The Awakening of the Newborn Human Infant and the Emergence of Consciousness

ABSTRACT

Consciousness develops gradually in the womb and after birth, rather than being an all or none phenomenon. A newborn infant is aroused and wakes up at birth, due to the enormous sensory stimulation and stress that it undergoes during the transition from an aquatic environment to air. Its first breaths activate the locus coeruleus, as indicated by the large pupils of the newborn. The infant seems to be aware of its body and can recognise its mother's facial expressions, voice and smell. A default mode network matures soon after birth which appears to keep the brain in a conscious state. Thus the newborn infant is probably conscious, albeit at a low level. The foetus also shows some signs of being conscious after about 24 weeks of gestation, although it is mainly asleep in the womb and less aware of its environment. Before that stage, the nerves from the primary somatosensory, visual and auditory areas are not yet connected with the site of consciousness in the cerebral cortex.

Summary.

• Newborn infants wake up at birth and they seem to be aware of their body and their mother's facial expressions, voice and smell.

• Consciousness develops gradually and this process starts in the womb at about 24 weeks of gestation.

• Infants seem to be conscious about what they are seeing at 5 months and another important milestone is at 9 months, when they become more sociable.

1. Introduction

Birth is one of the most dramatic events in life [1]. The transition from an aquatic environment to breathing air occurs over a few hours, compared to the 100 million years it took evolution to progress from fish to amphibians [2]. Newborn infants also make the transition from lower to higher oxygen levels, a process that has occurred in the atmosphere since the earth was formed. It is a remarkable process that enables the sleeping foetus to wake up and take its first breaths of air. The big question is whether consciousness emerges before or after birth, that is, at what point an individual becomes aware of itself and the environment (see Box 1). This has now become a topic of interest from a philosophical perspective [11, 12]. The aim of this review is to present the emergence of consciousness during the perinatal period from a more neurobiological view, by building on work published earlier this century [3, 13].

BOX 1. Definition and models of consciousness.

Consciousness is mainly defined as a person's awareness of their identity and surroundings, from basic sensory awareness in newborn infants to language and abstract thinking in older humans [3, 4]. This content is distinguished from states of consciousness, such as wakefulness, sleep, comas and general anaesthesia.

It is generally believed that the content of human consciousness is processed in the cerebral cortex and the thalamus, as other areas of the central nervous system can sustain lesions without loss of consciousness [5].

There is controversy about whether it is possible to be conscious during rapid eye movement sleep, but insight and self‐reflexion are absent and time does not exist whilst dreaming. Furthermore, purposeful movements are not usually performed, as reported in foetal sheep [6].

Various theories of consciousness may apply to human foetuses and infants [7], including the controversial panpsychism theory. This states that all animals, including human foetuses, have consciousness and all constituents of reality have some phenomenal properties [8].

A more plausible model is the global neuronal workspace in the forebrain [9], where perceptions, memories, emotions and feelings become subjectively integrated. Based on a metaphor by Baars [10], it suggests that some kind of synthesis between the past, present and future can take place in this space [3, 4].

The global neuronal workspace comprises long neurons that interconnect various associative brain areas, like the prefrontal, dorsal parietal and anterior cortex and the anterior cingulate cortex. This means that impressions from the sense organs, such as familiar faces, voices, tastes and smells, can create conscious experiences from old and new memories.

2. Brain Development Before Birth

The construction of the brain, and its neural correlate of consciousness [14], starts 14 days after conception, with the formation of the neural plate on the dorsal side of the embryo. Many believe that this is the moment when the mind is attached to the foetus. This period was established as the moral limit for research on embryos by the philosopher Lady Mary Warnock [15] and legally enforced by the UK Government's Human Fertilisation and Embryology Act 1990. The need for this limit was prompted by the expansion of in vitro fertilisation and the accumulation of unused embryos. However, it has been questioned in other countries.

The neural plate is transformed into a neural tube during the embryonic period, which covers conception to 8 weeks of gestation. It bends, folds and balloons to form a hemispheric forebrain, with ventricles, a midbrain and a hindbrain [16]. During the early foetal period, 10–20 weeks after the last menstrual period, neurons are generated from the embryonic stem cells in the bottom layer of the ventricles. They migrate centripetally and form the cortex and a subplate below [17]. The first synapses are generated, which play a crucial role in the connectivity of the neurons. During the mid‐foetal period, from 17 to 25 weeks of gestation, the neurons are laminated and endogenous electric action potentials are spontaneously generated [18].

Nerves from the sensory organs, with the exception of olfaction, are connected to the cortical plate via the thalamus from around 24 weeks of gestation [19]. The emergence of these thalamocortical connections (Figure 1) means that the nerves from the sensory organs can provide input to the cortex. The foetus moves in response to sensory, noxious and auditory stimulation before this point, but those reflexes cannot be processed in the neural correlate of consciousness for anatomical reasons. Furthermore, the ascending systems from the subcortical hubs that are involved in states of consciousness, such as wakefulness, emotions and reward, have not yet reached the cortex [20].

FIGURE 1.

The development of the foetal brain from 10 weeks of gestation to 2 years of age. The nerves from the sensory organs do not reach the cortex, via the thalamus, until 25 weeks and the foetus cannot be conscious. After that, the first thalamo‐cortical connections are established and the fetus may be aware of its mother speaking and singing. The newborn infant can recognise human faces and the formation of a default mode network begins. At 2 years of age, the child can recognise itself in a mirror and its global neuronal workspace is mature.

3. Foetal Behaviour

The sulci and gyri develop rapidly after 24–26 weeks of gestation. Long associative pathways are formed, dendrites differentiate and synaptogenesis increases. That is why the foetus can develop behavioural signs of having a neural correlate of consciousness. The foetus frequently uses one hand to touch its head, face, mouth and other hand [21]. Furthermore the foetus can habituate to repeated vibroacoustic sound stimulation [21], because it has developed its short memory, which is part of the criteria of consciousness. One study used a so‐called auditory oddball paradigm, which consisted of exposing foetuses of about 35 weeks of gestation to a sequence of identical tones, via their mother's abdomen, before ending with a different tone. Magnetoencephalography showed that the event‐related responses were different from the last tone, which indicated that they remembered the identical tones that preceded this [22, 23]. Other research has demonstrated that foetuses appeared to learn their mothers' speech in the womb [24]. For example, Swedish newborn infants recognised the typical Swedish ‘u’ vowel, which is pronounced ‘yyy’, but American infants recognised the typical English ‘eee’ vowel better. Being able to perceive, and respond to, what they can hear and to react to speech does not prove that they are awake and conscious, because learning can take place during sleep [25]. In fact, the foetus exists in a continuous sleep‐like state, even if it opens its eyes. Although it can demonstrate reflexes in response to noxious stimuli, these stimuli cause a defence state with inhibition rather than cortical arousal to an awake state. Furthermore, the foetus is living at a low oxygen level and is suppressed by sleep‐inducing and analgesic agents, such as adenosine [26]. This means that the foetus can only be regarded as conscious at a rudimentary level, without awareness of pain [6, 27]. It has been suggested that foetuses have islands of consciousness, like severely brain‐damaged adults [28].

4. Metamorphosis at Birth

Birth is a major ordeal for the foetus, due to the dramatic transition from the aquatic environment in the womb to air. The first breaths of the air have historically been regarded as an important landmark when life begins and the soul is established. These are reflected by the Greek word pneuma and the Latin word spiritus, which both stand for air and soul.

The first breaths of air normally occur in < 30 s after birth and seem to be triggered by the intense sensory stimulation of delivery, particularly cooling when the amniotic fluid evaporates. Breathing is initiated by the pre‐Bötzinger complex [29]. This excites the arousal centre in the brain, known as the locus coeruleus (Figure 2). It excites the entire brain and the nerve terminals release noradrenaline, which is distributed to the entire brain. You can tell that the locus coeruleus has been activated because the newborn infant opens its eyes and has large pupils [26]. Acetylcholine may be the main neurotransmitter of consciousness [14], because cholinergic afferents from the sensory periphery [20] are involved in the awakening process. The evidence for this includes one animal study, which found that arousal was reduced in transgenic mice pups who lacked nicotinic acetylcholine receptors [30].

FIGURE 2.

A number of factors increase the level of consciousness after delivery. The transition from the aquatic environment to air triggers the first breaths. The arousal and awakening of the newborn baby are mediated by the dramatic increase in sensory stimulation and the stress of being born. Large pupils indicate that the noradrenergic nucleus locus coeruleus has been activated. Excitatory neurotransmitters dominate, whilst inhibiting factors decrease.

Arousal is probably also excited by the stress of being born [1]. The squeezing and squashing of the foetus, particularly during a vaginal delivery, triggers a surge of stress hormones, particularly catecholamines. The rapid activation of retinal photoreceptors at birth initiates a sudden brain shift, which affects neurotransmitter releases and circadian rhythm [31]. Genetic and epigenetic mechanisms are probably involved [32]. This is supported by a study of newborn rats, which found birth‐related expressions of immediate early genes and neuromodulator messenger ribonucleic acid in their respiratory centres [33]. These studies demonstrate considerable activation of the neural correlate of consciousness at birth. Infants delivered by elective Caesarean sections experience less distress, as indicated by their lower catecholamine surge at birth [34]. However, their breathing and awareness are slightly delayed [35]. Furthermore, this may also increase the risk of developing behavioural problems, such as autism spectrum disorders [36, 37].

5. The Newborn Infant

After birth, synaptogenesis increases substantially in the brain, which leads to further maturation of the neural correlate of consciousness. The limbic system is rapidly changing at this point, which is important for emotional and social interactions. A default mode network emerges soon after birth, which has been detected by functional magnetic resonance imaging [38, 39]. This appears to keep the brain in a conscious state, by promoting self‐reference, social cognition and episodic and language memory.

From the first day, newborn infants can imitate gestures and facial expressions [40] and they are aware of their bodies and recognise that other people are like them. They can also recognise their mother's smell and voice and detect facial expressions of happiness or disgust.

6. The Preterm Infant

The consciousness of preterm infants can be compared to that of foetuses at corresponding gestational ages. However, the transition to a different environment and breathing oxygen at birth changes both the state and content of their consciousness. The preterm infant is awake for short periods from about 24 weeks of gestation. It can open its eyes and focus more on human faces than the hospital monitors it is surrounded by. It shows aversion, by moving when it is disturbed by caregivers. Preterm infants were previously regarded as organisms, rather than conscious patients, and subjected to several painful procedures without analgesia. However, studies that used near‐infrared spectroscopy have reported that moderately preterm infants showed extensive cortical responses to pain. This indicated that they may have been conscious of the sensation [41, 42].

During the 1980s the German‐American psychologist Heidelise Als introduced the Neonatal Individualised Developmental Care and Assessment Program. It was initially regarded as controversial, but it caused a paradigm shift and stimulated neonatal care that recognised consciousness. This was shown to be effective in randomised studies [43]. Another example of progress in neonatology has been Kangaroo care, or skin‐to‐skin care, which was developed by R. Martinez and N. Charpak in Bogota, Colombia [44]. Although it was originally introduced due to a lack of incubators, this close contact probably makes infants more conscious of their parents.

7. Consciousness After the Newborn Period

Postnatal development of consciousness occurs in revolutionary steps [45].

Feeding and sleeping dominate the infant's first postnatal weeks. But, around 2 months of age, they start to spend longer time awake and alert. As Rochat says, they ‘manifest themselves as explicit explorers and active scrutinisers of the world’ [45]. The most striking event is that the infant starts to smile from about 6 weeks of age, responding to their parents and other adults. Protoconversation also starts about this age and they can respond negatively to adults when they see a sudden still face. The parents start to feel that their child has become a person. It has been claimed that human babies should be born after a longer pregnancy, so they are more mature at birth, like lambs and calves. These are just two animals who are more conscious than humans at birth and seek their mother's breast almost immediately after birth. However, it would be too difficult for a bipedal animal like a human to deliver an infant with a larger head.

At about 5 months an infant becomes more conscious of what it is seeing and hearing, as demonstrated by a study that used a psychophysical technique [46]. It monitored event‐related potentials with electro‐encephalography and found that infants seemed to be conscious when they saw attractive faces, but not when they were masked (Box 1). This response was weak and delayed in 5‐month‐old infants, but more similar to adult responses when they were 12–15 months of age. Infants develop a more social brain by 9 months of age [45], by pointing at objects or animals and including others whilst they roam and explore their environment. They can also respond to what others are looking at. Infants also become wary of strangers, if they are carried around by unfamiliar adults, and start to explore the environment by crawling around on all fours.

Another hallmark of consciousness is when an infant recognises itself in a mirror at about 2 years of age [47]. Their first words, such as hi and bye‐bye, occur during social interactions after 1 year of age. Combining two words can demonstrate improved conscious awareness and this normally happens after about 2 years of age. The default mode network matures successively and becomes adult‐like by 2 years of age. It takes 4 years for the theory of the mind to develop, which is when the child understands what other people are thinking [48].

8. Conclusion

The emerge of consciousness is a gradual process, rather than an all or nothing phenomenon. Its neural correlate emerges around 24 weeks of gestation in the human foetus, when the nerves from the sensory organs are connected to the cortex via the thalamus. Although the infant shows behavioural signs of consciousness, it is mainly asleep. There is an exciting shift at birth, when the foetus is aroused, wakes up and takes its first breaths of air. Even preterm infants exhibit more signs of being conscious than foetuses of a corresponding gestational age. The finding that the neural correlate of consciousness does not emerge until around 24 weeks of gestation in foetuses and preterm infants has been used to support legal abortions up to that age [27]. Intensive care for more or less brain‐damaged extremely preterm infants [49] may also be withheld or withdrawn [50].

Author Contributions

Hugo Lagercrantz: conceptualization, writing – original draft.

Conflicts of Interest

The author declares no conflicts of interest.