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Journal of Child Psychology and Psychiatry 52:4 (2011), pp 368–397 doi:10.1111/j.1469-7610.2010.02306.x

Annual Research Review: All mothers are not created equal: neural and psychobiological perspectives on mothering and the importance of individual differences

Jennifer Barrett and Alison S. Fleming

Department of Psychology, University of Toronto at Mississauga, Mississauga, Ontario, Canada

Quality of mothering relies on the integrity of multiple physiological and behavioral systems and on two maternal factors, one proximal and one distal, that have a great impact on how a mother mothers: postpartum depression and early experiences. To mother appropriately requires the action of systems that regulate sensation, perception, affect, reward, executive function, motor output and learning. When a mother is at risk to engage in less than optimal mothering, such as when she is depressed or has experienced adversity in childhood, the function of many or all of maternal and related systems may be affected. In this paper, we will review what is currently known about the biological basis of mothering, with attention to literature on hormones but with a particular focus on recent advances in the fields of functional neuroimaging. Instead of discussing strictly ‘maternal’ brain imaging studies, we instead use a systems approach to survey important findings relevant to brain systems integral to and/or strongly related to the mothering experience: (a) social behavior; (b) reward and affect; (c) executive function; and

(d) maternal behavior. We find that there are many commonalities in terms of the brain regions iden- tified across these systems and, as we would expect, all are sensitive to the influence of, or function differently in the context of, depression and adverse early experience. It is likely that the similarity and cross-talk between maternal, affect and stress systems, observed behaviorally, hormonally and in the context of brain function, allows for mood disturbance and early adverse experiences to have a signif- icant impact on the quality of mothering and the motivation to mother. Keywords: Adversity, maternal depression, brain imaging, parenting, mothers.

The interaction between a mother and her infant can be like a dance. There are routines, standards and missteps, there is give and take, there is unparalleled intimacy, there are often vast differences in skill level and motivation, there is learning. A mother must learn to be an adept partner, being sensitive to the needs of her offspring while ultimately guiding the quality and nature of care to ensure normal growth and development. This dance can beautiful, it can be tender, it can be awkward, it can be difficult. And sometimes it just does not occur!

Romanticism aside, the mother–offspring dance is influenced by and interacts with many factors, including mothers’ physiology, cultural and family context, maternal cognitions, maternal affect and stress and the early environment, notably a mother’s own early experiences in her family of origin. Bio- logical influences certainly include how mothers’ brains are organized and how genes and environ- ment interact in brain development. It is believed that over the course of pregnancy and through the postpartum period, changes in the levels of certain hormones likely ‘activate’ or affect key brain regions to ensure that the mother is especially attracted to her baby, that she is attentive and sensitive to her

Conflict of interest statement: No conflicts declared.

baby’s needs, that she learns from her experiences and that she behaves appropriately.

In humans, across cultures there exist as many differences as similarities in the ways that mothers interact with their infants (Leiderman & Leiderman, 1977). In some cultures the infants are carried in cradleboards on the mothers’ backs; in others they are carried in a pouch or sling on the mothers’ ventrum; in many Western cultures, especially if the terrain is smooth, infants are transported in strollers or perambulators (Anisfeld, Casper, Nozyce, & Cunningham, 1990; Chisholm, 1978). Customs relating to sleeping also vary across cultures, from swaddling, sleeping in the mother’s bed, to sleeping in a cot next to the mother, to sleeping away from the mother in another room (Van Sleuwen et al., 2007; Thoman, 2006). Mothers also exhibit a range of dif- ferent kinds of communicative responses to their infants: some look at them directly while others gaze avert (Brazelton, 1977); some keep their babies unclothed and stroke their bodies; others swaddle them instead (see Corter & Fleming, 2002). Some talk or sing to their babies; others do not (Tronick, 1987). Soothing methods, for example pacifier use or use of specific herbs or teas, can greatly vary by culture (Abdulrazzaq, Kendi, & Nagelkerke, 2009). More subtly, within a culture mothers show large variations in the postpartum development of

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Neurobiological perspectives on mothering 369

nurturant feelings, from minutes to months (Leifer, 1980; Moss & Jones, 1977; Robson, 1967; Robson & Kumar, 1980; Trevathan, 1983), and, once ‘attached’ or emotionally committed, in the intensity with which they exhibit different caregiving behaviors. Within all cultures most mothers are motivated to provide warmth, shelter, and food to the infant while in all cultures there are mothers who neglect or even abuse their infants (see Corter & Fleming, 2002; Hrdy, 2005, 2009).

Despite these differences, in most cultures moth- ers nurse their infants, although there are some mothers in each that may also bottle-feed (Kannan, Carruth, & Skinner, 2004; Pak-Gorstein, Hak, & Graham, 2009; Thulier, 2009). In many different cultures, mothers engage in a form of expression called ‘motherese’, where the mother talks to the infant in a high prolonged pitch and sings with a characteristic cadence and rhythm (Trehub, Unyk, & Trainor, 1993). In most cultures mothers provide kinesthetic stimulation by stroking and rocking the baby and respond contingently to infant cries and other indices of distress, often by vocalizing ‘in response’ (Ainsworth, Bell, & Stayton, 1974; Corter & Fleming, 2002; Pederson et al., 1990). Here we will not address the issue of cross-cultural differences, important though they are (Cote & Bornstein, 2009; Gu¨ ngo¨r & Bornstein, in press). Instead we focus on the cross-cultural similarities and focus most dis- cussion on studies that describe mothers from Western and industrialized societies, where most of the psychobiological research has occurred (see the work of Marc Bornstein for a program of research well suited to a cross-cultural analysis).

For this paper our primary focus is reflected in the idea that mothering is not unitary, but is instead complex, and comprised of many behavioral pro- pensities that are mediated, moderated, and regu- lated by multiple physiological and brain systems. To engage in mothering behavior, mothers have to be sensitive to infant cues and select those cues for processing, utilizing multiple sensory and percep- tual modalities; the cues must be attractive and salient for the mother, recruiting reward and approach systems. Mothers must be emotionally prepared and positively motivated to engage socially with the infant, depending on systems regulating affect. They must selectively attend to the offspring in the context of competing stimuli, enacted through systems that regulate attention; and they must be restrained and consistent in their responsiveness, depending on systems that regulate impulsivity. Finally, mothers gain through experiences, acquired both early in life and with young as juveniles and in adulthood. These experiences are acquired, consoli- dated, and stored as motor or sensory memories and are based on extensive brain plasticity.

Thus, to mother appropriately requires the action of multiple systems in the domains of sensation, perception, affect, reward, executive function, motor

output and learning. When a mother is at risk to engage in less than optimal mothering, such as when she is depressed or has experienced adversity in childhood, the function of many or all of these sys- tems may be affected. In this paper, we will use a systems approach to review and critique what is currently known about the biological basis of moth- ering, with a particular focus on recent advances in the field of functional neuroimaging. We will often combine information from the animal world with the human. We will briefly review what has informed knowledge of the neurobiology of mothering up until this point (hormones). Finally, whenever possible, we will try to put these basic mechanisms into the context of important individual differences related to maternal psychopathology (depression) and early adversity.

I. Maternal behavior is affected by mothers’ cognitions, executive function, and theory of mind
Overview

How mothers relate to their infants is affected by multiple psychological propensities, including her cognitive style and her affective state. In this first section we discuss individual differences related to cognitive functions: functions that are thought to provide an important foundation for quality of mothering and maternal behavior and are also, in many cases, known to interact with affect/mood and early experiences. Processes such as cognitive flexi- bility, working memory and attentional control are fundamental components of mothering and key to maternal sensitivity. A mother must have the atten- tional command to focus on her infant which allows her to be sensitive to infant needs, that is, to respond contingently, appropriately and in a timely manner. She must also have the cognitive flexibility to switch her attention…