Mother-young bond in non-human mammals: Neonatal communication pathways and neurobiological basis

Abstract

Mother-young bonding is a process by which the young establish social preferences for their mother. It fosters reproductive success and the survival of offspring by providing food, heat, and maternal care. This process promotes the establishment of the mother-young bond through the interaction of olfactory, auditory, tactile, visual, and thermal stimuli. The neural integration of multimodal sensory stimuli and attachment is coordinated into motor responses. The sensory and neurobiological mechanisms involved in filial recognition in precocial and altricial mammals are summarized and analyzed in this review.

Keywords: bonding; licking; maternal recognition; olfactory; sensitive period; visual; vocalization.

Figure 1

Tactile recognition in sheep. Tactile cues include licking the newborn, particularly during the first hour of life. By starting at the head, nose, ears, and the anogenital region, the mother encourages the offspring to stand up and consume colostrum. The endocrine response in lambs activates zones in the LC, AMY, and BNST, where an increase in noradrenergic neurons, adrenergic, oxytocin or V1a receptors occurs. AMY, amygdala; LC, locus coeruleus; NE, norepinephrine; V1a, vasopressin 1a.

Figure 2

Visual imprinting in birds. The stimulus captured by the retina is projected to the thalamus DLA and Wust, a region of the hyperpallium analogous to the mammalian primary visual cortex. Through connections to the IHA and HDCo, visual signaling reaches the IMM, the main structure involved in long-term memory, early learning, and imprinting. During the sensitive period, amounts of glutaminergic neurons and NMDAr in this zone increase to promote imprinting. AMY, amygdala; DLA, dorsolateralis anterior thalami; Dopa, dopamine nuclei; GLU, glutamate; HDCo, hyperpallium densocellulare; Hipp, hippocampus; IHA, hyperpallium apical; IMM, intermediate medial mesopallium; MSt, medial striatum; NMDAr, N-methyl-D-aspartate receptors; OT, optic tectum.

Figure 3

Olfactory signaling and processing in rabbit pups. Although pups cannot see at birth, perimammary odors are responsible for olfactory signaling in newborns. The mammary pheromone (2 MB2), a pheromone presents in sebaceous structures and released in the milk, is known to incite the head-searching and oral grasping movements of the newborn. Rabbit pups can detect the pheromone through peripheral (VNO) and central (olfactory bulb) structures of the auditory system, promoting an endocrine response that contributes to behavioral changes. GG, Grueneberg ganglion; P4, progesterone; PRL, prolactin; SOM, septal organ of Masera.

Figure 4

Olfactory mother-young recognition in rodents. During this process in neonate rats, the hypofunction of the amygdala (to block odor preference) and the greater number of noradrenergic neurons in the locus coeruleus are the main features that promote the interaction. In mothers, oxytocin secretion and its action on the MPOA, VTA, PVN, and BNST are associated with the presentation of maternal behaviors. AMY, amygdala; BNST, bed nucleus of the stria terminalis; Hipp, hippocampus; GABA, gamma-aminobutyric acid; MPOA, medial preoptic area; NE, norepinephrine; OB, olfactory bulb; PVN, paraventricular nucleus; VTA, ventral tegmental area.