Maternal Neglect: Oxytocin, Dopamine and the Neurobiology of Attachment

“Yet, while DA neurons function as general-purpose stimulators to reward-related targets, it is their close links with OT receptors in striatum, where OT receptors abound [18,19], that imbue attachment bonds with incentive value and direct action toward affiliative goals, such as maternal care [9,20,21].”

“Alternatively, given the central role of the mesolimbic dopamine system in attachment-related behavior (Strathearn, 2011), the absence or unpredictability of an attachment figure in early development may reduce opportunities for learning about the rewarding nature of affiliative interactions and social bonds; the abse…”

“…responses to infant cues (Lenzi et al., 2013; Riem, Bakermans-Kranenburg, van IJzendoorn, Out, & Rombouts, 2012; Strathearn, 2011; Strathearn, Fonagy, Amico, & Montague, 2009), as well as to differences in peripheral oxytocin response to infant contact (Strathearn, 2011; Strathearn et al., 2009).”

“Whereas striatal DA responses to natural rewards, such as infants’ cues, may be blunted in animals exposed to lower levels of maternal caregiving (Champagne et al., 2004; Strathearn, 2011), responses to stress and stimulant drugs appear to be increased.”

“35 In addition, subtle emotional maltreatment because of psychologically unavailable parents may be associated with poor attachment, behavioural problems and academic difficulties.”

“Recent developments in the neuroscience of addiction and parenting suggest a significant overlap in the neural circuitry involved with chronic drug use and parenting (Rutherford, Williams, Moy, Mayes, & Johns, 2011; Strathearn, 2011; Strathearn, Fonagy, Amico, & Montague, 2009).”

“Finally, Strathearn (2011) stressed the role of the dopamine reward system in the effects of OT on maternal neglect and in line with these ideas Riem et al. (2012) showed that activation of the reward system by laughing infants reduced amygdala activation but enhanced functional connectivity…”

“In the mother, the connection of the dopaminergic and oxytocinergic systems enable her to correctly process the sensory cues she received from the infant, and respond accordingly (Strathearn, 2011).”

“Importantly, although oxytocin facilitates the onset and maintenance of maternal caregiving behavior, the quality of the caregiving environment itself, stimulates the development of the oxytocinergic system in the offspring (Strathearn, 2011).”

“…have suggested the involvement of both oxytocinergic and dopaminergic reward systems as the neurobiological basis of neglect in childhood, associating behaviors such as anhedonia to the development of the attachment system in childhood on a neurobiological level (Strathearn, 2011; Rilling, 2013).”

“the Hypothalamo-Pituitary-Adrenal (HPA) axis (Julius, Beetz, Kotrschal, Turner, & Uvnäs-Moberg, 2013; Strathearn, 2011).”

“Furthermore, evidence from both animal and human studies suggests strong interactions of the OT and the dopaminergic system in the context of social behavior (Baskerville & Douglas, 2010 ; Strathearn, 2011).”

“In addition to being an anxiolytic and potentially increasing perceptual salience of social cues, OXT may exert its effects on social behavior via a third mechanism: increased reward sensitivity (Leckman, 2011; Strathearn, 2011; Dolen et al., 2013).”

“The current understanding is that OT circuits interact closely with dopaminergic circuits to regulate the expression of maternal behavior (Shahrokh et al., 2010; Strathearn, 2011).”

“, 2013) there is a variety of “hard-wired” oxytocinergic nerve fibers from the hypothalamus to limbic, mesencephalic, and cortical brain regions that allow fine-tuned and fast modulation of target structures (Knobloch et al., 2012; Landgraf and Neumann, 2004; Stoop, 2012; Strathearn, 2011).”

“The oxytocin system is one of the systems important to mothering (Galbally et al. 2011; Strathearn 2011) and is also likely important in the context of breastfeeding (Jonas et al.”

“Researchers found that shortly after birth, oxytocin release may enhance maternal parenting behaviors (Strathearn, 2011).”

“For instance, neuroimaging research has found that (among both parents and nonparents) the perception of young children stimulates increased activity in the dopaminergic reward pathway (Bartels & Zeki, 2004; Caria et al., 2012; Strathearn, 2011).”

“oxytocinergic system has received attention as a key neural substrate of maternal caregiving, involved in the emergence and maintenance of maternal behaviors (Feldman, 2012; Strathearn, 2011).”

“Thus, oxytocin may be an important moderator (but not a mechanism) of reward-stress interactions via its interactive role with the dopamine and opioid systems (Onaka et al., 2012; Strathearn, 2011; Tops et al., 2014).”

“…of parenthood on neural activation has received recent attention, most of the studies have focused on the activation of neural regions during active motherhood and less so on the potential longterm changes in neural activation associated with a prior parity (Strathearn, 2011; Kim et al., 2014).”

“This preclinical literature suggests that the use of synthetic oxytocin in the peripartumperiodmayhave long-termeffects on mood in both mothers and their offspring and led to the recent introduction of oxytocin manipulations as potential therapeutic targets for the treatment of postpartum psychiatric disorders (Bell,…”

“Adding a neurobiological component to this model, either at the distal level of caregiver experiences (e.g., Fonagy, 2012; Strathearn, 2011; Strathearn, Fonagy, Amico, & Montague, 2009; Strathearn, Iyengar, Fonagy, & Kim, 2012; Strathearn, Li, Fonagy & Montague, 2008) or at the more proximal level…”

“Consistent behavioral evidence indicates that OT can improve maternal attachment, parenting styles, tolerance to normal post-partum stress and at the same time reduce neglect.(26) Some of these effects have been related to changes in regional brain activation using fMRI.”

“, 2001), a hormone implicated in facilitating maternal behaviors (Strathearn, 2011).”

“In addition, decreased responsiveness of the dopaminergic and oxytocinergic systems was found in mothers showing emotional neglect (Strathearn, 2011).”

“In particular, the central increase in oxytocin levels may contribute to the generation of mother–infant bonding, which may be associated with an increase activation of oxytocin and dopamine pathways in the brain (Nissen et al., 1998; Strathearn, 2011).”

“…oxytocin, hormonal factors, and sensory (tactile and olfactory) cues from pups, as well as pheromonal and ultrasonic cues from intruder males (AngoaPérez et al., 2014; Angoa-Pérez & Kuhn, 2016; Pawluski, Li, & Lonstein, 2019; Pruessner, Champagne, Meaney, & Dagher, 2004; Strathearn, 2011).”

“Oxyto-cinergic neurons project to brain regions involved in social and maternal behavior [30].”

“Optimal maternal caregiving responses may involve both sensitive attunement to infant cues, via oxytocin-mediated mechanisms, and decision making and planning to meet the temporal needs of a family, as mediated by the nigrostriatal dopaminergic system (Strathearn, 2011).”

“…of mother–infant interactions including breastfeeding (Altemus, 1995; Carter et al., 2001) and mother–infant bonding (Carter, 1998; Feldman, 2012), andmaybe involved in postpartumwomen's increased responsiveness to infant stimuli (Carter et al., 2007; Galbally et al., 2011; Strathearn, 2011).”

“(36) © 2011 The Author, Journal of Neuroendocrinology.”

“Thus, it is hypothesized that both insecure attachment and substance abuse may affect maternal brain and behavior (125).”

“…suggest involvement of oxytocin, and adenosine through adenosine A2A receptors, in modulating DA-mediated maternal behavior (Afonso et al. 2009; Douglas 2010; Nissen AC C EP TE D M AN U SC R IP T et al. 1998; Olza-Fernández et al. 2014; Pereira et al., 2011; Shahrokh et al. 2010; Strathearn 2011).”

“Specifically, addiction and attachment may engage the mesocorticolimbic and nigrostriatal dopaminergic systems as well as the oxytocinergic system (BuismanPijlman et al., 2014; Johns, Lubin, Walker, Meter, & Mason, 1997; Strathearn, 2011).”

“28 It has been proposed that difficulties in social cognition are underpinned by disruption in the amygdala and the dopamine and oxytocin circuitry linked to socio-emotional processing, which are also implicated in schizophrenia.”

“Infusions of oxytocin in the VTA result in increased dopamine release within the ventral striatum along with increased maternal behaviors, whereas the injection of an oxytocin antagonist results in the opposite behavior of maternal neglect (Strathearn 2011).”

“Neglecting of a child’s emotional needs in early infancy can alter the development of brain reward and oxytocin systems [53], which can have negative consequences on later health.”

“Maternal love is accompanied by activation in areas of the OT system (Bartels and Zeki, 2004; Strathearn, 2011).”

“Further understanding the underlying biologic processes may help future prevention and interventions of child neglect (6).”

“Developments in the neuroscience of addiction and parenting suggest a significant overlap in the neural circuitry involved with chronic drug use and parenting (Rutherford, Williams, Moy, Mayes, & Johns, 2011; Strathearn, 2011; Strathearn, Fonagy, Amico, & Montague, 2009).”

“Motherhood provides the earliest laboratory for infant social learning, and plays a critical role in shaping infant socio-emotional development (Sroufe, 2005; Feldman, 2007; Strathearn, 2011; Mills et al., 2013).”

“Similar connections are taking place in the maternal brain; this now also includes dopamine centers, which are fundamental to all other parenting circuits (Strathearn, 2011).”

“Interestingly, single nucleotide polymorphisms of the mu-opioid receptor modulate levels of attachment in many different species (Shayit, Nowak, Keller, & Weller, 2003; Warnick, McCurdy, & Sufka, 2005), as does oxytocin (Strathearn, 2011).”

“Oxytocinergic neurons project to brain regions involved in social and maternal behavior (Gimpl and Fahrenholz, 2001; Strathearn, 2011).”

“High-quality maternal care is vitally important for newborn survival and their behavioural and metabolic health later in life, evidenced by the catastrophic consequences when maternal care is poor or absent [1–3] (S1 Table).”

“Oxytocin has been associated with maternal caregiving behavior (Strathearn, 2011), which in turn is crucial for infant social and emotional development (for review see Cassidy, 2008).”

“Less than optimal adjustment to motherhood has increasingly been linked uthor M anuscript A uthor M anuscript A uthor M anuscript to OT-related dysfunctions (Kim, 2015; Strathearn, 2011).”

“Such findings converge in a model suggesting that a general function of OT is to modulate the perceptual salience of social signals by enhancing attention orienting to social cues through interactions with the dopaminergic system (Shamay-Tsoory and Abu-Akel, 2016; Strathearn, 2011).”

“The dopaminergic reward system in the midbrain is crucial for the motivation of caregiving in new mothers (Numan and Numan 1997; Strathearn 2011).”

“Interaction with their offspring, in the postpartum period further stimulated oxytocin response in mothers (Feldman et al., 2010, 2011), though significant interindividual variations have been found in the oxytocin plasma levels (Strathearn, 2011; Strathearn et al., 2012).”

“The cocktail of neurochemicals discussed above including oxytocin, vasopressin, endorphins and dopamine likely contribute to the increasing circle of social awareness in maternal mammals [20,94,95].”

“Studies have found, for example, that oxytocin is reduced in insecurely attached and emotionally neglected children (Strathearn, 2011; Wismer Fries et al., 2005).”

“This increased vulnerability seems to be related to brain monoaminergic dysfunction which includes an altered dopamine (DA) signaling from the ventral tegmental area (VTA) (Authement et al., 2015; Heim and Nemeroff, 2002; Pena et al., 2017; Sinha, 2008; Strathearn, 2011).”

“In addition to the psychological changes from an attachment perspective, motherhood is also characterized by neurobiological and hormonal changes that help establish maternal caregiving behaviors (Kim et al., 2010; Strathearn, 2011; Swain et al., 2014).”

“For example, Strathearn (2011) pointed out numerous biological influences of neglect.”

“In both human and animal studies, biological systems that contribute to maternal behavior have been identified, focusing on the oxytokinergic and dopaminergic systems, as oxytocin activates dopamine pathways in response to social cues [103].”

“Postpartum infant stimuli perpetuate a profound maternal morphological and functional neuroplasticity, which begins with pregnancy and birth [74,75].”

“brains, leading to impaired parental care giving in the subsequent generation [29].”

“…interactions are essential for the proper neurobehavioral development of the offspring, and disruptions in these relationships may result in neuroendocrine, neurochemical, and behavioral alterations in adulthood (Hanson et al. 2013; Insel & Young, 2001; Manduca et al. 2012; Strathearn, 2011).”

“…prairie voles, sheep, and primates including humans (Feldman, Gordon, Schneiderman, Weisman, & Zagoory-Sharon, 2010; Kendrick, Keverne, & Baldwin, 1987; Maestripieri, Hoffman, Anderson, Carter, & Higley, 2009; Neumann, 2008), and it reduces the occurrence of maternal neglect (Strathearn, 2011).”

“In another neuroimaging study by Strathearn, reduced activation of the mesocorticolimbic dopamine pathways was found in mothers with insecure or dismissed attachment [59].”

“For example, noting the low base rates of oxytocin in neglectful mothers, Strathearn and colleagues [42] are”