response leads to a restoration of cortisol levels to within normal limits (Yehuda. Direct evidence for the harmful eﬀects on brain development of a reactive HPA axis. There are thus several connections between the peripheral sympathetic adrenaline and central (brain) noradrenaline actions in response to stress (Krystal. Livingston. they send messages via the HPA axis to reduce the level of cortisol secretion. These are not uncommonly met with in children who have suﬀered long-term abuse (Shields. Both the sympathetic nervous system and the catecholamines are activated by stress. there may be a cost to the reduced cortisol levels. there is a diurnal variation in cortisol levels. whose functions also include the planning and organising of actions using ‘‘ working memory ’’ and the inhibiting of inappropriate responses and attention to distractions (‘‘ executive functions’’). Whereas the catechol amines epinephrine (adrenaline) and norepinephrine (noradrenaline). GLASER to secrete adrenocorticotropic hormone (ACTH). Interestingly. This is released into the blood and. Stress. Elevated Cortisol. sweating. Long-term eﬀects of the stress response. The sympathetic nervous system and catecholamines. namely a dysfunctional. Whereas there was a parallel decrease of both cortisol and behavioural responses to stress between 2 and 6 months. there is a diﬀerential response to the same stressor from the two measures. Guyre. which reduces crying. and consequent elevated cortisol levels. and feelings of passive fear (Hart. use of a dummy. The rate of secretion of cortisol is regulated by a negative feedback loop to maintain an optimal level. In the normal state. Krystal. Brodersen. Southwick. stimulate the locus coeruleus and thus noradrenaline secretion in the brain. Messages are also relayed by sympathetic nerves from the brain stem to the medulla of the adrenal gland. It has. in others. which explain the emotional as well as the physical experiences associated with stress. or less than optimal. falling to lower levels in the afternoon. 1991). this reaction may become sustained and this physiological arousal is accompanied by passive and withdrawn behaviour (Suomi. instead. the Hippocampus. and Holbrook (1984). 1982) and with greater emotional and social competence in boys with haemophilia (Mattson. Conversely. there are situations that require an elevation of cortisol in the body. & Charney. and CRH from the hypothalamus. & Hall. Its actions include suppressing the immune response. However. Jenkins. stimulates the cortex to produce and release cortisol into the circulation (Chrousos & Gold. In monkeys. and Memory While being a necessary physiological response to acute stress. to the detriment of the body’s homeostasis. when reaching the adrenal gland. one of whose functions is to produce coping responses to stress. Howe. elevated cortisol may also be harmful. and when certain signals are perceived by the brain. 1992). 1993). Cortisol levels can be measured noninvasively by assays of saliva and in the urine. which secretes adrenaline and noradrenaline. 1971). can be modulated by maternal behaviour. which is concerned with actively responding to fear-inducing stimuli in times of acute threat. Hurst. increasing the level of circulating glucose. whose production marks the sympathetic nervous system’s response to stress. 1994) and may be reﬂected in the (D) category of infant attachment. 1999). a stress response that commences in early infancy. Gunnar. particularly in early life. In some monkeys. belies the fact that elevation of cortisol continues (Gunnar. Gunnar. what is particularly interesting and important is the notion. In preclinical studies. and Krueger (1996) showed a diverging stress response in infancy. Raised levels of noradrenaline and dopamine are positively associated with dysfunction of the prefrontal cortex (Arnsten. 1995). This dysfunction leads to symptoms clinically recognised as Attention Deﬁcit Hyperactivity Disorder (ADHD). Lowy. as well as adverse eﬀects on the hippocampus (see later). McEwen (1999) describes several more and less adaptive responses of the stress hormone axis to chronic stress. with higher levels found in the morning. that the stress-induced increase in glucocorticoid (cortisol) levels protects not against the original stressor but. with the aim of avoiding the overreaction of these responses. Coping may take the form of a reduction in felt anxiety or distress. Very young animals and human infants show reactions to stress that. 1995). proposed by Munck. Cortisol level is only one measure of a stress response. behaviour being a further one. crying increased again by 15 months. Gross. An indication of a similar mechanism in humans comes from Gunnar and Nelson (1994) who showed that in 12-month-old infants. 1996). Southwick. since cortisol also exerts an eﬀect on the amygdala. & Hall. ﬁrst came from animal experiments.
place. 1994). This ﬁnding held whether the children were rated as constitutionally inhibited in new social situations. It is possible that some of these regions (although not the amygdala) may be adversely aﬀected by excess cortisol levels early in life (Gunnar. and salivary cortisol levels. left with an unfamiliar babysitter for 30 minutes. enduring changes have been found in the pattern of EEG asymmetry between the left and right prefrontal lobes in patients who had suﬀered from depression but had made a symptomatic recovery (Henriques & Davidson. Nachmias et al. hypoglycaemia. 1994). namely hypoxia. despite the behavioural adaptation which they showed. Cicchetti. and toxic chemicals. Lerner. Hershey. is manifested in the brain as activity in the left prefrontal cortex. caregiver was friendly. Healthy adults have shown a decline in explicit memory with sustained increases in dexamethasone (a glucocorticoid) (Newcomer. & Brodersen. Larson. Similar patterns of asymmetries have been found in 3year-old children who were temperamentally extremely inhibited and shy (Davidson. a repetition of which may therefore not be as aversive. Prolonged high levels of cortisol lead to hippocampal cell death. and damage to the hippocampus in humans. which promotes early degeneration of these neurons (Sapolsky. 1992). Thus. Buﬀers to the Stress Response and the Inﬂuence of Attachment Status Gunnar (1998) suggests that in view of the potentially damaging eﬀects of elevated cortisol levels on the brain early in development. 1995). probably due to increased neuronal vulnerability to glutamate toxicity. the hippocampus is believed to integrate the diﬀerent aspects of a memory. 1990). in contrast to a cold and distant babysitter (Gunnar. Rebert. Exposure to high levels of cortisol causes atrophy of hippocampal dendrites. Davidson (1994) has suggested that a particular form of positive emotion. Bender. Erickson. In some of these children. for obsessive compulsive disorder) bring about change on PET scanning (Baxter et al. In his paper entitled Why stress is bad for your brain. we learn that hypo-responsiveness to stress in the very early days of postnatal life is achieved by maintaining close contact between mother and pup (Suchecki. and context (Bremner & Narayan. epileptic seizures. it appeared that higher cortisol levels interfered with activity of the hippocampus. underscoring the contribution of nonphysical. mechanisms have evolved to lower reactivity of the HPA axis to stress. & Finch. The hippocampus has a high concentration of receptors for glucocorticoids. Carlson. Gunnar. It was also shown that for these latter infants. and Poland (1991) showed that the verbal memory of asthmatic children on high doses of prednisolone was poorer than on low doses. Primate hippocampal neurons are adversely aﬀected by sustained high levels of cortisol. From animal (rodent) work. The salivary cortisol levels in 9-month-old infants. 1992). showed no elevation of cortisol when responding fearfully to the approach of a stranger (a clown). there is evidence that behavioural therapies. which are the physiological concomitants of observed behaviour.g. the cortisol response to the same procedure (well-baby examination with inoculation) decreased from a high to a lower response between the age of 2 and 4 months. the right side is more involved with visual memory (Bremner et al. Calkins. both in adults and in children. 1990). EEG Changes Fox. By contrast. . did not rise if the Psychological Therapies and Neurobiological Changes Alongside evidence of speciﬁc brain functioning and structure. This test is a mild stressor compared to most experiences of child abuse and neglect and these results reﬂect the extent of these children’s vulnerability to stress. Rosenfeld. but not toxic. 1989a). There are other brain regions with glucocorticoid receptors. part of the temporal lobe of the brain. & Bardgett. Infants who showed a disorganised\ disoriented attachment response were found to have higher cortisol levels during the Strange Situation Test (Hertsgaard. physical trauma. Long-term elevated. 1995). or buﬀer. Whereas the left hippocampus is believed to play a more important role in verbal memory. Askins. and Krueger (1996) have shown that in 72 infants. which is reversible when exposure is brief. by 24 months. 1998) that the equivalent protector. Whether these enduring physiological changes are indicators of continuing vulnerability in these children. for example. maternal intrusiveness and insensitive encouragement of the infant towards the clown contributed to the elevated cortisol response. In other words.. and Bell (1994) have shown particular EEG asymmetries between the electrical activity of the right and left frontal lobes in 4-month-old infants who had shown early diﬃculties in coping with the arousal induced by new stimuli.. cortisol levels render hippocampal neurons susceptible to the eﬀects of commonly encountered threats to the brain. 1992). and frontal brain regions. The disorganised attachment pattern is associated with abuse and neglect (V. The hippocampus. who was present. enthusiasm). 1998). psychological treatments to neurobiological change. At the time of recollection. Hertsgaard. constitutionally inhibited and insecurely attached children showed a signiﬁcant elevation in salivary cortisol when approached by the clown. & Levine. amygdala. including the cingulate gyrus. 1993).g. Gunnar. High-dose cortisol medication has been shown to aﬀect memory adversely. associated with the motivation towards attaining a goal (e. Barnett. and further between 6 and 15 months. as well as to locate the memory in time. and sensitive. (1996) have shown that 18-month-old children who had a secure attachment to their mother. Uno. It is postulated (Gunnar. is not known. & Nachmias. This has important implications for intervention. of the HPA axis in human infants is the security of attachment with the primary caregiver. In adults.CHILD ABUSE AND NEGLECT AND THE BRAIN 105 (ERPs). there had been a behavioural adaptation but the original EEG asymmetry endured. 1998). Craft. which reﬂect hippocampal activity in ‘‘ laying down a memory ’’. & Braunwald. or not. playful. as well as drug therapy (e. Sapolsky (1996) has succinctly summarised recent evidence indicating a signiﬁcant correlation between sustained stress. excess cortisol. Brodersen. is integrally concerned with memory (Squire. This change possibly reﬂected the child’s capacity to recall the previous experience.
In childhood studies. including sexual abuse. and 13 were normal matched controls. Much abuse and neglect. is not perceived by the child as trauma. Those maltreated children who were classiﬁed as depressed using the Child Depression Inventory (Kovacs. Post and Weiss (1997) describe the ‘‘ worst case scenario ’’. the area concerned with language. which may have been related to the anticipatory stress of returning to an abusive home. Broca’s area in the left hemisphere. (3) it overwhelms the individual’s coping capacity . some of which would be clearly regarded as child abuse. and possibly were still being. who were also less socially competent. As part of a longitudinal study of sexually abused girls using a self-selected sample of girls of mean age 11. ﬁndings have been found to be discrepant about the response of the HPA axis to maltreatment. De Bellis & Putnam. (1994) found dysregulation of the HPA axis with a blunted ACTH response to ovine corticotropin-releasing hormone (oCRH). if only because of the very predictable and chronic nature of some forms of maltreatment. 1996). lower cortisol levels are found in conjunction with a possibly enhanced negative feedback in the HPA axis. This lack of HPA responsiveness may have evolved as a protective factor for the brains of these very vulnerable children. (1995) found that. 1. 1995). A hypothesised explanation for this ﬁnding is that the previous stress of the abuse had caused CRH hypersecretion with consequent adaptive down-regulation of the HPA axis. GLASER Eﬀects of Child Abuse and Neglect on the Brain Broadly and theoretically. & Larrieu. 4. the distinction between omission and commission within child maltreatment is not as clear cut. Zeanah. et al. Keshavan. there was concomitant heightened activity in their right amygdala and associated areas of the temporal and frontal cortex. Results showed no diﬀerences in the cortisol response to the CRH . and (4) it violates basic assumptions about the environment’s (human or physical) benevolence and safety (adapted from Eisen & Goodman. The authors suggest that this provides a neurobiological illustration of the clinically encountered tendency in PTSD to re-experience emotions as physical states rather than as declarative verbal memories. or familiarity with. other aspects of neurobiological dysfunction in relation to child abuse and neglect. using PET scanning. Gunnar. Trauma and abuse are not synonymous. 1996). Weisaeth & van der Hart. stressful situations to which these maltreated children have therefore become habituated and do not respond physiologically. whilst stressful. 2.g. during early brain development. an average of 5 years after sexual abuse. and Cicchetti (1996) have found that 131 9-year-old children who had been. it is by no means an invariable consequence. and diurnal variation of cortisol level. that when patients suﬀering from PTSD were presented with vivid accounts of their own traumatic experiences and showed autonomic arousal. While PTSD is not infrequently found in children who have been maltreated (De Bellis. maltreated showed slightly elevated afternoon salivary cortisol levels. The depressed children were recruited from inpatient and outpatient psychiatric clinics. a set of criteria for diagnosing PTSD in young children under the age of 4 years has been developed and shown to have good inter-rater reliability (Scheeringa. a group of 33 maltreated children aged 4 to 6 years. This is in contrast to depressed children who have not been abused. which are not easily subsumed under that diagnosis (van der Kolk. in which young children experience both abuse and neglect. but without increased cortisol secretion. which suggests a blunting of the HPA axis. in whom an alteration in HPA axis functioning has not been found. 13 were depressed without a history of abuse . will be considered. van der Kolk and colleagues consider that the diagnosis of PTSD is most appropriate for traumatised adults. Measures include ACTH response to injected CRH. mean age 9. and that their results replicate those found by Kaufman (1991) for depressed maltreated children. The 13 girls were no more depressed than a comparison group at the time of the study. Alternatively. Hart et al. Neurobiological Stress Responses to Child Abuse and Neglect HPA axis responses. Chronic abuse and neglect are likely to have a pervasive eﬀect on a child’s psychological and biological regulatory processes rather than to lead to discrete conditioned behavioural and emotional responses such as are found in PTSD (van der Kolk. Next. In practice. At the same time. Drell. 1992) showed attenuated morning cortisol levels. Chrousos. 1994). However. neglect leads to deprivation of input needed by the infant brain at times of experience-expectant maturation. were shown not to have elevated salivary cortisol levels in situations of stress brought on by conﬂictual social interactions. 1998).. in comparison to nonmaltreated children. Deprivation has been found to result in a stress response as well as in deﬁcits in development.. in which they compared ACTH response to CRH stimulus in three groups of children. was ‘‘ turned oﬀ ’’ (Rauch et al. The authors point out that maltreatment is not a unitary concept. The set of criteria relies on observed behaviours and has been tested prospectively on 12 young children known to have undergone signiﬁcant trauma. Both early neglect and abuse therefore have the potential to aﬀect subsequent brain functioning. although 54 % had a history of severely depressed mood and self-harming behaviour. total level of cortisol being secreted. 1994). Thirteen were depressed with additional histories of physical and\or sexual and\or emotional abuse . Golier and Yehuda (1998) summarise a number of studies mostly suggesting that some years after experiencing trauma. 1999). (1997). Child abuse is a potent source of stress. The ensuing section will commence with a discussion of aspects of the stress response to various forms of child maltreatment. and much of the literature on the relationship between child abuse and neglect and neurobiology has examined the eﬀects of stress on the brain (e. Interesting work has shown. 3. De Bellis. 1996). Further ﬁndings have been reported from a more recent study by Kaufman et al.106 D. Hart. and that children develop much more complex reactions. et al. as well as in the right visual cortex. but not reﬂecting a stress response. it may reﬂect lack of novelty of. Most would agree that trauma includes the following ingredients : (1) it seriously threatens the health or survival of the individual . There continues to be a considerable lack of clarity and tight operational deﬁnition about what distinguishes traumatic from stressful events (Shalev. not infrequently encountered. while abusive experiences aﬀect brain development at experience-dependent stages. (2) it renders the individual powerless in the face of overwhelming fear or arousal .5 years.
Bremner et al. although results from many animal experiments. Seventy-one per cent of the subjects suﬀered from PTSD and 71 % from a dissociative disorder. Stein. et al. Trickett. Schacter. in comparison with a nonabused group. including primates as well as rodents. Also. 1. may be aﬀected as reﬂected by the partial hippocampal atrophy. Twelve sexually abused girls were found to secrete signiﬁcantly greater amounts of homovanillic acid. In the De Bellis. Carlson and Earls (1997) report that at the age of 2 years. for understandable reasons. in comparison to 21 subjects who had experienced no childhood abuse. The picture is further complicated by ﬁndings recently reported by De Bellis. As Stein et al.. Baum. these children did not show the usual diurnal variation of cortisol levels that was found in home-reared Romanian comparison children. which remained elevated relative to the lower afternoon levels.. respectively. (1997) suggest. et al. while retrograde memory. depressed nonabused. point out that. showed increased levels of 24 hour urinary cortisol in comparison to healthy controls (but not in comparison to nonabused anxious controls). The deprived. These ﬁndings are presumed to indicate an enduring stress response. than a comparison group. however. Torchia. Increased levels of urinary catecholamine excretion have been found in adult PTSD (Southwick et al. In summary. as well as Sapolsky (1996). Binder-Brynes. . will aﬀect short-term memory (Bremner et al. They found that 18 prepubertal children (mean age 10. De Bellis. The diﬀerence in this sample of maltreated children is that they suﬀered from PTSD. the contribution of depression to these ﬁndings is not clear.4 years) who were suﬀering from PTSD following previous signiﬁcant abuse. This would explain why trauma (e. indicating higher catecholamine activity. Chrousos. seven depressed abused children who were continuing to experience active emotional abuse showed a signiﬁcantly elevated ACTH response. Severity of the latter correlated positively with degree of hippocampal volume reduction. Koverola. a metabolite of dopamine.. the integrative function of the hippocampus. and Mclarty (1997) similarly found statistically signiﬁcant left hippocampal volume reduction (5 %) in 21 women who reported experiences of severe childhood sexual abuse. presumably from excess cortisol secretion brought on by the stress of the abuse. or may be compensated for during childhood development by the process of neural plasticity. What is not clear is the implication for later functioning of continued dysregulation of the HPA axis. Catecholamine response. military combat) ﬁrst encountered in adult life. What this does not explain is why in one of the studies (Bremner et al. were found to be aﬀected by early and late trauma. and Putnam (1994) in the longitudinal study of sexually abused girls mentioned above (De Bellis. that stress in early life. amnesia associated with hippocampal damage is usually conﬁned to subsequent events. there is evidence of impairment in the HPA axis following. Koustaal. Yet. (1999) also showed that abused children suﬀering from PTSD excreted signiﬁcantly greater concentrations of baseline noradrenaline and dopamine in comparison to nonabused anxious and healthy controls. in particular the emotional and tactile caregiving aspects. Urinary catecholamine excretion was measured by De Bellis. The authors suggest the possibility. The authors suggest that their ﬁndings may be explained by a lack or immaturity of adaptation of the HPA axis. Baum. In their further study reported above. Hanna. various forms of abuse and neglect. Although there is evidence of damage or shrinking of the hippocampus following traumatic events. particularly for emotionally charged memories of trauma. However. 1997). while there was no diﬀerence between the ACTH responses of the control. supported by animal experiments. 6. The children in the orphanages had signiﬁcantly lower morning cortisol levels. although adults who suﬀer from PTSD show lower urinary cortisol levels (Yehuda. et al. only one girl met DSM-IIIR criteria for PTSD. that is. Postulating a stress response. The respective researchers. Diﬀerential hippocampal response to stress at diﬀerent stages of development might also explain why the left and right hippocampi. it is possible that the relatively small magnitude of the hippocampal damage found in adult survivors of childhood abuse does not impair explicit memory. 1995). The relationship between hippocampal atrophy and adult short-term memory recall remains unclear. both their memories for the abuse and their current memory functioning were intact. when neural plasticity is no longer functioning suﬃciently.g. in combination with acute or ongoing adversity. memory for events preceding the hippocampal damage. leads to a raised ACTH response to CRH. measures correlating signiﬁcantly with duration of abuse. there was no indication of ongoing adversity and this supports the explanation postulated here. Kahana. et al. Lefter. and depressed abused children who were now living in a stable environment. (1997) have reported 12 % left hippocampal volume reduction in 17 adult male and female survivors of severe childhood physical and sexual abuse who now suﬀered PTSD. et al. no associated memory impairment. There was.. would support this possibility. is spared (Squire. Interestingly. interestingly. The association between hippocampal atrophy and adult PTSD following either childhood or adult trauma may be explained by the suggestion that metamemory. 1993). The study of the eﬀects on human infants of extreme deprivation. of the comparison children. In the absence of a comparison group of nondepressed. and during continuing experiences of. abused children who continued to experience abuse. 1994).CHILD ABUSE AND NEGLECT AND THE BRAIN 107 stimulus between any of the groups. orphanage-reared children also showed signiﬁcantly poorer performance on the Bayley Scales of Infant Development and the Denver Development Screening Test. some showing raised levels of cortisol with others showing protective adaptation expressed by the presence of normal levels of cortisol. there was no associated impairment of memory functioning. and who were now living in stable situations. there is currently no conclusive evidence for a causal explanation in the direction of abuse leading to hippocampal damage. (1994) study described above. 1995) there was short-term memory recall deﬁcit in adulthood following childhood abuse. Hippocampal volume. Chrousos. 1992).. leading to the phenomena associated with PTSD. has been carried out on infants reared in Romanian orphanages. 5. M. Interestingly. (1999). and Norman (1996) report a series of 22 women who experienced prolonged and severe child sexual abuse and who showed reduction of volume of the left hippocampus on MRI (magnetic resonance imaging).
Infant monkeys deprived of their mother’s care were found to have lower levels of cerebrospinal ﬂuid (CSF) noradrenaline and its metabolites than control monkeys (Higley. 1995). Stilwell. Perry (1994) has reported decreased platelet adrenergic receptors in a small group of children with PTSD following serious abuse. which is correlated with DβH level in the cerebrospinal ﬂuid (CSF). In this process the vagus nerve. This hypervigilance and hyperactivity is seen equally commonly in girls and boys who have been abused. and abnormal return of heart rate to baseline levels after an orthostatic challenge. a ﬁnding suggesting downregulation of the peripheral adrenergic receptors in response to higher levels of circulating catecholamines. (1995). These ﬁndings of a continuing eﬀect on catecholamine functioning following abuse primarily apply to children with PTSD. Infants of depressed mothers also show less distress when separated from them. The children are often not actually aware of the source of the arousing cue. Moreover.. which interfere with their functioning. suggesting an overactive sympathetic nervous system in these children. Perry also found increased resting heart rate. Kraemer. These ﬁndings bear similarities to those found in rhesus monkeys. alter the perception of painful stimuli (Abercrombie & Jacobs. The authors postulate that the ﬁndings regarding processing of values of conscience requires an intact behavioural inhibition system that is. showed more interference with an aspect of conscience development. The recognition of these cues as danger signals is conveyed to the amygdala. In the infants of depressed mothers. Ebert. The reduced blood level of the enzyme. 5. 1998). is believed to be long-lasting. Clinically they are described as having brief. in infants of depressed mothers when the infants were engaged in social interaction.. Rogeness and McClure (1996) report similar ﬁndings in a group of children (mean age 10. Hessl. in part. both cortisol and noradrenaline. which was also noted by Field. unlike ADHD without trauma. either with their mother or with another adult. children will later react to cues or apparently minor reminders of the past traumatic experiences by dissociating. Kopta. in a group of boys hospitalised in a psychiatric hospital (Galvin et al. Dawson. the physiological stress response was not. Pollard. Suomi & Linnoila. associated with behaviourally observable distress. Stress hormones. some aspects or reminders of the experience become cues capable of evoking apprehension and fear. which is found particularly in very young children and in girls.and peer-derived rules of conscience. In psychiatrically hospitalised boys who had experienced signiﬁcant neglect with or without abuse in the ﬁrst 3 years of life. 1992 . and being the victim of some forms of sexual abuse. As with the arousal response. which is far more common in boys. becomes activated. Kaufman et al. Children might thus become hyper-aroused. their threshold to reacting to stress is lowered. disengaging attention from the present reality. The extent to which this behaviour is the same entity as the commonly encountered disorder is not clear. GLASER 2. ‘‘ resorts ’’ to dissociation. & Vigilante.5 years) hospitalised for psychiatric treatment. 3. endogenous opiates. When interacting with their depressed mothers. Perry found an improvement in arousal symptomatology as well as in basal heart rate in the children suﬀering from PTSD. Some of these children show behaviour that symptomatically resembles ADHD and which is a manifestation of post-traumatic arousal. 6. the child faced with a frightening experience. is described by Perry et al. and found a raised level of . Serotogenic response. being the recipient of direct physical threat or abuse. infants have been observed to be less active. This includes the witnessing of domestic violence. Subsequent reactive repression of enzyme activity leads to the ﬁndings of lowered DβH level. as well as with a history of early maltreatment. Galvin et al. mediated by noradrenaline. Galvin. and inattentive spells. Shekhar. in contrast to infants of nondepressed mothers who do show a rise in heart rate when displaying negative aﬀect. 1996). the parasympathetic part of the autonomic nervous system. Baker. leading to a slowing of the heart rate and a fall in blood pressure.. 1988). In fact. associated with dopamine systems that arise in the brain stem and are activated by stress. & McKinney. 4. A very diﬀerent reaction to trauma. experiencing raised heart rate and feelings of anxiety when faced with an apparently neutral occurrence or stimulus. Pickens and Fox (1995). This enzyme is involved in the conversion of dopamine to noradrenaline. blank. 1991). and their reaction shows sensitisation to early indicators of potentially frightening or threatening cues (Perry. However. a physiological measure of being stressed. those maltreated before the age of 3 years. and show more gaze aversion than a comparable group of infants of nondepressed mothers. Here. These diﬃculties correspond closely with essential features of conduct disorder. 1998). (1998) also measured serotogenic functioning in their study reported above (Kaufman et al. even when not accompanied by or following the trauma. They found reduced plasma DβH levels as well as lowered blood pressure in association with a history of early neglect. and those who had lower serum DβH. In his uncontrolled trial of medication using clonidine. Whether these eﬀects would be found without the PTSD and whether they abate following treatment is less certain. 1994). which sets oﬀ a fear response (Gallagher & Chiba. with or without abuse. namely the valuation of authority. This physiological stress response could be the result of both increased sympathetic adrenergic activity or lowered vagal (parasympathetic) tone. and McKasson Goldfarb (1997) have gone on to show that among psychiatrically hospitalised boys. Some traumatic forms of child abuse and neglect are repeated experiences. Fear is perceived in the amygdala (LeDoux. and unable to escape. recent guidelines for treatment of children and adolescents with PTSD state that ‘‘ there is no empirical support for the use of any particular medication to speciﬁcally treat PTSD in children ’’ (Cohen. Blakley. Following maltreatment. postulate that the early neglect and abuse which these boys suﬀered led to an overstimulation of the noradrenergic system due to the stress response with enzyme induction. 1997). and Frey (1994) also found increased heart rate. which might include a particular smell or a sound associated with the abuse. It is postulated that as part of the dissociation process. Schmidt. vocalize less. 1989). Parasympathetic nervous system response. 1995). have been found to be elevated in depressed mothers and infants (Field. the same group of researchers had previously reported an association between low serum DβH and undersocialised conduct disorder. an association has been found with reduced levels of plasma dopamine beta hydroxylase (DβH) (Galvin et al. however.108 D.
2. The authors point out that the left frontal lobe is specialised for the expression of positive emotions such as joy. size. Chrousos. (1994). & Swett. & Brumaghim. Unlike the nonmaltreated children. It is important to note that this childhood study did not ﬁnd a predicted decrease in hippocampal volume. A preliminary study with 10 non-patient adult subjects who had experienced early trauma and 10 comparison subjects found that the traumatised subjects showed greater right-sided brain activity when recalling a traumatic memory than did the comparison group (Schiﬀer. particularly the middle and posterior regions. Field. Speciﬁcally. and Hessl (1997). (1999) discuss explanations for the diﬀerences in hippocampal volumes between children and adults. Keshavan. Moreover. using a questionnaire designed to test limbic system dysfunction in adults. Gado.. Lefter. The ﬁndings held both for children who were no longer being abused and for those still being emotionally abused. gender. et al. et al. The pattern is one of relatively increased right frontal lobe activity. 5. & Fox. De Bellis. and chemical changes in the brain. 4. rather than the happy. Teicher. & Friesen. & Vannnier. & Ackerman. an impairment in their cognitive functioning. and EEG abnormalities in the left side of the frontal and temporal region of the brain (Ito.CHILD ABUSE AND NEGLECT AND THE BRAIN 109 plasma prolactin secretion in 10 depressed-abused children. Using MRI scans. 1996 . and chemical changes in the brain. in contrast to adult survivors of childhood abuse. 1992) and possibly raised cortisol levels. Impoverished environments and lack of mental stimulation in the early lives of these children could also be contributing factors. 1998 . The children were instructed to press a button when seeing either angry or happy faces. Compared to the controls. 1990). Frey. Surrey. Ekman. through to 3 years of age (Jones. and handedness. both of whom had suﬀered childhood abuse and PTSD. 1. As the authors show and discuss. nonabused controls. Todd. between functional. Tanner stage. 1993). pictures of happy and angry faces interspersed between neutral pictures were shown under 2 conditions to 23 maltreated and 21 non-maltreated children aged 9 years. Cicchetti. 1993). hypothalamus. indicating limbic system dysfunction (Teicher. The disturbances included diﬃculty in falling asleep and increased activity during sleep. et al. were smaller . This follows an earlier study by the same group which showed that. and therefore possibly related to increased catecholamine concentrations (Simantov et al.. In a group of 115 psychiatric inpatient children. Similar EEG changes have also been shown by Dawson. It is therefore diﬃcult to determine whether this ﬁnding is considered to be part of a stress response to previous abuse or whether it is associated with familial and experiential factors as well as with current psychopathology. and the area of the total corpus callosum correlated negatively with duration of abuse.. The implication is that being presented with negative aﬀect carries a diﬀerent meaning to maltreated children and elicits a physiologically measurable diﬀerent response. These ﬁndings indicate that brain changes depend both on maturational factors and course of illness. age-dependent changes in sensitivity to the neurotoxicity of glutamate receptor blockers have been found such that cell death in corticolimbic regions did not occur in immature animals. and negatively with intracranial volume and total corpus callosum midsagittal area. Diﬀerences may be due to diﬀerences in methods of measurement. 3. An important implication for these abused children with PTSD is. The limbic system includes the amygdala. the maltreated children were slower. The brain volume was correlated positively with age of onset of PTSD and negatively with duration of the abuse. Some of the children had also participated in the study reported by De Bellis. Glod. Although the numbers were small. the children with PTSD were found to have 7 % smaller cerebral volumes . Glod. adult psychiatric outpatients with a history of childhood physical or sexual abuse had a signiﬁcantly higher score. 1995). 1996). The right frontal region is speciﬁcally activated during withdrawal-related negative aﬀective states (Davidson. Saron. a signiﬁcant association has been shown between a history of child physical. Csernansky. but increased towards adulthood (Farber et al. In preclinical rat studies. structural. sexual. While being as accurate in their responses. which has been recorded from 1 week of age. faces (Pollak. 1997). The authors discuss possible explanations for their ﬁndings. They describe the EEG changes in 13–15-month-old infants of depressed mothers as relatively decreased left frontal lobe EEG activity. This may be adaptive in abusive situations but may become maladaptive when used indiscriminantly in diﬀerent settings. There have been diverse examples of an association . Functional. Their mean ages were 12 years. 1995). In comparison to depressed and normal children. Osterling. Panagiotides. or psychological abuse. and a history of child abuse and neglect. hippocampus. the authors speculate that their ﬁndings indicate that traumatic memories may be preferentially stored in the right cerebral hemisphere. they were also found to have higher amplitude of ERPs when instructed to respond to the angry. individually matched for age. Ito et al. Teicher. there is a positive correlation between IQ measures and brain size. The volumes of the left and total lateral ventricles correlated positively . whereas the right frontal lobe is concerned with sadness and other negative emotions. (1999) have also recently measured the size of brain lateral ventricles and various brain structures in 44 maltreated children suﬀering from PTSD and 61 healthy. and total lateral ventricles and cortical and prefrontal cortical CSF volumes were larger. Klorman. compared to depressed-nonabused and normal controls. Senulis. There are early and continuing EEG changes in both infants and their depressed mothers. & Papanicolaou. 1997). suggesting that these brain size changes could be due to the traumatic early childhood experiences. Particular relationships have been found between the ERP responses of maltreated and non-maltreated children to aﬀect-containing stimuli. in human adults the extent of hippocampal atrophy following major depression correlated positively with the total life-time duration of depression (Sheline. the total midsagittal area of the corpus callosum. De Bellis. PTSD symptomatology correlated positively with ventricular volume. Other Neurobiological Responses to Child Abuse and Neglect Cerebral volume. therefore. Wang. several of which are summarised here. and prefrontal cerebral cortex. sleep disturbances have been found in prepubertal children who had been physically and sexually abused and who had been referred for inpatient or outpatient psychiatric treatment. structural.
Bornstein. It is important to continue to study factors leading to positive outcomes for these children. Living in the presence of parental violence is one particularly common situation. All the mothers had contemplated or actively sought termination of the pregnancy. since one purpose of this review is to point to areas of possible intervention to minimise harm to the child’s development. in which the lack of input to the developing child at certain critical stages of development will result in delay or absence of development of certain skills. The fact that many of these changes are related to aspects of the stress response is not surprising. and Larrieu (1997) rightly point out the complex interactions between risk and protective factors that must be encompassed in the understanding of the development of psychopathology. the Court of Appeal adjudicated that the rights and wishes of the mother prevail over those of her unborn child. Haynes. Implications for Future Practice Early recognition of infants and young children whose development is rendered vulnerable by neglect. In rats. This needs to include the construction of a coherent account by the child of her or his own experiences. and Brockington (1997) describe ﬁve depressed. Hyperarousal. both ego-control and egoresilience are likely to be temperamentally determined. as has the fact that maternal depression is one common context in which this occurs. the process of early brain development is constantly modiﬁed by external events which impact on that process. When. The neurobiological ﬁndings shed some light on the many emotional and behavioural diﬃculties which children who have been abused and neglected show. Zeanah. However. However. using the concepts developed by Block and Block (1980). as Block and Block point out. even in the absence of clear maternal depression. However. self-esteem is therefore both dependent on some contributors to good outcome and an independent contributor to outcome. as well as acknowledging negative feelings towards their unborn child. maltreated children aged 8–13 years. 1997). non-maltreated comparison group. For instance.. the caregiver also abuses or neglects the child. Mayes. Kent. This is particularly so for abuse that is traumatic. Nevertheless. psychological. there are situations in which we currently have no means other than education to intervene eﬀectively in such undesirable practices as drug and alcohol abuse in pregnancy. which may be partially explained by the poor quality of attachment relationships found in maltreated children (Cicchetti & Barnett. only ego-overcontrol diﬀerentiated between the maltreated and a disadvantaged.. At least in the U.K. active enquiry about possible foetal abuse. in the ﬁeld of child abuse and neglect there is not infrequently a conﬂict between the interests of the parent or abuser and the child. in a recent case in the U. The ﬁndings from neurobiological studies of brain development dealing with experience-expectant periods lead to an assumption of a deﬁcit model. The book is replete with reputable references as well as quotes from extensive conversations with researchers in the related ﬁelds. They also point to the caregiving relationship as the mediator of both extrinsic and intrinsic risk factors. and educational underachievement thus begin to be better understood. 1996) has only latterly acquired the recognition it deserves. As has been illustrated. and self-esteem each contributed to better overall adjustment in a group of 129 disadvantaged.110 D. while predictive of good adjustment. in child maltreatment. Condon (1987) found that 8 % of 112 pregnant women and 4 % of their male partners acknowledged the urge to hurt or punish their unborn child. 1995). Thus. In the light of the stability of resilient and nonresilient functioning (Cicchetti & Rogosch. 1991). Future prospective research will need to continue to test the hypothesis that a greater and earlier direct investment in children who are maltreated leads to enduring improvement in their functioning. Cicchetti. ego-overcontrol. pregnant women who repeatedly actively punched their own pregnant abdomen. This would allow for the possibility of actual prevention of very early child neglect or abuse. In this review. GLASER The disturbance was worse in the physically abused children and was found to be related to the abuse rather than to PTSD (Glod. & Harakal. even if the expression of these wishes will be to the detriment of the future child (St George’s Healthcare NHS Trust v. Lynch. 1997). Emotional neglect (Erickson & Egeland. diﬃculties with aspects of executive functions. The neurobiological ﬁndings go some considerable way towards explaining the emotional. adoption has been shown to reverse the eﬀects of prenatal stress (Maccari et al. 1994 . 1998). exposure to trauma.K. It is therefore interesting to note that empirical ﬁndings about the eﬀects of deprivation point to stress responses as much as to deﬁcits. This is encouraging. Teicher. As the authors point out.. As is evident. Boris. S. There are pragmatic reasons for this choice. in which young infants may not be considered as victims. it is possible to recognise active foetal abuse. Chawarska. & Granger. 1983) and personal eﬃcacy and achievement and. and Holt (1993) found that ego-resiliency. and neglect on the developing brain and subsequent child development has been ampliﬁed descriptively in intelligible lay language in a new book by Karr-Morse and Wiley (1997). Rogosch. which at times requires the legal mandating of intervention in favour of the child. despite evidence of the harmful consequences to the development of the future child (Jacobson & Jacobson. 1996). Conclusions There is considerable evidence for changes in brain function in association with child abuse and neglect. Three of these mother–child relationships remained very troubled after birth. in . since it is probably more feasible to encourage children to develop strategies of gaining control over their actions and responses than to become more ﬂexible. The stress response oﬀers one explanatory model for the neurobiological ﬁndings. abuse. Hartman. is indicated. at least. Much of what has been discussed above about the deleterious eﬀects of trauma. aggressive responses. and behavioural diﬃculties which are observed in abused and neglected children. only the contribution of the environment postnatally was considered. self-organization by the child needs to be encouraged and fostered by those intervening in abuse and neglect. self-esteem is a resultant of both good nurturance (Harter. These environmental factors commence their inﬂuence in utero. the mediating relationship itself is the source of risk. dissociative reactions. Laidlaw.. or direct abuse is an important step. Moreover.
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