Mother-Young Bonding: Neurobiological Aspects and Maternal Biochemical Signaling in Altricial Domesticated Mammals

Abstract

Mother-young bonding is a type of early learning where the female and their newborn recognize each other through a series of neurobiological mechanisms and neurotransmitters that establish a behavioral preference for filial individuals. This process is essential to promote their welfare by providing maternal care, particularly in altricial species, animals that require extended parental care due to their limited neurodevelopment at birth. Olfactory, auditory, tactile, and visual stimuli trigger the neural integration of multimodal sensory and conditioned affective associations in mammals. This review aims to discuss the neurobiological aspects of bonding processes in altricial mammals, with a focus on the brain structures and neurotransmitters involved and how these influence the signaling during the first days of the life of newborns.

Keywords: bonding; imprinting; maternal anogenital licking; maternal recognition; olfactory; vocalization.

Figure 1

Neurodevelopmental differences between altricial, precocial, and semi-altricial species. According to the type of species, newborns from altricial, precocial, and semi-altricial females establish a different degree of bonding. In the case of precocial species, whose cerebral development starts during gestation, the time they require for maternal nursing is shorter since they can stand and move freely almost immediately after birth. In contrast, the maturation of sensorial systems in altricial species occurs during the postnatal period, where they are completely dependent on the mother to survive. Semi-altricial species are in between; while some of their senses are functional at birth, the mother nurses them until they are highly independent after several days after parturition.

Figure 2

Neurobiology of maternal behavior in altricial species. To develop a maternal response in females, a series of neuroendocrine and sensorial stimuli need a dual interaction in cerebral structures, such as the MPOA, BNST, VTA, AMY, VNO, and OB, among others, to suppress aggressive and avoidance behaviors, while activating appetitive and motivational maternal pathways. AHN: anterior hypothalamic nucleus; BNST: bed nucleus of the stria terminalis; cFos: transcription factor and marker of neuronal activity; DA: dopamine; GABA: gamma-aminobutyric acid; FosB: Fos protein; MeA: medial amygdala; MOE: main olfactory epithelium; MPOA: Medial PreOptic Area; OB: olfactory bulb; PAG: periaqueductal gray; VNO: vomeronasal organ; VP: ventral pallidum.

Figure 3

Influence of pain and aversion on maternal behavior in altricial species. Although pain is a physiological trait in the parturition process, if dystocia occurs and the pain is prolonged in the mother, the activation of nociceptors (A-delta and C fibers) activates the sympathetic nervous system, and the consequent release of catecholamines and glucocorticoids. Moreover, the conscious recognition of pain in the somatosensorial cortex alters maternal behavior and reduces milk production, resulting in a negative trait for both the mother and the offspring. On the other hand, the activation of aversion pathways in non-parturient females prevents them from maternal responsiveness. However, in species such as rodents, short periods of pup exposure elicit similar responses in multiparous, parturient, and lactating animals. EPN: entopeduncular nucleus; LH: lateral hypothalamus; LHb: lateral habenula; LPO: lateral preoptic area; MS: medial septal nucleus; PFC: prefrontal cortex; VP: ventral pallidum; VTA: ventral tegmental area.