Elsevier

Medical Hypotheses

Volume 81, Issue 5, November 2013, Pages 816-822
Medical Hypotheses

A neurobiological model for cry-fuss problems in the first three to four months of life

https://doi.org/10.1016/j.mehy.2013.09.004Get rights and content

Abstract

Although problem crying in the first three to four months of life is usually self-limiting, it is not a trivial condition. Early intervention is important, yet families receive conflicting advice from health professionals. The past decade has seen significant advances in neuroscience, lactation science, and developmental psychology, including new insights into the significance of developmentally sensitive windows. We propose a neurobiological model to explain the mechanisms of cry-fuss problems in the first months of life, and the mechanisms which underlie effective intervention, with a view to facilitating research collaboration and consistency of advice across health disciplines. We hypothesise that crying in the first three to four neurodevelopmentally sensitive months signals activation of the hypothalamic–pituitary–adrenal axis and adrenergic neuronal circuitry in response to perceptions of discomfort or threat. Susceptible infants may be conditioned by early stress, for example, by unidentified feeding difficulties, into a sensitised stress response, which usually settles at three to four months of age with neurodevelopmental maturity. Bouts of prolonged and unsoothable crying result from positive feedback loops in the hypothalamic–pituitary–adrenal and adrenergic systems. Importantly, epigenetic modulation of the infant’s limbic neuronal circuitry may explain correlations between regulatory problems in the first months of life, and behavioural problems including feeding problems in later childhood.

Section snippets

Background

One of the most common problems parents bring to paediatricians, general practitioners, child health nurses, midwives, psychologists and Emergency Departments in the first weeks and months of life is the baby who cries and fusses. One in five new parents report that their baby has problem crying [1]. Infant cry-fuss behaviour is a complex problem, emerging out of multiple dynamically interacting and co-evolving factors, including genetics, temperament, an individual baby’s unique level of

Cry-fuss problems emerge out of disrupted maternal-infant neurobehavioural synchrony

Biologically programmed, or innate, patterns of synchrony operate between the neuroendocrine systems of mother and infant, increasingly elucidated by functional MRI imaging of the brain and neurohormonal assay. These morphological and neurohormonal changes correlate with mother–infant neurobehaviours, for example, during birth, infant care, or feeds. Due to the highly social nature of our species, maternal–infant neuroendocrine and neurobehavioural synchrony may be either supported or impeded

The infant’s nervous system

Neuroscience increasingly elucidates the neurocorrelates of mother–infant interaction and the neuronal circuitries of depression, anxiety and fear [14]. We hypothesise that when an infant’s amygdala, which are mature at birth, are activated by a perceived need or threat either internally or in the environment, the hypothalamic–pituitary–adrenal (HPA) neurohormonal circuitry upregulates, triggering sympathetic nervous system (SNS) activity and adrenaline release, with associated cardiovascular,

Neurohormonal mechanisms which underlie clinical intervention

The translation of a metanarrative review of the heterogenous and interdisciplinary evidence concerning cry-fuss problems in the first months of life into a systematic, five-domain clinical intervention (“The Possums Approach”) is detailed elsewhere [31], [73], [77], [78]. This intervention aims for early identification and management of problems that disrupt maternal–infant neurobehavioural synchronies. Regardless of feeding method, our intervention systematically addresses relevant factors in

Discussion

This neurobiological explanatory model for infant cry-fuss problems in the first few months of life (“The Possums Model”) has been developed from a synthesis of the evidence across multiple disciplines. The model proposes first, that crying in the first three to four neurodevelopmentally sensitive months signals activation of the HPA axis and adrenergic neuronal circuitry in response to perceptions of discomfort or threat. Second, this neurobiological model proposes that susceptible infants are

Conclusion

Despite the self-limiting nature of the condition for most, unsettled behaviour in the first few months of life requires early, integrated intervention. Our synthesis of the heterogenous evidence across multiple disciplines elucidates the underlying neurobiological mechanisms of infant crying, and the underlying neurobiological mechanisms of a five domain interdisciplinary clinical intervention. This shared explanatory framework aims to facilitate collaboration between researchers from

Conflict of interest statement

Pamela Douglas and Peter Hill declare that they have no conflict of interest to report.

Competing interests

None declared.

Funding

No specific funding.

Author’s contributions

PSD conceived of the study. PSH participated in conceptualization and critique of concept. PSD drafted the manuscript. PSH critically reviewed and edited the manuscript. Both authors approve the final version.

Acknowledgements

We thank Professor Debra Creedy, Griffith University, and Associate Professor Yvette Miller, Queensland University of Technology, for reading this paper in an early draft and offering critique.

References (90)

  • P.S. Douglas

    Excessive crying and gastro-oesophageal reflux disease in infants: misalignment of biology and culture

    Med Hypotheses

    (2005)
  • C.U. Rask et al.

    Infant behaviours are predictive of functional somatic symptoms at ages 5–7 years: results from the Copenhagan Child Cohort CCC2000

    J Pediatr

    (2013)
  • S.J. Meldrum et al.

    Allergic disease in the first year of life is associated with differences in subsequent neurodevelopment and behaviour

    Early Hum Dev

    (2012)
  • M. Wake et al.

    Prevalence, stability, and outcomes of cry-fuss and sleep problems in the first 2 years of life: prospective community-based study

    Pediatrics

    (2007)
  • G. Schmid et al.

    Predictors of crying, feeding and sleeping problems: a prospective study

    Child Care Health Dev

    (2011)
  • P.S. Douglas et al.

    The unsettled baby: how complexity science helps

    Arch Dis Child

    (2011)
  • G. Sirvinskiene et al.

    Infant difficult behaviors in the context of perinatal biomedical conditions and early child environment

    BMC Pediatr

    (2012)
  • T. Fujiwara et al.

    Infant distress at five weeks of age and caregiver frustration

    J Pediatr

    (2011)
  • I. James-Roberts et al.

    Infant crying and sleeping in London, Copenhagen and when parents adopt a “proximal” form of care

    Pediatrics

    (2006)
  • C. Howard et al.

    Parental responses to infant crying and colic: the effect on breastfeeding duration

    Breastfeed Med

    (2006)
  • T. Vik et al.

    Infantile colic, prolonged crying and maternal postnatal depression

    Acta Paediatr

    (2009)
  • M.H. Hemmi et al.

    Associations between problems with crying, sleeping and/or feeding in infancy and long-term behavioural outcomes in childhood: a meta analysis

    Arch Dis Child

    (2011)
  • S.M. McCallum et al.

    Unsettled infant behaviour and health service use: a cross-sectional community survey in Melbourne Australia

    J Paediatr Child Health

    (2011)
  • J.E. Swain et al.

    Brain basis of early parent-infant interactions: psychology, physiology, and in vivo functional neuroimaging studies

    J Child Psychol Psychiatry

    (2007)
  • Douglas P, Hill PS. Behavioural sleep interventions in the first six months of life do not improve outcomes for mothers...
  • P. Douglas

    Diagnosing gastro-oesophageal reflux disease or lactose intolerance in babies who cry alot in the first few months overlooks feeding problems

    J Paediatr Child Health

    (2013)
  • K.G. Dewey et al.

    Risk factors for suboptimal infant breastfeeding behavior, delayed onset of lactation, and excess neonatal weight loss

    Pediatrics

    (2003)
  • A. Brown et al.

    Impact of birth complications on breastfeeding duration: an internet survey

    J Adv Nurs

    (2012)
  • V.S. Sakalidis et al.

    A comparison of early sucking dynamics during breastfeeding after cesarean section and vaginal birth

    Breastfeed Med

    (2012)
  • L. Feldman-Winter et al.

    Residency curriculum improves breastfeeding care

    Pediatrics

    (2010)
  • M. Renfrew et al.

    Preventing Disease and Saving Resources: The Potential Contribution of Increasing Breastfeeding Rates in the UK

    (2012)
  • H. Wasser et al.

    Infants perceived as “fussy” are more likely to receive complementary foods before 4 months

    Pediatrics

    (2011)
  • R. Li et al.

    Why mothers stop breastfeeding: mothers’ self-reported reasons for stopping during the first year

    Pediatrics

    (2008)
  • S. Redsell et al.

    Parents’ beliefs about appropriate infant size, growth and feeding behaviour: implications for the prevention of childhood obesity

    BMC Public Health

    (2010)
  • E. Odom et al.

    Reasons for earlier than desired cessation of breastfeeding

    Pediatics

    (2013)
  • V. Huhtala et al.

    Low plasma cholecystokinin levels in colicky infants

    J Pediatr Gastroenterol Nutr

    (2003)
  • C. Miller-Loncar et al.

    Infant colic and feeding difficulties

    Arch Dis Child

    (2004)
  • S.S. Yalcin et al.

    Relationship of lower breastfeeding score and problems in infancy

    Breastfeed Med

    (2011)
  • P. Douglas et al.

    Managing infants who cry excessively in the first few months of life

    BMJ

    (2011)
  • B. de Lauzon-Guillain et al.

    Breastfeeding and infant temperament at age three months

    PLoS One

    (2012)
  • M. Ammaniti et al.

    Maternal psychopathology and child risk factors in infantile anorexia

    Int J Eat Disord

    (2010)
  • H.W. Davies et al.

    Reconceptualizing feeding and feeding disorders in interpersonal context: the case for a relational disorder

    J Fam Psychol

    (2006)
  • S.A. Silva et al.

    Where is the wisdom? II – Evidence-based medicine and the epistemological crisis in clinical medicine. Exposition and commentary on Djulbegovic, B., Guyatt, G. H. & Ashcroft, R. E. (2009) Cancer Control, 16, 158-168

    Cancer Control

    (2009)

    J Eval Clin Pract

    (2009)
  • J.A. Mindell et al.

    Behavioral treatment of bedtime problems and night wakings in infants and young children

    Sleep

    (2006)
  • P.D. Hill et al.

    Primary and secondary mediators’ influence on milk output in lactating mothers of preterm and term infants

    J Hum Lact

    (2005)
  • Cited by (25)

    • Does childbirth experience affect infant behaviour? Exploring the perceptions of maternity care providers

      2019, Midwifery
      Citation Excerpt :

      There are several reasons why this may occur, including possible residual pain in the infant from procedures such as forceps, or medications used during labour (Taylor et al., 2000; Ransjo-Arvidson et al., 2001; Brown and Jordan, 2013). High cortisol levels circulating during labour might also overstimulate an infant's hypothalamic–pituitary–adrenocortical axis, leaving them in a state of arousal, and potentially altering their stress response (Douglas and Hill, 2013). However, how maternal psychological experience of childbirth might indirectly affect her infant's behaviour has yet to be fully considered.

    • Practice-based interpretation of ultrasound studies leads the way to more effective clinical support and less pharmaceutical and surgical intervention for breastfeeding infants

      2018, Midwifery
      Citation Excerpt :

      Secondly, a neurotypical baby who has repeated experiences of frustration at the breast due to an inability to maintain positional stability and transfer milk comfortably may develop a conditioned hyperarousal of the sympathetic nervous system and hypothalamic-pituitary-adrenal axis (referred to here as conditioned SNS hyperarousal), either when presented with the breast or as the feed progresses. This mechanism is elucidated in the neurobiological model of infant cry-fuss problems (Douglas and Hill, 2013). Conditioned SNS hyperarousal due to positional instability is evident in fussiness with latching, repeated pulling off the breast, back-arching, and crying, and may be referred to as ‘aversive feeding behaviour’, ‘breast refusal’ or ‘oral aversion’.

    View all citing articles on Scopus
    1

    Present Address: School of Population Health, The University of Queensland Herston, Queensland 4029, Australia.

    View full text