Preparing for Life After Birth: Introducing the Concepts of Intrauterine and Extrauterine Sensory Entrainment in Mammalian Young

Abstract

Simple Summary A key event in the life of a mammalian fetus is its birth, especially in view of the exceptional change in its environment that occurs at birth. An area of great interest is the extent to which factors within the uterus prepare the fetus for birth and postnatal life. These and other factors are evaluated here for mammalian young that exhibit mature, moderately immature, and exceptionally immature neurological development at birth. A striking finding is the basic uniformity of various preparatory processes despite the diversity of birth-related circumstances among different terrestrial mammals. Numerous scientific disciplines have contributed to understanding in this area. Accordingly, the major purpose of this review is to construct from these diverse sources an integrated account of important facets of our current understanding. The primary focus is on how a progressive improvement in the functional effectiveness of the sensory systems for touch, temperature, taste, smell, balance/movement, hearing, and sight equips young mammals to cope successfully with the considerable challenge of being expelled from the uterus into the outside world. It is shown that the sensory environment in the uterus interacts with the genetically preprogrammed development of the apparatus for each sensory modality. It is also shown that the way this occurs can embed stimulus-response capabilities that can be accessed and beneficially utilised after birth. This phenomenon is called “trans-natal sensory continuity”. This embedding of sensory capabilities has previously been described as “learning” and the subsequent accessing of these embedded capabilities as “memory”. However, it is noted that such “learning” and “memory” processes are sometimes mistakenly thought to require the fetus to be conscious, a view which does not accord with established understanding of learning processes, nor with compelling contrary evidence from direct studies of fetal brain states. The solution proposed is to describe trans-natal sensory continuity in terms of the neurophysiological mechanisms involved and not as learning and memory outcomes. Introduced here, therefore, is the concept of “intrauterine sensory entrainment”. Its specific mechanistic basis is the well-established way nervous systems respond to sensory stimuli by reorganising their neural structures, functions, and connections. Known as neuroplasticity, this is recognised as integral to both prenatal and postnatal brain development and as the basis of postnatal learning and memory. Thus, intrauterine sensory entrainment is the mechanism by which trans-natal sensory continuity is achieved. It begins with the prenatal embedding of responsiveness to particular sensory inputs which are generated by the stimulation of specific receptors once the neurological apparatus for that sensory modality has begun to develop. Thereafter, this process continues until birth, and this makes all such entrained sensory capabilities available to operate after birth. Nevertheless, all sensory systems that exhibit some level of functionality at birth continue to mature postnatally, and in some species various sensory systems do not become functional until after birth. Accordingly, also introduced here is the concept of “extrauterine sensory entrainment”, which is the postnatal continuation of “intrauterine sensory entrainment”. Such extrauterine entrainment therefore contributes to the continuing maturation of the sensory systems that are operational at birth, the later development and maturation of those systems that are absent at birth, and the combined impact of these factors on the behaviour of newborn and young mammals. Abstract Presented is an updated understanding of the development of sensory systems in the offspring of a wide range of terrestrial mammals, the prenatal exposure of those systems to salient stimuli, and the mechanisms by which that exposure can embed particular sensory capabilities that prepare newborns to respond appropriately to similar stimuli they may encounter after birth. Taken together, these are the constituents of the phenomenon of “trans-natal sensory continuity” where the embedded sensory capabilities are considered to have been “learnt” and, when accessed subsequently, they are said to have been “remembered”. An alternative explanation of trans-natal sensory continuity is provided here in order to focus on the mechanisms of “embedding” and “accessing” instead of the potentially more subjectively conceived outcomes of “learning” and “memory”. Thus, the mechanistic concept of “intrauterine sensory entrainment” has been introduced, its foundation being the well-established neuroplastic capability of nervous systems to respond to sensory inputs by reorganising their neural structures, functions, and connections. Five conditions need to be met before “trans-natal sensory continuity” can occur. They are (1) sufficient neurological maturity to support minimal functional activity in specific sensory receptor systems in utero; (2) the presence of sensory stimuli that activate their aligned receptors before birth; (3) the neurological capability for entrained functions within specific sensory modalities to be retained beyond birth; (4) specific sensory stimuli that are effective both before and after birth; and (5) a capability to detect those stimuli when or if they are presented after birth in ways that differ (e.g., in air) from their presentation via fluid media before birth. Numerous beneficial outcomes of this process have been reported for mammalian newborns, but the range of benefits depends on how many of the full set of sensory modalities are functional at the time of birth. Thus, the breadth of sensory capabilities may be extensive, somewhat restricted, or minimal in offspring that are, respectively, neurologically mature, moderately immature, or exceptionally immature at birth. It is noted that birth marks a transition from intrauterine sensory entrainment to extrauterine sensory entrainment in all mammalian young. Depending on their neurological maturity, extrauterine entrainment contributes to the continuing maturation of the different sensory systems that are operational at birth, the later development and maturation of the systems that are absent at birth, and the combined impact of those factors on the behaviour of newborn and young mammals. Intrauterine sensory entrainment helps to prepare mammalian young for life immediately after birth, and extrauterine sensory entrainment continues this process until all sensory modalities develop full functionality. It is apparent that, overall, extrauterine sensory entrainment and its aligned neuroplastic responses underlie numerous postnatal learning and memory events which contribute to the maturation of all sensory capabilities that eventually enable mammalian young to live autonomously.