Mother-infant bonding and the evolution of mammalian social relationships

Abstract

A wide variety of maternal, social and sexual bonding strategies have been described across mammalian species, including humans. Many of the neural and hormonal mechanisms that underpin the formation and maintenance of these bonds demonstrate a considerable degree of evolutionary conservation across a representative range of these species. However, there is also a considerable degree of diversity in both the way these mechanisms are activated and in the behavioural responses that result. In the majority of small-brained mammals (including rodents), the formation of a maternal or partner preference bond requires individual recognition by olfactory cues, activation of neural mechanisms concerned with social reward by these cues and gender-specific hormonal priming for behavioural output. With the evolutionary increase of neocortex seen in monkeys and apes, there has been a corresponding increase in the complexity of social relationships and bonding strategies together with a significant redundancy in hormonal priming for motivated behaviour. Olfactory recognition and olfactory inputs to areas of the brain concerned with social reward are downregulated and recognition is based on integration of multimodal sensory cues requiring an expanded neocortex, particularly the association cortex. This emancipation from olfactory and hormonal determinants of bonding has been succeeded by the increased importance of social learning that is necessitated by living in a complex social world and, especially in humans, a world that is dominated by cultural inheritance.

Figure 1

The importance of hormones for signalling context across and synchronizing biologically relevant events in the brain and somatic compartments.

Figure 2

Convergence of main and accessory olfactory systems for distinguishing and appropriately engaging behaviour through the NAcc/ventral striatal ‘reward’ system. The hormones of pregnancy upregulate oxytocin receptors (filled circle) and opioid (open circle) receptors which provide the ‘maternal’ context. AMY (BL), basolateral amygdala; AMY (Me), medial amygdala; 5HT, 5-hydroxytryptamine; VMN, ventromedial nucleus.

Figure 3

(a) A substantial number of olfactory receptors are coded for by non-functional pseudogenes which increase in number with the enhanced development of the neocortex. (b) Congruent with this reduction in olfactory receptors, there is a reduction in the proportion of cortex given over to processing olfactory information. This decreases from insectivores through primates.

Figure 4

Redundancy in the olfactory systems together with increases in the volume of the prefrontal cortex provide for complex polymodal cues to address the ventral striatal ‘reward’ system. Emotionally arousing cues (infant distress cries, infant faces and infant suckling) signal release of DA in the ventral striatum both within and beyond the context signalled by the hormones of pregnancy.