How amniotic fluid shapes early odor-guided responses to colostrum and milk (and more)

RevueAmong the multiple transitions that characterize mammalian development, birth certainly is the most abrupt and spectacular. It is also the most challenging for newborns when one considers their high mortality rates in any mammalian species. Although evolution has selected newborn organisms that possess the physiological and behavioral keys leading to adapt to this harsh psychobiological challenge, their capabilities cannot be considered separately from the maternal organism and the environment she creates. Mammalian females provide indeed passive (physiological) and/or active (behavioral) assistance to complement and boost their offspring’s capacities. One notable strategy of mammalian females is to generate “sensory continuities” between the consecutive environmental niches their offspring have to go through to survive. Such sensory continuities are produced by different mechanisms based on the basic biological principle that earlier steps in development prepare the organization of the next steps. In vertebrates and invertebrates, the “prenatal” development of sensorimotor and neurocognitive abilities conditions such abilities in postnatal development. These organizational and inductive functions of prenatal experience have been best evidenced in the attunement of sensory systems of newborn organisms. Some stimuli from the complex information flow of the postnatal environment are more salient than others (Alberts, 1987; Smotherman and Robinson, 1987, 1995). This initial neonatal selectivity, often termed “innate” in the soft (etymological) way, is actualized by distress cessation, attention, positive orientation, and coordinated approach responses, as well as facilitated consumption, and eventually metabolic optimization, adapted growth, and cognitive integration. Such transnatal stimulus continuities probably occur in all sensory modalities, as a consequence of their structural and functional construction within the specificities of the fetal ecology proper to each species, and, within species, to local or individual conditions conveyed by and through the maternal organism. First, specialized sensory abilities in neonates may result from perceptual canalization in the species-specific fetal environment, definable as the set of stimuli to which any fetus of a given species is inevitably exposed. These may include tactile cues of body containment, kinesthetic cues caused by regularities in maternal movements, physiological noises related to vascular or heart beats (Salk, 1962; De Casper and Sigafoos, 1983), and possibly odor- or taste-active compounds derived from normal metabolism. Second, local or individual-specific properties of the fetal environment may render neonates selectively reactive to soft tactile stimulations (Scafidi et al., 1990), odorants or tastants transferred into the amniotic fluid from the maternal environment (among which diet, eg, Mennella et al., 2001; Schaal et al., 1995a, 2000), and idiosyncrasies of maternal language, voice, or environmental sounds (De Casper and Fifer, 1980; De Casper and Spence, 1986; Hepper, 1988a; Fifer and Moon, 1995). A third way through which prenatal experience might impinge on neonatal expectations is through nonspecific mechanisms related to the perception of environmental intensity or variability without reference to given qualities. Thus, for example, fetal encoding of generally low-intensity or of different degrees of qualitative variability of the uterine environment, may fix later preferences for low-intensity, or more easily tolerate or appreciate constantly changing stimuli. This chapter will focus on the role of olfaction in the perinatal adaptive responsiveness of mammalian neonates. Specifically, I will address mechanisms by which olfactory experience in the amniotic environment prepare neonates’ selective responsiveness in the postnatal odor environment, especially in the context of the vial ingestion of colostrum and milk, and its consequences for food acceptance in the long run of later life. Although mainly based on studies conducted in human perinates, comparative results obtained with rat, mouse, rabbit, and porcine, ovine or caprine perinates will be mentioned at places, to assess the generality of the phenomena involved in the rapid expression of adaptive responses at birth and after

Mammary odor cues and pheromones: mammalian infant-directed communication about maternal state, mammae, and milk.

International audienceNeonatal mammals are exposed to an outstandingly powerful selective pressure at birth, and any mean to alleviate their localization effort and accelerate acceptance to orally grasp a nipple and ingest milk should have had advantageous consequences over evolutionary time. Thus, it is essential for females to display a biological interface structure that is sensorily conspicuous and executively easy for their newborns. Females' strategy to increase the conspicuousness of nipples could only exploit the newborns' most advanced and conserved sensory systems, touch and olfaction, and selection has accordingly shaped tactilely and olfactorily conspicuous mammary structures. This evolutionary modification has worked either by affecting structural features of mammaries or indirectly by affecting maternal behavioral propensities to create olfactory traces on them. These predictions are considered here in mammalian cases that have received empirical attention among marsupials, rodents, lagomorphs, ungulates, carnivores, and primates. It appears that broadcasting chemical cues and/or signals from the mammae is a pan-mammalian reproductive strategy to pilot neonatal arousal, motivation and attraction to the mother, provide assistance in localizing and orally grasping the mammae, and boost up learning. But the ways by which these chemical cues are produced and assembled on the mammae are both diverse between species and complex within species, offering an outstanding opportunity for comparative analyses in chemical communication