NDC neurobiological model: why parent-infant biobehavioural synchrony in the first 100 days matters for optimal developmental outcomes

Biology-culture mismatch in very early life generates environmental factors which increase developmental risk in susceptible infants

A susceptible infant experiences biology-culture mismatch as adversity. Although the human infant is highly adaptive across a wide variety of culturally-determined infantcare practices, a significant gap between cultural practices and evolutionary expectation may result in chronic SNS-HPA hyperarousal in very early life, in addition to other risks.26, 80-87

The NDC model proposes that initial motor and sensory-motor neural lesions or deficits are more likely in susceptible children when environmental factors are mismatched with biological expectations during the critically neuroplastic, injury-sensitive first 100 days post-birth, resulting in chronic SNS-HPA hyperarousal which either triggers or perpetuates multi-directional cascades of atypical development.

The infant has hardwired biological expectations which evolved in our environment of evolutionary adaptedness

In very early life, the infant evolved, in the Homo sapien’s environment of evolutionary adaptedness, to expect

1. Rich environmental stimulation, including

   • Prolonged physical contact with older children and adults, including co-sleeping and diverse and frequent social sensory-motor enrichment

   • High levels of postural variability

   • Multi-centric social interactions

   • Complex non-social environmental stimulation e.g. outdoors.

2. Affect-driven (that is, emotion-driven), increasingly long, sensory-motor reciprocity chains with caring older children and adults. Mutual positive affect between adults and infants, or enjoyment and delight, has ensured Homo sapiens’ evolutionary survival.

3. Human milk transferred directly from the lactating breast to the infant gut, optimizing the gut microbiome, and metabolic, endocrine, and immune protection. Frequent and flexible breastfeeding facilitates increasingly long and complex motor and sensory-motor reciprocity chains.

Infants are exposed to complex 21st century environments which don't easily match evolutionary expectations

Currently, in very early life, parents receive a great deal of conflicting advice from health professionals concerning breastfeeding, infant sensory needs, unsettled infant behavior and parent-infant sleep, and consult with multiple providers.88, 89 There are serious gaps in health professional training across disciplines in management of breastfeeding and infant behavior problems;90-93 widespread inappropriate medicalisation of infant behavior, risking worsened outcomes; and substantial evidence that popularly applied approaches to breastfeeding and infant regulatory problems do not help parents and babies, or make breastfeeding, crying and sleep problems worse.94-103

That is, the gap between biological expectation and socioculturally-determined advice concerning infantcare is profound in contemporary societies, placing susceptible infants at neurodevelopmental risk, and increasing the risk of maternal postnatal anxiety and depression.104-106 Infant cry-fuss, feeding, and sleep problems are often highly stressful for parents, and predispose to maternal postnatal depression.48, 106, 107

NDC hypothesizes that three key environmental factors emerge from biology-culture mismatch, and interact in the complex adaptive system of the parent and infant, increasing the risk of neurodelopmental challenges and neurodivergence in susceptible infants: suboptimal environmental stimulation, disruption of parent-infant biobehavioral synchrony, and gut dysbiosis or feeding problems.

Suboptimal environmental stimulation

In Australia and in many countries today, parents continue to be advised that sleep training or FWB approaches are necessary for optimal developmental outcomes and good sleep habits. (Table 4) Infant sleep training emerged in the 1950s and 1960s when the first wave of the school of behaviorism (FWB) in psychology was applied to infantcare. Yet high level evidence demonstrates no decreased night waking or reliably improved maternal mood scores as a result of FWB interventions, and no improvement in developmental outcomes.98, 103, 108-113

NDC proposes that application of FWB approaches to infant sleep in very early life impacts negatively on neurodevelopmental outcomes in ASD-susceptible infants, because FWB approaches decrease environmental stimulation in four ways

1. Parents are advised to teach the infant ‘good sleep habits’ by having the infant sleep in a cot or on an immobile surface, often in a quiet dim room with deliberately minimised visual stimulation, iteratively throughout the day. This regular recourse to a low sensory interior environment impoverishes sensory-motor experience, both social and non-social, and fails to offer susceptible infants adequate task demands for optimal development of skills in interpretation of sensory information, adaptation of movements in response to external stimuli, and organisation of postural control.

2. Stimulation is problematized. Parents are advised to avoid social and non-social ‘overstimulation’.

3. Inadequate sensory-motor stimulation results in SNS-HPA arousal (crying and fussing), which parents are advised to interpret as ‘tired signs’ or ‘overstimulation’, triggering more attempts to put the baby to sleep.

4. Patterns of inadequate environmental enrichment may result in chronic infant SNS-HPA hyperarousal.31, 114, 115 (Box 6)

Disruption of parent-infant biobehavioral synchrony

Our environment of evolutionary adaptedness offered infants rich opportunities for increasingly long and complex motor and sensory-motor reciprocity chains across the two dominant sites of parent-infant transaction in very early life, feeds and sleep. Cued care has been demonstrated in cross-cultural studies to downregulate both infant and parent’s SNS-HPA axis.116-118 Parent-infant biobehavioral synchrony is disrupted by problems of crying and fussing, breastfeeding, and sleep.

Inappropriate medicalisation of infant cry-fuss behaviors

The neurobiological model of cry-fuss problems proposes that chronic SNS-HPA hyperarousal, manifesting as crying and fussing in otherwise well infants, emerges out of a mismatch between environment of evolutionary adaptedness and various socioculturally-determined environmental factors in contemporary life. But overdiagnosis and overtreatment, including in children, is a growing global concern, and occurs commonly in very early life, with deleterious effects.119, 120 Parents are often taught that their infant’s cry results from physical pain e.g. from reflux, aerophagia-induced reflux, food allergies or intolerances, lactose intolerance, or from oral connective tissue restrictions.97, 99, 101, 102, 121 The resultant inappropriate medicalisation risks unintended outcomes and perpetuates disruption to parent-infant biobehavioral synchrony. (Table 3)

First wave behavioral interventions for parent-infant sleep

In response to emerging neuroscience and psychological attachment research, FWB approaches have adopted a discourse which emphasises the importance of cued care for secure attachment and optimal mental health outcomes. Yet paradoxically, FWB sleep advice continues to actively disrupts cued care and biobehavioral synchrony, by advising parents to behave in directive and non-contingent ways, iteratively, day and night. (Box 6) More extreme FWB strategies, such as minimising eye contact and interaction at sleep-time throughout the days and nights, iteratively present a ‘still face’ to the infant, which is known to result in greater efforts by the infant to engage at first, before he or she withdraws from cueing.122 Standard FWB approaches advise parents to not respond to SNS-HPA arousal, or to delay responses, or to respond but not as they believe the baby intends. Parents are advised to iteratively override the powerful biological cues of sleepiness after feeds by applying behaviors such as burping, holding upright, or wrapping, at the same time as they are instructed to achieve prescribed nap frequencies and durations.

FWB approaches may exacerbate parental anxiety, which predisposes to poor sleep efficiency and postnatal depression.123, 124 The parent trying to enforce sleep because she believes it necessary for her baby’s healthy development is likely to feel anxious and distressed when the baby ‘resists sleep’ multiple times a day; the infant ‘resisting sleep’ (that is, whose sleep pressure is not yet high enough for easy sleep) is repeatedly subject to the biological stress of a low sensory environment, resulting in chronic SNS-HPA hyperarousal and increased allostatic load. This cycle may place behaviorally hypo-aroused infants at particular risk.

The link between sleep problems in very early life and behavioral and sleep problems in later childhood may be, paradoxically, mediated by the widespread sociocultural and clinical application of sleep training or FWB strategies, resulting in cascades of both parent and infant chronic SNS-HPA hyperarousal.115, 125, 126 FWB approaches also disrupt the dyadic synchrony of the circadian clock, by promoting long blocks of sleep during the day.127

Unidentified and unmanaged breastfeeding and unsettled infant behavior problems increase risk of maternal postnatal depression

Cry-fuss problems, poor maternal sleep efficiency, and breastfeeding problems are key modifiable risk factors for post-natal depression.48, 104-106, 128 Each of these may arise from, or be exacerbated by, a mismatch between popular sociocultural and clinical approaches, and infant biology. Health professionals report inadequate training in management of breastfeeding and unsettled infant behaviour problems, and often recommend approaches which have been shown not to help, or may even worsen these problems, with associated deleterious effects on parent-infant biobehavioral synchrony.90, 93, 94, 98, 103, 108-113, 123, 124

There is widespread recognition of the importance of prevention of, or early detection and treatment of, perinatal anxiety and depression, the most common mental health condition post-birth. Winnicott proposed that a state of maternal preoccupation or heightened sensitivity develops toward the end of pregnancy and lasts throughout the postpartum period. From an evolutionary perspective, this heightened state supports a woman’s ability to anticipate her infant’s needs and to respond to her infant’s unique cues, and may include anxious, hypervigilant and intrusive thoughts about the infant. In contemporary contexts, often characterised by minimal social support, the same heightened state increases her risk of postnatal anxiety and depression if infant behaviour problems emerge.