Maternal Regulation of Infant Brain State

Abstract

Summary Patterns of neural activity are critical for sculpting the immature brain and disrupting this activity is believed to underlie neurodevelopmental disorders [1-3]. Neural circuits undergo extensive activity-dependent postnatal structural and functional changes [4-6]. The different forms of neural plasticity [7-9] underlying these changes have been linked to specific patterns of spatiotemporal activity. Since maternal behavior is the mammalian infant's major source of sensory driven environmental stimulation and the quality of this care can dramatically impact neurobehavioral development [10], we explored, for the first time, whether the infant cortical activity was influenced directly by interactions with the mother within natural nest environment. We recorded spontaneous neocortical local field potentials (LFP) in freely behaving infant rats, from postnatal days ~12-19 during natural interactions with their mother. We show that maternal absence from the nest increased cortical desynchrony. Further isolating the pup by removing littermates induced further desynchronization. The mother's return to the nest reduced this desynchrony, and nipple attachment induced a further reduction but increased slow-wave activity. However maternal simulation of pups (grooming, milk-ejection) consistently produced rapid, transient cortical desynchrony. The magnitude of these maternal effects decreased with age. Finally, systemic blockade of noradrenergic beta receptors led to reduced maternal regulation of infant cortical activity. Our results demonstrate that during early development, mother-infant interactions can immediately impact infant brain activity, in part via a noradrenergic mechanism, suggesting a powerful influence of the maternal behavior and presence on circuit development.

Stress and the social brain: behavioural effects and neurobiological mechanisms

“…Moreover, mother-infant interactions are essential determinants of a pup's corticosterone responses to stressful stimuli during early life and influence the extent to which early-life stress affects behavior and emotionality in adulthood 215,216 . In infants, changes in cortical synchrony (i.e., the level of synchronization of neural oscillations at particular frequencies, a fundamental mechanisms for enabling coordinated neural activity and essential for brain development) may be modulated by maternal contact 217 , and this might be a mechanism through which mother-infant interactions can affect circuit development.…”

Neurobiology of infant attachment: attachment despite adversity and parental programming of emotionality

“…Since it is hard to directly assess what is going on in a human infant brain, clues from animal research are helping us discover how parents regulate the infant brain. A seminal study by Sarro et al displayed for the first time that infant rat brain activity is directly influenced by interactions with the mother in their natural nest (via, in part, to a noradrenergic neurotransmitter mechanism), with the magnitude of maternal regulation decreasing with age [22]. …”

“…We argue that this sensitive period may be intimately linked to the caregiver’s ability to profoundly regulate infant physiology during typical caregiver-infant interactions [22], and in the presence of stressors by buffering infant reactivity [52] (Figure 1). In rodents, powerful maternal regulation of stress hormone reactivity and amygdala fear learning occurs throughout the first two weeks of life [7,49], and maternal regulation of infant brain state during caregiving interactions wanes as pups approach weaning [22], supporting the notion that this sensitive period is confined to infancy and childhood.…”

Pilot study demonstrates that salivary oxytocin can be measured unobtrusively in preterm infants

“…Furthermore, mothers should preferably not even be in the infants’ room during the saliva collections before Kangaroo care according to the impression that was given by the results from the interaction intensity at baseline and the intensity increase parameters. We argue that, like the sheer presence of rat dams appeared to influence the electro‐encephalogram of their pups in the study by Sarro et al 29, the sheer presence of a mother might influence the infant's baseline oxytocin measurement. However, the average oxytocin response of the mothers did not seem related to the pooled oxytocin response of their preterm infants in this pilot study.…”