Neuroendocrine Mechanisms Underlying the Intergenerational Transmission of Maternal Behavior and Infant Abuse in Rhesus Macaques

Abstract

SummaryParenting style in rhesus macaques (Macaca mulatta) can vary dramatically among individuals along the two orthogonal dimensions of maternal protectiveness and maternal rejection. High rates of maternal rejection can be accompanied by infant abuse. We investigated the effects of exposure to variable parenting styles on offspring behavioral and neuroendocrine development to identify the possible mechanisms underlying the intergenerational transmission of maternal behavior and infant abuse. Forty-three non-crossfostered male and female infants and 16 crossfostered female infants were followed through their first three years of life or until they reproduced for the first time.Half of the infants were reared by abusive mothers and half by nonabusive controls. Cerebral spinal fluid (CSF) concentrations of the serotonin metabolite, 5-HIAA, were measured at six-month intervals. Abused infants were rejected more by their mothers than controls, and infants exposed to higher rates of maternal rejection had significantly lower CSF 5-HIAA in the first three years of life. When the crossfostered females gave birth for the first time, their rates of maternal rejection matched those of their foster mothers and were negatively correlated with CSF 5-HIAA. Approximately half of the females reared by the abusive mothers exhibited abusive parenting, whereas none of the females reared by controls did. The abused females who became abusive mothers had lower CSF 5-HIAA than the abused females who did not. These findings provide evidence that maternal rejection and infant abuse are transmitted across generations and suggest that experience-induced, long-term alterations in brain serotonergic function may play an important role in the intergenerational transmission of normal and abnormal parenting.

Interaction of serotonin transporter linked polymorphic region and childhood neglect on criminal behavior and substance use for males and females

“…Studies have shown that females, on average, exhibit higher levels of HPA axis activity (Young, Korszun, Figueiredo, Banks-Solomon, & Herman, 2007) and lower levels of serotonin activity than males (Biver et al, 1996;Fischette, Biegon, & McEwen, 1983;Rubinow, Schmidt, & Roca, 1998). Further, nonhuman primate research has revealed that maltreated subjects who carry a copy of the short allele exhibit lower levels of 5-hydroxyindoleacetic acid, exhibit higher levels of ACTH responses to stress, and exhibit more aggressive and anxious behaviors in response to stress than maltreated subjects who do not carry a copy of the short allele (Maestripieri, 2005;McCormack et al, 2009). These negative effects have been shown to be more pronounced for females than males (Barr, Newman, Schwandt, et al, 2004).…”

“…Bennett et al's (2002) analysis of 132 rhesus macaques revealed that subjects who carried a short allele and who experienced maternal separation had lower cerebrospinal fluid 5-hydroxyindoleacetic acid concentrations than separated subjects who did not carry a short allele. Lower serotonin activity resulting from the interaction of 5-HTTLPR and maltreatment is somewhat expected given the animal literature that (a) maltreatment is associated with lower levels of serotonin (Champagne & Curley, 2009;Ichise et al, 2006;Maestripieri, 2005;Matthews, Dalley, Matthews, Tsai, & Robbins, 2001) and (b) the short allele of 5-HTTLPR is associated with lower levels of overall serotonin activity (Williams et al, 2001), by way of the short allele leading to fewer serotonin transporters, less reuptake of serotonin from the synaptic cleft, and the subsequent downregulation of postsynaptic receptors (David et al, 2005;Lesch et al, 1996). The lack of inhibition that may arise from lower serotonin activity, coupled with a greater sensitivity to stress from a hyperactive HPA axis, may increase the likelihood that maltreated individuals who carry the short allele will engage in disruptive and maladaptive behaviors (i.e., substance use, depression; Andersen & Teicher, 2009).…”

Adolescent risk taking, impulsivity, and brain development: Implications for prevention

“…Suomi's research with rhesus monkeys that are either reared by their mothers or by much less nurturant peers finds that peer-reared males exhibit greater externalizing behavior in adolescence (Suomi, 1997). In research with rhesus macaque monkeys, Maestripieri and colleagues have examined neurobehavioral effects of maternal abuse and neglect on offspring (Maestripieri, 2008). They also find that maternal maltreatment is transmitted by behavior rather than genetics.…”

The neuroendocrinology of primate maternal behavior

“…Moreover, the abused females, both crossfostered and non-crossfostered, who became abusive mothers had lower CSF 5-HIAA concentrations than the abused females who did not become abusive mothers (Maestripieri et al, 2006a). This finding suggests that experience-induced, long-term alterations in serotonergic function in females reared by abusive mothers may contribute to the manifestation of abusive parenting in adulthood (Maestripieri, 2008b). …”