Bidirectional Effects of Mother-Young Contact on the Maternal and Neonatal Brains

Abstract

Adaptive plasticity occurs intensely during the early postnatal period through processes like proliferation, migration, differentiation, synaptogenesis, myelination and apoptosis. Exposure to particular stimuli during this critical period has long-lasting effects on cognition, stress reactivity and behavior. Maternal care is the main source of social, sensory and chemical stimulation to the young and is, therefore, critical to "fine-tune" the offspring's neural development. Mothers providing a low quantity or quality of stimulation produce offspring that will exhibit reduced cognitive performance, impaired social affiliation and increased agonistic behaviors. Transgenerational transmission of such traits occurs epigenetically, i.e., through mechanisms like DNA methylation and post-translational modification of nucleosomal histones, processes that silence or increase gene expression without affecting the DNA sequence. Reciprocally, providing maternal care profoundly affects the behavior, learning, memory and fine neuroanatomy of the adult female. Such effects are in many cases permanent and sometimes they involve the hormones of pregnancy and lactation. The above evidence supports the idea that the mother-young dyad exerts profound and permanent effects on the brains of both adult and developing organisms, respectively. Effects on the latter can be explained by the neural developmental processes taking place during the early postnatal period. In contrast, little is known about the mechanisms mediating the plasticity of the adult maternal brain. The bidirectional effects that mother and young exert on each other's brains exemplify a remarkable plasticity of this organ for organizing itself and provide an immense source of variability for adaptation and evolution in mammals.

Maternal Regulation of Pups’ Cortical Activity: Role of Serotonergic Signaling

“…As highlighted by Kolb et al (2012) , the PFC has an extended developmental period and early life experience, such as maternal care, can critically shape this development leading to long-term consequences in adulthood. Indeed, it has been shown that maternal separation leads to modification of the dendritic arborization in PFC pyramidal neurons ( Monroy et al, 2010 ; González-Mariscal and Melo, 2017 ). In addition, Chugani et al (2001) showed that institutionalized orphans display reduced glucose metabolism in prefrontal areas associated with neurocognitive deficits.…”

“…Subsequent studies have shown that handling/licking/grooming regulate glucocorticoid receptor transcription via the serotonergic system ( Mitchell et al, 1990, 1992 ; Laplante et al, 2002 ; Hellstrom et al, 2012 ). Interestingly, in rats, maternal separation decreases the 5-HIAA/5-HT ratio in PFC ( Xue et al, 2013 ; González-Mariscal and Melo, 2017 ). Relative to the different 5HT receptor subtypes, it has notably been shown that animals subjected to maternal separation exhibit deregulation of 5-HT2R function ( Benekareddy et al, 2010 ).…”

Abnormal Serotonin Levels During Perinatal Development Lead to Behavioral Deficits in Adulthood

“… Arborelius and Eklund (2007) found that maternal separation (P1-P13) modified the tissue levels of 5-HT and 5-HIAA in the dorsal raphe nucleus (both increased during long maternal separation) and in the amygdala (decreased during brief maternal separation) of adult female rats. Moreover, the 5-HIAA/5-HT ratio in the rat prefrontal cortex was decreased by maternal separation ( Xue et al, 2013 ; Gonzalez-Mariscal and Melo, 2017 ). Analysis of the metabolite/monoamine turnover ratio is a useful estimator of serotonergic activity.…”

Early postnatal development of electrophysiological and histological properties of sensory sural nerves in male rats that were maternally deprived and artificially reared: Role of tactile stimulation

“…Manipulations that result in increased maternal grooming, such as the early handling paradigm, improve maternal responsiveness in the adult offspring, in addition to decreasing anxiety and fearfulness, and promoting better spatial learning and improving adaptive responses to a novel environment (Pryce et al, 2001a,b;Arnold and Siviy, 2002;See Melo, 2015). Opposite effects have been reported for manipulations in which pups were repeatedly separated from the nest for longer periods of time (1, 3, or 6 h per day; the partial maternal separation paradigm), or were completely deprived of maternal contact, in the AR paradigm Pryce et al, 2005;see Cirulli et al, 2003;Melo, 2015;Lomanowska and Melo, 2016;Gonz alez-Mariscal and Melo, 2017). AR is a novel experimental paradigm that is useful to assess the participation of distinct classes of stimuli (sensory, social or hormonal) associated with the mother-infant interaction, while eliminating confounding effects that are present in other deprivation paradigms (e.g., chronic stress or undernourishment; Gonzalez et al, 2001;Ward et al, 2004;Melo et al, 2006Melo et al, , 2009Lomanowska et al, 2011;Lomanowska and Melo, 2016).…”