In mammals, the mother-young bond formation is essential for newborn survival and involves a set of neurological, behavioral, and cognitive mechanisms. Mutual recognition between the mother and the newborn is essential to establish and maintain the bond and guarantee maternal care during the young development (Bolhuis, 2009; Mota-Rojas et al., 2021). The process of mutual recognition between the mother and the newborn involves multimodal sensory signals in the brain of both individuals and occurs during a sensitive period (Broad et al., 2006). This period is important for the mother to recognize and identify their newborn, avoiding misdirected care, reducing energy outlays, and enhancing their reproductive success. Imprinting is a process, mostly studied in birds (Vallortigara and Versace, 2018), by which newborns establish a social preference for their mother, another individual, or even an object (Hess, 1972; Ohki-Hamazaki, 2012). According to Hess (1959), the process of imprinting, observed by Lorenz in European birds, is a phenomenon also reported in other animals such as insects, fish, and some mammals (sheep, buffalo, and deer). However, in the present paper, we will deal with the bonding and interaction process between a young and its mother.

The process of mother-young recognition requires specific sensory stimuli integrated by brain structures (Bolhuis, 1999). It involves structural changes in cortical regions and the release of neurotransmitters that allow newborns to learn to identify their mother—or the individual/object imprinted—through visual, auditory, tactile, and olfactory cues (Sullivan and Wilson, 1994; Insel and Young, 2001; Debiec and Sullivan, 2017). These areas interconnect with other regions to promote the secretion of neurotransmitters associated with the behavioral responses observed during mutual bonding, such as oxytocin, gamma-amino-butyric acid (GABA), glutamate, acetylcholine, and among others (Ohki-Hamazaki, 2012). Neonatal recognition’s set time varies from a few hours to a few days depending on the species. As the mother-young interaction depends on the newborn’s locomotor, sensory, and neuronal level of development, it varies in precocial and altricial species. Offspring from precocial species (e.g., goat kids, lambs, and calves) are born fully developed, have a more developed thermoregulatory system (Muir, 2000; Glatzle et al., 2017), and thus, shortly after birth are capable of following the mother and feed with more independence (Muir, 2000; Glatzle et al., 2017). These species develop discriminative care, allowing exclusive suckling, and a clear chemosensory recognition between the offspring and the dam soon after birth (Horrell and Hodgson, 1992; Booth and Katz, 2000). On the other hand, offspring from altricial species (e.g., canids, rodents, and felines) are not fully developed and have limited sensory and locomotor abilities at birth (Lévy and Keller, 2008), requiring continuous parental protection during the first postnatal weeks, parental grooming, feeding (Scheiber et al., 2017), and in nidicolous species (e.g., rats, mice, rabbits), nesting behavior represents a protective physical barrier, delimiting the space where the mother-young interaction develops (Frohlich, 2020). In many altricial species such as canines, puppies are born with non-functional ears and eyes, and are severely limited in their capacity for mechanical movement (Czerwinski et al., 2016). The cognitive, sensory, and locomotor capacities of both precocial and altricial species are associated with prenatal neurogenesis and degrees of brain maturation (Glatzle et al., 2017).

Complementary, the imprinting process can occur between a young and a human handler, such as observed during artificial rearing in sheep (Markowitz et al., 1998) and sea lions (Lynn et al., 2010). This type of imprinting can be also used as a tool to simplify foal handling (Spier et al., 2004). In these circumstances, the young establish a preferential bond toward the human and activates neuronal pathways related to emotional bond (Coulon et al., 2013). This review aims to summarize and analyze the sensory and neuronal mechanisms of mother-young bonding in non-human mammals.

The sensitive (or critical) period is a length of time after birth for a mother to become bonded to her young. The formation of this bond depends on maternal responsiveness, social cues from members in the dyad, neuroendocrinological changes, and the display of maternal and neonatal behaviors. The establishment of a mother-young bond implies the social preference of the mother and the offspring for each other. There are several stimuli of distinct origins required for the mother-young bond, that vary according to the development of the offspring’s senses (Bolhuis, 1999; Yamaguchi et al., 2012; Lemche, 2020). At the cerebral level, a key architectural and biochemical configuration gives rise to neuronal circuits, such as the frontal cortex and excitatory neurotransmitters. These circuits participate in creating the neonatal cerebral pathways to establish stable, or preferred, connectivity patterns that act as guidelines for developing a set of behavioral patterns and strategies required for the offspring’s survival (Knudsen, 2004) and even for their adulthood traits, such as sexual behavior (Bateson, 1990). The sensitive period and the structural configuration of brain connectivity depend entirely on the degree of learning achieved. On the other hand, atypical interference can cause irreversible alterations in these brain mechanisms and, therefore, affect the establishment of the bond (Moriceau and Sullivan, 2005). Modifications of neuronal plasticity in the offspring may involve such mechanisms as synaptic consolidation through molecular adhesion cells, abolition of the activation of synapses because of the insertion of stabilizing molecules, and the construction of synapses through the growth of axons or dendrites. In addition, it has been suggested that the development of neuronal networks also requires a certain level of connectivity, or degree of brain maturity. This, however, depends on innate mechanisms, including connections close to the retina or spinal cord. It is important to note that some brain regions involved in the development of the offspring, including the amygdala, cerebral cortex, and hippocampus, maintain a constant level of plasticity throughout life so they can establish long-lasting connection patterns (Knudsen, 2004). In this regard, studies have demonstrated that in numerous mammal species, the primary visual cortex performs a selective elimination of connections in the thalamic axons and that certain actions require the participation of various brain centers (Sullivan and Wilson, 1994; Maekawa et al., 2006;Mora-Medina et al., 2018; Orihuela et al., 2021). Likewise, cascades of molecular elements have been reported to orchestrate the beginning and end of periods of mutual recognition (Sullivan and Wilson, 1994; Insel and Young, 2001; Sullivan, 2003; Moriceau and Sullivan, 2005; Debiec and Sullivan, 2017).

This process requires the integration of several sensory inputs that come together from hypothalamic structures, the limbic system, and the cerebral cortex (Mora-Medina et al., 2018; Orihuela et al., 2021). Multimodal signals are transmission pathways that allow learning using sensory stimuli (sight, hearing, smell, taste, and thermal; Glatzle et al., 2017; Mora-Medina et al., 2018; Orihuela et al., 2021). The main involved pathways are conditioned by the degree of sensory functionality characteristic of the offspring at birth (Mora-Medina et al., 2018). Dams can recognize auditory, visual, and odor signals, but newborns are conditioned by the degree of their sensory development, so they are incapable of capturing certain features of their physical and social environment until their senses and communication channels reach optimal levels of development (Muir, 2000; Werneburg et al., 2016). In altricial species, olfactory cues are essential for the onset of young-mother interaction after parturition (Poindron et al., 1988; Lévy and Nowak, 2017), and communication is practically unidirectional (Muir, 2000). For instance, rat pup-dam licking behavior is regulated by the pup’s preputial gland secretion (Brouette-lahlou et al., 1991b). However, some altricial neonates, including those of feline species, can detect odor stimuli that help them locate the mother’s mammary gland (Vitale, 2018). In mice, Al Aïn et al. (2013) elegantly demonstrated that mouse pups imprint on their own mother’s odor in utero, and these imprinted odors from the amniotic fluid improve nipple attachment of the pups by inducing nipple grasping (Workman et al., 2013). The development of neural structures in the offspring is probably related to acquiring a more functional sensitive sensibility (Workman et al., 2013; Glatzle et al., 2017).

On the other hand, the offspring of precocial species can establish communication channels only a few minutes after birth, as they can perceive sensory stimuli and perhaps even follow the mother due to their fully-developed motor neurons (Workman et al., 2013). This occurs, for example, in water buffaloes, bovine cattle, goats, and sheep. These four precocial species are classified as prey animals that are in constant movement; therefore, the young and the mother must have the ability to identify each other immediately after birth, especially in the case of large social groups (Glatzle et al., 2017; Mora-Medina et al., 2018; Orihuela et al., 2021). Overall, the communication pathways depend on the degree of neurodevelopment of the neonate (Mora-Medina et al., 2018; Orihuela et al., 2021).

During mother young interaction, communication networks induced by essential neurotransmitters develop. These networks favor the learning process of the newborn (Castro-Sierra et al., 2007; Orihuela et al., 2021). The neuropeptides involved show activation of the hypothalamus, which secretes hormones and neurotransmitters (Insel, 2010). Several neuromodulators are involved in the mutual recognition, including oxytocin, GABA, glutamic acid (GLU), monoamines such as dopamine (DA) and serotonin (5-HT), as well as N-methyl-D-aspartate (NMDA), prolactin (PRL), and BDNF (Castro-Sierra et al., 2007). For example, newborn rats should learn their mother’s odor, orient to her, select a nipple and huddle to favor its’ development (Teicher and Blass, 1977). Nevertheless, this system improves both learning and attachment while pups are confined in the nest (Sullivan, 2003; Moriceau and Sullivan, 2005). In this attachment process, there are three important structures involved: the olfactory bulb, the noradrenergic locus coeruleus, and the amygdala (Sullivan, 2003).

Oxytocin is a hormone primarily synthesized in magnocellular neurons of the PVN and supraoptic nuclei (SON) of the hypothalamus. Its connection to the posterior pituitary, where it is stored as secretory vesicles, causes its release into the bloodstream. In addition, the dendritic release of oxytocin into the extracellular space through the brain has local effects on specific tissues and biological functions. Furthermore, smaller parvocellular neurons in the PVN also produce oxytocin and have connections to other brain structures including the limbic system (notably the amygdala and hippocampus) and the nucleus accumbens. Hence, oxytocin can also act as a neurotransmitter/neuromodulator. There is also a positive autoregulation action of oxytocin itself (Meyer-Lindenberg et al., 2011). Besides, it is influenced by gonadal steroids that foster its synthesis and modulation (Sharpey-Schafer, 1933; Orsucci et al., 2013). Oxytocin binds to the oxytocin receptor present in several cerebral regions, suggesting that the oxytocin receptor in the central nervous system has a wide variety of effects (Jurek and Neumann, 2018).

This neurotransmitter is involved in the mother-young bonding notably via the mediation of mother preference as shown in infant lambs treated with synthetic antagonist OT receptors which led to a decrease of the exploration of the mother’s body and impaired the expression of the mother preference (Nowak et al., 2021). Furthermore, these authors also showed that close social contact of the young with its mother during suckling periods (probably through somatosensory stimulations from the orogastric sphere) triggered the release of OT in the lamb’s plasma and cerebrospinal fluid, as also previously described in calves’ plasma (Lupoli et al., 2001).

PRL is a polypeptide neurohormone that plays multiple homeostatic roles in the organism in conjunction with the dopaminergic and oxytocinergic system, since PRL secretion is controlled by a complex network of positive (oxytocin) and negative (dopamine) feedback loops (Freeman et al., 2000; Kennett and McKee, 2012). PRL receptors on the MPOA participate in the initiation of maternal recognition (Salais-López et al., 2021), the development of neural systems that underline the control of maternal behavior, as well as immune and reproductive development of the offspring, as studied in rat pups deprived from maternally-derived PRL intake through the milk (Melo et al., 2009). This hormone and its role on the fetal brain and activation of neural circuits that trigger maternal behaviors when adults has been studied in mice pups, where the lack of receptors to produce PRL results in normal pups grow but nursing deficiencies when reaching adulthood (Sairenji et al., 2017). In addition, the expression of PRL receptors at all levels of the olfactory system of rat’s neonates indicates that PRL participates in the differentiation and development of the olfactory system. Thus, in the neonatal period, PRL may modulate olfactory function that plays a key role in the interactions between the newborn pup and its mother (Freemark et al., 1996).

Another example is BDNF, a transmitter that modulates the plasticity of the visual cortex in rodents during early postnatal development, together with GABAergic neurons. This is relevant because studies have shown that a higher concentration of these markers promotes an active interaction with their environment, including the mother, enhancing the level of licking in these pups and, consequently, a precocious maturity of the visual system (Cancedda et al., 2004).

In intensive production systems, neonates and dams are frequently separated shortly after birth, truncating the mother-young bonding process, and its associated neurobiological developments that can reduce the welfare of both mother and newborn, including until later at the adult age. Hence, an especially important field for the future study includes the development of new procedures that do not impact the performance of production units but benefit animal welfare. In that sense, it is important to understand the processes in different species to propose new production models that enhance the current practices. New research perspectives are opening, focusing on analyzing the neurobiological processes inherent to the mother-young recognition, where pheromonal communication also plays an important role. However, although this kind of mediation has been studied in female rodents (Larsen et al., 2008), the role of maternal pheromones on the neonatal brain is still a research field that could be investigated thoroughly.

The implication of mother-young mutual recognition and parenting behavior on the maternal behavior of the newborn in their adulthood is also of interest, where studies in rodents have shown that oxytocin release and an adequate mother-young dynamic promotes enhanced maternal care for future generations (Nagasawa et al., 2012). Likewise, social behavior is an important aspect in breeding of farm animals, notably the agonistic interactions. In that sense, Toinon et al. (2022) showed that lambs reared with or separated from their mother displayed different social behaviors after weaning and mixing, with dam-reared kids initiating more but receiving less agonistic interactions the dam-separated kids.

Future research could also aim to qualify the particular effect of mother-young attachment on the young’s brain and whether the term imprinting could or could not apply to mammals as a notion of “brain imprinting” or “neurobiological imprinting” to describe the impact of the maternal bond on brain circuits and functioning on the later offspring phenotype, as it is already done in genetics with the term “genomic imprinting” found in mammals to describe the influence of a particular parental allele on offspring’s gene expression and phenotype (Tucci et al., 2019).

Imprinting is a process that is not exclusively created between the mother and the neonate but can be observed in newborns and humans. For example, imprint-trained foals to a human tactile stimulus (e.g., gentle rubbing) at birth decreased the defensive behaviors of the same animals at 3 months of age, facilitating their handling (Spier et al., 2004). A similar case was observed in lambs of 1- to 9-days old who were fed and handled by humans reduced avoidance behavior (Markowitz et al., 1998). However, some other reports on foals mention that early exposure to humans does not have significant differences in foal behavior at haltering and handling after 6 months (Williams et al., 2003), and even the cases where human aid on the first suckling causes an evasion response at 1 month (Henry et al., 2006).

In contrast to the importance of imprinting in domestic animals, in the area of wildlife rehabilitation, a fundamental requirement for the successful release of animals into their natural habitat consists, precisely, of preventing imprinting (Perry and Averka, 2020). Lynn et al. (2010) reported in a hand-reared sea lion that filial imprinting can cause disrupted social behaviors, where the sea lion needed to be returned to captivity since the animal responded to human voice and seek human presence following release. To prevent this, wildlife rehabilitation and reintroduction programs use techniques that prevent contact between animals and humans to impede the development of attachment (Royal Society for the Prevention of Cruelty to Animals, 2010). For example, “costume-rearing” is used with young animals in whooping cranes in reintroduction programs (Olive and Jansen, 2017). Imprinting processes and the responses they generate depend not only on species but also on the purpose for which animals are raised.

Mother-young bonding is an essential process for establishing the relationship between offspring and the dam. Auditory, olfactory, tactile, and visual stimuli participate in the onset of bonds through cerebral structures like the LC, with a key role of NE concentrations. During the sensitive (critical) period, the newborns’ brain is highly receptive to their mothers’ stimuli, a feature that is an essential component for affective bonding and the learning of information necessary for survival. To trigger this mechanism, structures such as the olfactory bulb, auditory cortex, visual cortex, locus coeruleus, and some areas of the limbic system are activated. They communicate through neurotransmitters that promote early learning in the newborn and maternal behaviors in the dam. Neonatal recognition of the mother thus depends on a whole series of neurobiological processes that begin with the uptake of multimodal sensory stimuli, which promote the formation and development of communication channels initiated by neurotransmitters. Oxytocin has been described as the principal neurochemical substance associated with affiliative and learning behaviors through conditioned affective associations that become integrated into motor responses.

Finally, it is important to emphasize that although the bonding mechanisms promoted by the aforementioned stimuli are typical of both precocial and altricial animals, differences among them may make one mechanism more important than others during the first days of life; for example, olfactory interaction in rodents. Learning more about these characteristics will help ensure that initial contact and response of non-human animals contribute to neonatal survival by promoting or preventing bonding, depending on the species.

DM-R, CB-F, MM-R, AD-O, PM-M, KL-G, and AO contributed to the conceptualization and writing and reading of the manuscript. All authors contributed to the article and approved the submitted version.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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