© Springer International Publishing AG 2018
Maria Muzik and Katherine Lisa Rosenblum (eds.)Motherhood in the Face of TraumaIntegrating Psychiatry and Primary Carehttps://doi.org/10.1007/978-3-319-65724-0_77. Maternal Trauma and Related Psychopathology: Consequences to Parental Brain Functioning Associated with Caregiving
Virginie C. Perizzolo Pointet1, Dominik A. Moser2, 1, Francesca Suardi1, Molly Rothenberg1, Sandra Rusconi Serpa1, 3 and Daniel S. Schechter4, 1, 5
(1)
Child & Adolescent Psychiatry Service, University of Geneva Hospitals, Geneva, Switzerland
(2)
Department of Psychiatry, Icahn School of Medicine at Mount Sinai, New York, NY, USA
(3)
Faculty of Psychology and Education Sciences, University of Geneva, Geneva, Switzerland
(4)
Department of Psychiatry, Faculty of Medicine, University of Geneva Hospitals, Geneva, Switzerland
(5)
Department of Child & Adolescent Psychiatry, New York University School of Medicine, New York, NY, USA
Abstract
The chapter takes as its departure point the Winnicottian notion of “Good-enough mothering” as being tied to the capacity of the primary caregiver to engage in mutual emotion regulation during sensitive periods of early development. Maternal experience of interpersonal violence and related psychopathology (i.e. posttraumatic stress disorder) through associated emotional dysregulation and activation of traumatic memory traces even by routine mother–infant interactions (i.e. interactions such as separations involving child helplessness) perturbs this mutual regulation. Original research from the Geneva Early Childhood Stress Project is described to support that both neural activity and epigenetics of stress-linked genes are promising as (1) important markers of these hypothesized mechanisms and (2) useful measures of the effectiveness of targeted parent–child interventions. The role of individual differences played by possible endophenotypes in the intergenerational transmission of trauma and associated psychopathology, as for example that noted for mothers with prominent dissociative symptoms, is discussed with its clinical implications.
7.1 Introduction
Winnicott described the “good-enough mother” as one who indulges the initially completely dependent infant enough to permit him/her to feel comfortable and safe, but who also later supports that the infant abandons this early fantasy of complete ‘synchrony’ and learns to tolerate frustration (Winnicott 1953). “Good-enough” parenting, borrowing from this concept of the “good-enough mother,” is thus a very complex set of tasks that involves a consistent, predictible physical and emotional presence, while being neither too intrusive nor too distant. It is only when one takes a moment to reflect on all of the many functions that one actually performs as a parent that it suddenly seems daunting. From the beginning of the child’s life, parenting requires the procedurally encoded application of a multitude of social and emotional skills. For example, the emotional development of the child requires the parent both to model and to engage mutually in emotion and arousal regulation. This complex function coexists with many other types of critical caregiving tasks, such as nurturing, regulation of sleep and wakefulness, and surveillance of the environment.
It follows that in order to be a good-enough parent, a number of psychological and biological functions need to work well together. And as a command central of all of those functions, the parental brain shoulders a heavy load. Human beings aremost often physiologically prepared to become a parent over the course of gestation. The work by Barrett and Fleming (2011) demonstrated that during pregnancy and the postpartum period, several changes occur in the levels of specific hormones (e.g., gonadal hormones, oxytocin), which activate or affect specific regions in the maternal brain. For example, the rise in oxytocin hormone levels is thought to ensure that the mother will be attracted to her baby, will be attentive and sensitive to her baby’s needs, and will behave in a way that supports and protects her baby’s development.
Swain et al. (2012) added that the transition to parenthood also involves changes in the maternal brain that imply greater plasticity and an increase in gray matter volume, particularly in specific key regions such as the insula, prefrontal cortex, parietal lobes, and midbrain structures (hypothalamus, substantia nigra, and amygdala). In fact, increased gray matter volume in the midbrain correlates with maternal positive perceptions of her baby (Kim et al. 2010). Parenting not only modifies brain structure but also modifies brain functioning. Generally, parenting tasks require activation of multiple systems in the brain related to sensation, perception, affect, reward, executive function, motor output, and learning (Barrett and Fleming 2011). Research has demonstrated that specific maternal brain regions are activated when mothers hear their own baby’s cries. These specific brain regions include the amygdala (relevant to detection of novelty and alarm), the striatum and nucleus accumbens (relevant for sense of motivation and reward), the anterior cingulate cortex (ACC) (the ventral part of the ACC, or vACC is relevant for affect response and regulation; the dorsal part of the ACC, or dACC, has been linked to the appraisal of negative emotion) and dorsal prefrontal cortex (dPFC, is relevant for appraisal of actual danger and decision making), and the ventral part of the medial prefrontal cortex (vmPFC, is relevant for the regulation of limbic activation underlying emotional expression in general). Other brain structures that are also implicated in the complex connections relevant to parental brain circuitry are the inferior frontal gyrus (IFG, involved in the interpretation of another’s emotional state and reappraisal of others intentions) (Grecucci et al. 2013), orbitofrontal cortex (OFC) (has a role in executive functions), insula (involved in the interpretation of others’ intentions, has a role in bottom-up regulation), and periaqueductal gray (PAG) (involved in the expression of maternal behaviors).
Overall, a mother’s neural activity in response to her child’s cues reflects her psychobiological functioning at the time of a given interaction and is associated with her observable caregiving behavior (Moser et al. 2013). Multiple brain structures play a synergistic role in the regulation of these very complex social-cognitive and affective functions, by which a mother responds adequately (“good-enough mothering”) to her child’s needs under optimal conditions (Swain et al. 2012). However, more recently, research has also begun to investigate these brain processes under suboptimal conditions, such as when a mother herself is feeling threatened or otherwise excessively stressed. At these threat conditions, these same brain circuits may be adversely affected.
7.2 Trauma, Psychopathology, and Brain Circuitry
A number of different parental psychiatric disorders may affect the psychobiological processes involved during the course of a given parent-child interaction and alter parenting behaviors (Schechter and Willheim 2009). Exposure to interpersonal violence (IPV, i.e., physical and sexual abuse and exposure to domestic violence during childhood and adolescence, as well as physical and sexual assault by intimate partners and others during adulthood) is among the most traumatogenic of human experiences. IPV often leads to acute dysregulation of emotion and arousal, which can undermine one’s usual social-emotional coping strategies (i.e., social-cognitive capacity). IPV, particularly when repeated over time and in the context of an otherwise unpredictable environment, can alter an individual’s stress physiology in a number of important ways. Convergent data from the literature highlights emotional and physiological dysregulation related to post-traumatic stress disorder (PTSD), as one common form of psychopathology with enduring effects that results in the wake of violent trauma (see Chap. 6 by Martinez et al. in this book).
In order to understand the effects of IPV-related PTSD (IPV-PTSD) on maternal brain functioning, it is useful to consider the neuroimaging literature that examines brain structure and neural activity, particularly in response to trauma-related stimuli, among IPV-PTSD adults. Multiple fMRI studies using violence-related stimuli including trauma scripts, suggestive still images, or fearful and angry facial expressions have shown what has become known as “cortico-limbic dysregulation” (Bremner 2002; Shin et al. 2005, 2006; Liberzon et al. 2007; Moser et al. 2015c). Under normal circumstances, a fear-inducing stimulus triggers the amygdala and surrounding limbic structures (“the emotional brain”) as an alarm of danger to the organism; the dACC and mPFC (“the rational brain”) meanwhile appraise and contextualize the degree of actual danger and modulate the limbic response to the original fear stimulus. Neural activity in IPV-PTSD is characterized by a hypoactivation of brain regions associated with threat appraisal (i.e., the “rational brain” vmPFC and dACC) and thus reduced top-down regulation of the limbic (“emotional brain”) system. The dACC is a particularly salient region as shown in the paper by Rougemont-Bucking et al. (2011) that involved a fear-conditioning and fear extinction paradigm. The authors showed that among PTSD patients, the vmPFC remained hypoactivated even after extinction was learned (i.e., the fear stimulus was paired with a positive stimulus that recontextualizes it and renders it less noxious). And yet the dACC became activated once extinction was learned. Another study (Liberzon and Sripada 2008), similarly in patients with IPV-PTSD, also found that reexposure to violent trauma induced over-activation of limbic structures such as the amygdala.
Thus, it appears that there are two mechanisms in place that are associated with trauma-induced PTSD symptoms, a “top-down” and a “bottom-up” mechanism of cortico-limbic dysregulation. In PTSD, over-activation of the amygdala and surrounding limbic structures seems to be associated with hyperarousal and hypervigilance symptoms of PTSD. It is thus clear that the way IPV-PTSD affects the brain should be relevant to many functions that are also relevant to parenting. A more nuanced understanding of the psychobiology and neural circuitry relevant to caregiving in parents with trauma may help clinicians develop a better understanding of traumatized parents’ challenges and needs, and advance understanding of treatment targets in existing and newly developed interventions.
7.3 The Geneva Study on IPV-PTSD and Brain Circuitry
As part of a large multisite research program in Switzerland,1 the Geneva Early Childhood Stress Project has focused on how maternal IPV-PTSD impacts the mother-toddler relationship (Schechter et al. 2015c). “The Geneva study on IPV-PTSD and Brain Circuitry” utilizes a multifaceted approach by studying the issue from a psychological, behavioral, physiologic, and neuroimaging perspective. The participants of these studies were IPV-PTSD mothers contrasted with healthy control mothers with children aged 12–42 months of age. The Geneva study on IPV-PTSD and Brain Circuitry indicated that mothers with IPV-PTSD have a psychobiological disadvantage during general socio-emotional processing (GSEIP) and that this disadvantage generalizes to parenting specific processing and behaviors (PSPB) when they interact with their children. This disadvantage expresses in the brain in three ways: (1) reduced activity and changed function of the ventromedial prefrontal cortex (vmPFC) likely indicating problems in emotional appraisal which probably drives increased negative emotionality; (2) altered functionality in the dorsal prefrontal cortex (dPFC), indicating that mothers with IPV-PTSD have altered “top-down” regulation of their emotion, primarily focused on negative emotions in general rather than arousal level. Moreover, the use of cognitive resources in mothers with IPV-PTSD as opposed to controls seems disassociated from their children’s emotional needs; and (3) increased hippocampus activation during emotionally aversive scenes, which suggests that IPV-PTSD mothers may have overactive emotionality and memory when dealing with their children in distress.
Specifically, some of the first studies within the Geneva project (Moser et al. 2015a, b) focused on understanding GSEIP among IPV-PTSD mothers. The probes that these studies used to capture brain activation in the MRI scanner were scenes of adult male-female interactions excerpted from fiction films with varying emotional content (e.g., scenes with menacing content and scenes with prosocial content). First, these studies found reduced ACC and vmPFC activity in response to emotional versus neutral scenes among the IPV-PTSD mothers compared to controls. The ACC and vmPFC have been linked to the appraisal of emotional stimuli and also to a more direct—and potentially subconscious—modulation of limbic system activity (i.e., “raw emotion”). This reduced ACC and vmPFC activity among IPV-PTSD individuals is likely linked to reduced emotional awareness and alexithymia (Frewen et al. 2008). In other words, the brain of IPV-PTSD mothers may have trouble correctly appraising and differentiating the way it has to adjust raw emotional arousal levels when scenes are menacing rather than prosocial.
The two studies cited above by Moser et al. (2015a, b) paradoxically found that ACC and vmPFC activity was negatively correlated with maternal sensitivity as coded from videotaped mother-toddler interactions utilizing a standard coding system in response to menacing adult male-female interactions versus positive, prosocial adult male-female interactions; in contrast, a different aspect of the mPFC, namely, dorsal mPFC activity was positively correlated with maternal sensitivity. This finding points to complex differences within the medial prefrontal cortex activation pattern that emerges in response to these emotionally evocative stimuli of both negative and positive valence with respect to maternal sensitivity, an attachment system-related variable as opposed to maternal IPV-PTSD, a fear-conditioning circuit-related variable (i.e., both vmPFC and dmPFC activity are negatively associated with maternal IPV-PTSD severity; see Schechter et al. 2012, 2015a, b). This differentiated reactivity of the vmPFC versus dmPFC in response to these emotionally evocative adult male-female interaction stimuli was found to be evident, independently of whether mothers were healthy (i.e., non-PTSD) controls or had a diagnosis of IPV-PTSD. One possible interpretation of this finding is that accurate appraisal of socio-emotional stimuli involves the vmPFC and dmPFC but that they may activate differently depending on the stimuli. In controls, the dmPFC has been linked to emotion regulation of both positively and negatively valenced stimuli (Viinikainen et al. 2010) and is generally linked to executive functions. The latter support a range of socio-emotional regulatory capacities. Evidence that these above findings are indeed directly relevant for parenting comes from several studies. These studies compared again IPV-PTSD mothers to healthy controls (HC) and exposed them to video stimuli of their own children and unfamiliar children during stressful (separation) and non-stressful (play) mother-child interactions (Schechter et al. 2012; Schechter et al. 2015; Moser et al. 2013). The IPV-PTSD mothers’ vmPFC activity was negatively correlated to reported parenting stress, that is, the less vmPFC activity, the more reported parenting stress (Schechter et al. 2015a). Thus, vmPFC in mothers with IPV-PTSD activity is related to both maternal sensitivity and how stressed mothers feel in their caregiving role. This finding again suggests that IPV-PTSD mothers are at a psychobiological disadvantage, when it comes to the appraisal of socio-emotional scenes, including those that take place during interactions with their children.
In addition to prefrontal cortex activation changes, self-reported stress in mothers with IPV-PTSD was also associated with greater limbic activity (emotion expression, Schechter et al. 2012). The limbic system is highly important to emotion expression, and limbic hyperreactivity has been shown to be related to PTSD symptoms of hyperarousal (Fonzo et al. 2010). Because one of the regions involved is the hippocampus, a region usually related to memory, one might hypothesize that IPV-PTSD mother’s viewing of children during separation may trigger patterns of neural activation similar to those triggered in response to traumatic reminders among adult PTSD patients.
With an eye toward psychotherapeutic intervention informed by clinical neuroscientific findings, the Geneva study on IPV-PTSD and Brain Circuitry points to the importance of addressing the appraisal of socio-emotional stimuli among mothers with IPV-PTSD. Too little accurate appraisal may keep the mother from considering the child’s perspective and from responding sensitively to her child’s behavior. It may cause difficulty for the affected mother to realize when a situation triggers child distress but is not life-threatening (i.e., non-menacing). For example, a laboratory mother-child separation does seem dangerous to the toddler, who does not yet have the ability to understand that his mother leaving the room does not mean that she has abandoned him or disappeared forever, yet it is important for the mother to distinguish that this situation while stressful for her toddler is not life-threatening and can be overcome. One avenue toward effective intervention with traumatized caregivers is to focus on improving the accuracy of their appraisal of emotional communication, particularly of communication by the child that may trigger parents’ own trauma-related memories.

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