Opinion

Feeding circuit development and early-life influences on future feeding behaviour

  • Nature Reviews Neuroscience volume 19, pages 302316 (2018)
  • doi:10.1038/nrn.2018.23
  • Download Citation
Published:

Abstract

A wide range of maternal exposures — undernutrition, obesity, diabetes, stress and infection — are associated with an increased risk of metabolic disease in offspring. Developmental influences can cause persistent structural changes in hypothalamic circuits regulating food intake in the service of energy balance. The physiological relevance of these alterations has been called into question because maternal impacts on daily caloric intake do not persist to adulthood. Recent behavioural and epidemiological studies in humans provide evidence that the relative contribution of appetitive traits related to satiety, reward and the emotional aspects of food intake regulation changes across the lifespan. This Opinion article outlines a neurodevelopmental framework to explore the possibility that crosstalk between developing circuits regulating different modalities of food intake shapes future behavioural responses to environmental challenges.

  • Subscribe to Nature Reviews Neuroscience for full access:

    $265

    Subscribe

Additional access options:

Already a subscriber?  Log in  now or  Register  for online access.

References

  1. 1.

    & Developmental programming of obesity in mammals. Exp. Physiol. 92, 287–298 (2007).

  2. 2.

    Early life programming of obesity: the impact of the perinatal environment on the development of obesity and metabolic dysfunction in the offspring. Curr. Diabetes Rev. 8, 55–68 (2012).

  3. 3.

    & The thrifty phenotype hypothesis. Br. Med. Bull. 60, 5–20 (2001).

  4. 4.

    et al. Thrifty metabolic programming in rats is induced by both maternal undernutrition and postnatal leptin treatment, but masked in the presence of both: implications for models of developmental programming. BMC Genomics 15, 49 (2014).

  5. 5.

    Early life nutrition, epigenetics and programming of later life disease. Nutrients 6, 2165–2178 (2014).

  6. 6.

    et al. The early origins of obesity and insulin resistance: timing, programming and mechanisms. Int. J. Obes. 40, 229–238 (2016).

  7. 7.

    & Developmental specification of metabolic circuitry. Front. Neuroendocrinol. 39, 38–51 (2015).

  8. 8.

    & Early life origins of metabolic disease: Developmental programming of hypothalamic pathways controlling energy homeostasis. Front. Neuroendocrinol. 39, 3–16 (2015).

  9. 9.

    , & Trophic action of leptin on hypothalamic neurons that regulate feeding. Science 304, 108–110 (2004).

  10. 10.

    , , & The timing of “catchup growth” affects metabolism and appetite regulation in male rats born with intrauterine growth restriction. Am. J. Physiol. Regul. Integr. Comp. Physiol. 297, R813–R824 (2009).

  11. 11.

    , , , & Developmental programming of energy balance regulation: is physical activity more 'programmable' than food intake? Proc. Nutr. Soc. 75, 73–77 (2016).

  12. 12.

    et al. Transgenerational effects of caloric restriction on appetite: a meta-analysis. Obes. Rev. 15, 294–309 (2014).

  13. 13.

    , & Prenatal exposure to a maternal low-protein diet programmes a preference for high-fat foods in the young adult rat. Br. J. Nutr. 92, 513–520 (2004).

  14. 14.

    , & A maternal 'junk food' diet in pregnancy and lactation promotes an exacerbated taste for 'junk food' and a greater propensity for obesity in rat offspring. Br. J. Nutr. 98, 843–851 (2007).

  15. 15.

    et al. Prenatal exposure to the Dutch famine is associated with a preference for fatty foods and a more atherogenic lipid profile. Am. J. Clin. Nutr. 88, 1648–1652 (2008).

  16. 16.

    , & Early life exposure to a high fat diet promotes long-term changes in dietary preferences and central reward signaling. Neuroscience 162, 924–932 (2009).

  17. 17.

    et al. Does birth weight predict childhood diet in the Avon longitudinal study of parents and children? J. Epidemiol. Commun. Health 59, 955–960 (2005).

  18. 18.

    Cerebral hemisphere regulation of motivated behavior. Brain Res. 886, 113–164 (2000).

  19. 19.

    Multiple neural systems controlling food intake and body weight. Neurosci. Biobehavioral Rev. 26, 393–428 (2002).

  20. 20.

    & Three pillars for the neural control of appetite. Annu. Rev. Physiol. 79, 401–423 (2017).

  21. 21.

    The direct and indirect controls of meal size. Neurosci. Biobehav Rev. 20, 41–46 (1996).

  22. 22.

    & Functional organization of neuronal and humoral signals regulating feeding behavior. Annu. Rev. Nutr. 33, 1–21 (2013).

  23. 23.

    Gustatory responses in the hypothalamus. Brain Res. 21, 63–77 (1970).

  24. 24.

    & Efferent connections of the parabrachial nucleus in the rat. Brain Res. 197, 291–317 (1980).

  25. 25.

    , , & Activation of lateral hypothalamus-projecting parabrachial neurons by intraorally delivered gustatory stimuli. Front. Neural Circuits 8, 86 (2014).

  26. 26.

    The parabrachial nucleus and conditioned taste aversion. Brain Res. Bull. 48, 239–254 (1999).

  27. 27.

    , & Integration of gastric distension and gustatory responses in the parabrachial nucleus. Am. J. Physiol. Regul. Integr. Comp. Physiol. 281, R1581–R1593 (2001).

  28. 28.

    , , & Genetic identification of a neural circuit that suppresses appetite. Nature 503, 111–114 (2013).

  29. 29.

    , , , & Glucagon-like Peptide1 receptor signaling in the lateral parabrachial nucleus contributes to the control of food intake and motivation to feed. Neuropsychopharmacology 39, 2233–2243 (2014).

  30. 30.

    Ascending projections from the caudal visceral nucleus of the solitary tract to brain regions involved in food intake and energy expenditure. Brain Res. 1350, 18–34 (2010).

  31. 31.

    , & Modulation of parabrachial taste neurons by electrical and chemical stimulation of the lateral hypothalamus and amygdala. J. Neurophysiol. 93, 1183–1196 (2005).

  32. 32.

    et al. GABAergic projections from lateral hypothalamus to paraventricular hypothalamic nucleus promote feeding. J. Neurosci. 35, 3312–3318 (2015).

  33. 33.

    et al. The distribution and mechanism of action of ghrelin in the CNS demonstrates a novel hypothalamic circuit regulating energy homeostasis. Neuron 37, 649–661 (2003).

  34. 34.

    , , , & Orexigen-sensitive NPY/AgRP pacemaker neurons in the hypothalamic arcuate nucleus. Nat. Neurosci. 7, 493–494 (2004).

  35. 35.

    , & AGRP neurons are sufficient to orchestrate feeding behavior rapidly and without training. Nat. Neurosci. 14, 351–355 (2011).

  36. 36.

    et al. Rapid, reversible activation of AgRP neurons drives feeding behavior in mice. J. Clin. Invest. 121, 1424–1428 (2011).

  37. 37.

    , , & Parallel, redundant circuit organization for homeostatic control of feeding behavior. Cell 155, 1337–1350 (2013).

  38. 38.

    , , & Ghrelin induces feeding in the mesolimbic reward pathway between the ventral tegmental area and the nucleus accumbens. Peptides 26, 2274–2279 (2005).

  39. 39.

    et al. Ghrelin modulates the activity and synaptic input organization of midbrain dopamine neurons while promoting appetite. J. Clin. Invest. 116, 3229–3239 (2006).

  40. 40.

    et al. Leptin receptor signaling in midbrain dopamine neurons regulates feeding. Neuron 51, 801–810 (2006).

  41. 41.

    et al. Evidence that the caudal brainstem is a target for the inhibitory effect of leptin on food intake. Endocrinology 143, 239–246 (2002).

  42. 42.

    et al. Endogenous leptin signaling in the caudal nucleus tractus solitarius and area postrema is required for energy balance regulation. Cell Metab. 11, 77–83 (2010).

  43. 43.

    , & Leptin receptor signaling in the lateral parabrachial nucleus contributes to the control of food intake. Am. J. Physiol. Regul. Integr. Comp. Physiol. 307, R1338–R1344 (2014).

  44. 44.

    , , & Sensory detection of food rapidly modulates arcuate feeding circuits. Cell 160, 829–841 (2015).

  45. 45.

    , , & Ghrelin modulates brain activity in areas that control appetitive behavior. Cell Metab. 7, 400–409 (2008).

  46. 46.

    , , , & Basolateral to central amygdala neural circuits for appetitive behaviors. Neuron 93, 1464–1479.e5 (2017).

  47. 47.

    & Excitatory synaptic transmission in the lateral and central amygdala. Ann. NY Acad. Sci. 985, 67–77 (2003).

  48. 48.

    et al. Circuit architecture of VTA dopamine neurons revealed by systematic input-output mapping. Cell 162, 622–634 (2015).

  49. 49.

    , , , & The inhibitory circuit architecture of the lateral hypothalamus orchestrates feeding. Science 341, 1517–1521 (2013).

  50. 50.

    et al. Maternal macronutrient and energy intakes in pregnancy and offspring intake at 10 y: exploring parental comparisons and prenatal effects. Am. J. Clin. Nutr. 91, 748–756 (2010).

  51. 51.

    et al. Maternal high-fat diet and obesity impact palatable food intake and dopamine signaling in nonhuman primate offspring. Obesity 23, 2157–2164 (2015).

  52. 52.

    & Appetitive learning in 1day-old rat pups. Science 205, 419–421 (1979).

  53. 53.

    Feeding and behavioral activation in infant rats. Science 205, 206–209 (1979).

  54. 54.

    , & Ontogeny of glucose inhibition of independent ingestion in preweanling rats. Brain Res. Bull. 17, 673–679 (1986).

  55. 55.

    , , , & Intake of different concentrations of sucrose and corn oil in preweanling rats. Am. J. Physiol. 262, R624–R627 (1992).

  56. 56.

    & Olfactory influences on the ingestive behavior of infant rats. Dev. Psychobiol. 20, 313–331 (1987).

  57. 57.

    , & Flavor preferences conditioned by postingestive effects of nutrients in preweanling rats. Physiol. Behav. 84, 407–419 (2005).

  58. 58.

    & Development of learned flavor preferences. Dev. Psychobiol 48, 380–388 (2006).

  59. 59.

    , & Naloxone decreases intake of 10% sucrose in preweanling rats. Pharmacol. Biochem. Behav. 54, 333–337 (1996).

  60. 60.

    & The effect of finite periods of undernutrition at different ages on the composition and subsequent development of the rat. Proc. R. Soc. Lond. B Biol. Sci. 158, 329–342 (1963).

  61. 61.

    , , & Intake and use of milk nutrients by rat pups suckled in small, medium, or large litters. Am. J. Physiol. 260, R1104–R1113 (1991).

  62. 62.

    & Development of the cyto- and chemoarchitectural organization of the rat nucleus of the solitary tract. Anat. Embryol. 203, 265–282 (2001).

  63. 63.

    & Establishment of vagal sensorimotor circuits during fetal development in rats. J. Neurobiol. 24, 641–659 (1993).

  64. 64.

    , & Retrograde transynaptic pseudorabies virus infection of central autonomic circuits in neonatal rats. Brain Res. Dev. Brain Res. 114, 207–216 (1999).

  65. 65.

    & A nutritive control of independent ingestion in rat pups emerges by nine days of age. Physiol. Behav. 46, 873–879 (1989).

  66. 66.

    Postnatal development of hypothalamic inputs to the dorsal vagal complex in rats. Physiol. Behav. 79, 65–70 (2003).

  67. 67.

    & Chronically decerebrate rats demonstrate satiation but not bait shyness. Science 201, 267–269 (1978).

  68. 68.

    , & Differential effects of upper gastrointestinal fill on milk ingestion and nipple attachment in the suckling rat. Dev. Psychobiol 15, 309–330 (1982).

  69. 69.

    & Progressive postnatal increases in Fos immunoreactivity in the forebrain and brain stem of rats after viscerosensory stimulation with lithium chloride. Am. J. Physiol. Regul. Integr. Comp. Physiol. 292, R1212–R1223 (2007).

  70. 70.

    , , & Exogenous cholecystokinin activates cFos expression in medullary but not hypothalamic neurons in neonatal rats. Brain Res. Dev. Brain Res. 77, 140–145 (1994).

  71. 71.

    & Postnatal development of the parabrachial gustatory zone in rat: dendritic morphology and mitochondrial enzyme activity. Brain Res. Bull. 21, 79–94 (1988).

  72. 72.

    , & Postnatal ontogeny of glutamate receptors in the rat nucleus tractus solitarii and ventrolateral medulla. J. Auton. Nerv. Syst. 65, 25–32 (1997).

  73. 73.

    & Activity-dependent reorganization of local circuitry in the developing visceral sensory system. Neuroscience 150, 905–914 (2007).

  74. 74.

    Postnatal development of catecholamine inputs to the paraventricular nucleus of the hypothalamus in rats. J. Comp. Neurol. 438, 411–422 (2001).

  75. 75.

    , & Formation of projection pathways from the arcuate nucleus of the hypothalamus to hypothalamic regions implicated in the neural control of feeding behavior in mice. J. Neurosci. 24, 2797–2805 (2004).

  76. 76.

    & Postnatal development of rat nucleus tractus solitarius neurons: morphological and electrophysiological evidence. Neuroscience 93, 293–305 (1999).

  77. 77.

    Ontogeny of hypothalamic-hindbrain feeding control circuits. Dev. Psychobiol 48, 389–396 (2006).

  78. 78.

    , , , & Neonatal onset of leptin signaling in dopamine neurons of the ventral tegmental area in the rat. J. Neuroendocrinol. 26, 835–843 (2014).

  79. 79.

    , , & Developmental responses of the lateral hypothalamus to leptin in neonatal rats, and its implications for the development of functional connections with the ventral tegmental area. J. Neuroendocrinol. 28, 12354 (2016).

  80. 80.

    , , & Differentiation of the midbrain dopaminergic pathways during mouse development. J. Comp. Neurol. 476, 301–311 (2004).

  81. 81.

    , , & The pre- and postnatal development of the dopaminergic cell groups in the ventral mesencephalon and the dopaminergic innervation of the striatum of the rat. Neuroscience 25, 857–887 (1988).

  82. 82.

    , , , & Postnatal development of the dopaminergic system of the striatum in the rat. Neuroscience 110, 245–256 (2002).

  83. 83.

    & Getting connected in the dopamine system. Prog. Neurobiol. 85, 75–93 (2008).

  84. 84.

    , & Differential ontogeny of multiple opioid receptors (mu, delta, and kappa). J. Neurosci. 5, 584–588 (1985).

  85. 85.

    & Development of opioid systems: peptides, receptors and pharmacology. Brain Res. 434, 397–421 (1987).

  86. 86.

    , , & Postnatal development of the rat neostriatum: electrophysiological, light- and electron-microscopic studies. Dev. Neurosci. 20, 125–145 (1998).

  87. 87.

    & Comparative postnatal development of dopamine D(1), D(2) and D(4) receptors in rat forebrain. Int. J. Dev. Neurosci. 18, 29–37 (2000).

  88. 88.

    , , & Changes in properties of neuronal responses in two cortical taste areas in rats of various ages. Neurosci. Res. 19, 407–417 (1994).

  89. 89.

    , & Pomc-expressing progenitors give rise to antagonistic neuronal populations in hypothalamic feeding circuits. Nat. Med. 16, 403–405 (2010).

  90. 90.

    et al. Leptin-dependent STAT3 phosphorylation in postnatal mouse hypothalamus. Brain Res. 1215, 105–115 (2008).

  91. 91.

    et al. Developmental changes in hypothalamic leptin receptor: relationship with the postnatal leptin surge and energy balance neuropeptides in the postnatal rat. Am. J. Physiol. Regul. Integr. Comp. Physiol. 296, R631–R639 (2009).

  92. 92.

    et al. Developmental switch of leptin signaling in arcuate nucleus neurons. J. Neurosci. 34, 9982–9994 (2014).

  93. 93.

    & Ontogeny of the hypothalamic neuropeptide Y system. Physiol. Behav. 79, 47–63 (2003).

  94. 94.

    & Neonatal leptin exposure specifies innervation of presympathetic hypothalamic neurons and improves the metabolic status of leptin-deficient mice. J. Neurosci. 33, 840–851 (2013).

  95. 95.

    et al. Neonatal ghrelin programs development of hypothalamic feeding circuits. J. Clin. Invest. 125, 846–858 (2015).

  96. 96.

    et al. Developmental changes in synaptic distribution in arcuate nucleus neurons. J. Neurosci. 35, 8558–8569 (2015).

  97. 97.

    , , , & Postnatal undernutrition delays a key step in the maturation of hypothalamic feeding circuits. Mol. Metab. 5, 198–209 (2016).

  98. 98.

    , & Postnatal leptin surge and regulation of circadian rhythm of leptin by feeding. Implications for energy homeostasis and neuroendocrine function. J. Clin. Invest. 101, 1020–1027 (1998).

  99. 99.

    , & Leptin alters metabolic rates before acquisition of its anorectic effect in developing neonatal mice. Am. J. Physiol. 277, R742–R747 (1999).

  100. 100.

    & Postnatal regulation of hypothalamic neuropeptide expression by leptin: implications for energy balance and body weight regulation. Regul. Pept. 92, 1–7 (2000).

  101. 101.

    & Developmental effects of ghrelin. Peptides 32, 2362–2366 (2011).

  102. 102.

    The development with age of hypothalamic restraint upon the appetite of the rat. J. Endocrinol. 16, 9–17 (1957).

  103. 103.

    et al. Targeted disruption of the melanocortin4 receptor results in obesity in mice. Cell 88, 131–141 (1997).

  104. 104.

    & Disruption of hypothalamic leptin signaling in mice leads to early-onset obesity, but physiological adaptations in mature animals stabilize adiposity levels. J. Clin. Invest. 120, 2931–2941 (2010).

  105. 105.

    et al. Obesity-programmed mice are rescued by early genetic intervention. J. Clin. Invest. 122, 4203–4212 (2012).

  106. 106.

    Developmental influences on circuits programming susceptibility to obesity. Front. Neuroendocrinol. 39, 17–27 (2015).

  107. 107.

    & Unique salience of maternal breast odors for newborn infants. Neurosci. Biobehav Rev. 23, 439–449 (1999).

  108. 108.

    , , & An assessment of the salient olfactory environment of formula-fed infants. Physiol. Behav. 50, 907–911 (1991).

  109. 109.

    et al. Maternal breast milk odour induces frontal lobe activation in neonates: a NIRS study. Early Hum. Dev. 86, 541–545 (2010).

  110. 110.

    The gustofacial response: observation on normal and anencephalic newborn infants. Symp. Oral Sens. Percept. 4, 254–278 (1973).

  111. 111.

    , , & Development of the children's eating behaviour questionnaire. J. Child Psychol. Psychiatry 42, 963–970 (2001).

  112. 112.

    , , , & Development and factor structure of the Baby Eating Behaviour Questionnaire in the Gemini birth cohort. Appetite 57, 388–396 (2011).

  113. 113.

    et al. Relationship between formula concentration and rate of growth of normal infants. J. Nutr. 98, 241–254 (1969).

  114. 114.

    The infant's ability to self-regulate caloric intake: a case study. J. Am. Diet Assoc. 84, 543–546 (1984).

  115. 115.

    & Caloric compensation and sensory specific satiety: evidence for self regulation of food intake by young children. Appetite 7, 323–331 (1986).

  116. 116.

    , , , & Relationship between portion size and energy intake among infants and toddlers: evidence of self-regulation. J. Am. Diet Assoc. 106, S77–S83 (2006).

  117. 117.

    & Prospective associations of eating behaviors with weight gain in infants. Obesity 23, 1881–1885 (2015).

  118. 118.

    , , & Appetitive traits and food intake patterns in early life. Am. J. Clin. Nutr. 103, 231–235 (2016).

  119. 119.

    , , , & Gateshead Milennium Study Core Team. Do maternal ratings of appetite in infants predict later child eating behaviour questionnaire scores and body mass index? Appetite 54, 186–190 (2010).

  120. 120.

    , & Hypothalamus of the human fetus. J. Chem. Neuroanat 26, 253–270 (2003).

  121. 121.

    , , & Energy intake, not energy output, is a determinant of body size in infants. Am. J. Clin. Nutr. 69, 524–530 (1999).

  122. 122.

    , , , & Predictors of body size in the first 2 y of life: a high-risk study of human obesity. Int. J. Obes. Relat. Metab. Disord. 28, 503–513 (2004).

  123. 123.

    , , , & Protein intake at 9 mo of age is associated with body size but not with body fat in 10yold Danish children. Am. J. Clin. Nutr. 79, 494–501 (2004).

  124. 124.

    et al. A frameshift mutation in MC4R associated with dominantly inherited human obesity. Nat. Genet. 20, 111–112 (1998).

  125. 125.

    , , , & Dietary protein intake is associated with body mass index and weight up to 5 y of age in a prospective cohort of twins. Am. J. Clin. Nutr. 103, 389–397 (2016).

  126. 126.

    , , & Developmental and age-related changes of dopamine transporter, and dopamine D1 and D2 receptors in human basal ganglia. Brain Res. 843, 136–144 (1999).

  127. 127.

    & Development of eating behaviors among children and adolescents. Pediatrics 101, 539–549 (1998).

  128. 128.

    , , , & Continuity and stability of eating behaviour traits in children. Eur. J. Clin. Nutr. 62, 985–990 (2008).

  129. 129.

    , , , & Variability and self-regulation of energy intake in young children in their everyday environment. Pediatrics 90, 542–546 (1992).

  130. 130.

    et al. Dietary intake of young twins: nature or nurture? Am. J. Clin. Nutr. 98, 1326–1334 (2013).

  131. 131.

    & Behavioral susceptibility to obesity: Gene-environment interplay in the development of weight. Physiol. Behav. 152, 494–501 (2015).

  132. 132.

    & Early life nutrition and metabolic programming. Ann. NY Acad. Sci. 1212, 78–96 (2010).

  133. 133.

    Developmental programming and diabetes - The human experience and insight from animal models. Best Pract. Res. Clin. Endocrinol. Metab. 24, 541–552 (2010).

  134. 134.

    , & Maternal obesity and developmental programming of metabolic disorders in offspring: evidence from animal models. Exp. Diabetes Res. 2011, 592408 (2011).

  135. 135.

    , & Obesity in young men after famine exposure in utero and early infancy. N. Engl. J. Med. 295, 349–353 (1976).

  136. 136.

    et al. Perinatal risk factors for childhood obesity and metabolic dysregulation. Am. J. Clin. Nutr. 90, 1303–1313 (2009).

  137. 137.

    , , , & Rapid weight gain during infancy and obesity in young adulthood in a cohort of African Americans. Am. J. Clin. Nutr. 77, 1374–1378 (2003).

  138. 138.

    et al. Anthropometric indicators of body composition in young adults: relation to size at birth and serial measurements of body mass index in childhood in the New Delhi birth cohort. Am. J. Clin. Nutr. 82, 456–466 (2005).

  139. 139.

    & Rapid infancy weight gain and subsequent obesity: systematic reviews and hopeful suggestions. Acta Paediatr. 95, 904–908 (2006).

  140. 140.

    et al. Association of weight gain in infancy and early childhood with metabolic risk in young adults. J. Clin. Endocrinol. Metab. 92, 98–103 (2007).

  141. 141.

    et al. Crossing growth percentiles in infancy and risk of obesity in childhood. Arch. Pediatr. Adolesc. Med. 165, 993–998 (2011).

  142. 142.

    & Flavor perception in human infants: development and functional significance. Digestion 83 (Suppl. 1), 1–6 (2011).

  143. 143.

    et al. Intrauterine growth restriction and the fetal programming of the hedonic response to sweet taste in newborn infants. Int. J. Pediatr. 2012, 657379 (2012).

  144. 144.

    et al. Severe intrauterine growth restriction is associated with higher spontaneous carbohydrate intake in young women. Pediatr. Res. 65, 215–220 (2009).

  145. 145.

    & Possible association between low birth weight and later heart disease needs to be investigated further. BMJ 316, 1247–1248 (1998).

  146. 146.

    , , , & Associations of gestational exposure to famine with energy balance and macronutrient density of the diet at age 58 years differ according to the reference population used. J. Nutr. 139, 1555–1561 (2009).

  147. 147.

    , , , & Nature and nurture in infant appetite: analysis of the Gemini twin birth cohort. Am. J. Clin. Nutr. 91, 1172–1179 (2010).

  148. 148.

    , , & Prospective associations between appetitive traits and weight gain in infancy. Am. J. Clin. Nutr. 94, 1562–1567 (2011).

  149. 149.

    , , & Appetite and growth: a longitudinal sibling analysis. JAMA Pediatr. 168, 345–350 (2014).

  150. 150.

    et al. Prospective associations of appetitive traits at 3 and 12 months of age with body mass index and weight gain in the first 2 years of life. BMC Pediatr. 15, 153 (2015).

  151. 151.

    , , & The association of birth weight and postnatal growth with energy intake and eating behavior at 5 years of age - a birth cohort study. Int. J. Behav. Nutr. Phys. Act 13, 15 (2016).

  152. 152.

    et al. To what extent do weight gain and eating avidity during infancy predict later adiposity? Public Health Nutr. 15, 656–662 (2012).

  153. 153.

    & Associations between multiple measures of parental feeding and children's adiposity in United Kingdom preschoolers. Obesity 15, 137–144 (2007).

  154. 154.

    , , & Parental obesity moderates the relationship between childhood appetitive traits and weight. Obesity 21, 815–823 (2013).

  155. 155.

    et al. Meal size is a critical driver of weight gain in early childhood. Sci. Rep. 6, 28368 (2016).

  156. 156.

    et al. Genetic and environmental effects on body mass index from infancy to the onset of adulthood: an individual-based pooled analysis of 45 twin cohorts participating in the COllaborative project of Development of Anthropometrical measures in Twins (CODATwins) study. Am. J. Clin. Nutr. 104, 371–379 (2016).

  157. 157.

    , & Patterning, specification, and differentiation in the developing hypothalamus. Wiley Interdiscip Rev. Dev. Biol. 4, 445–468 (2015).

  158. 158.

    , & The early origins of food preferences: targeting the critical windows of development. FASEB J. 29, 365–373 (2015).

  159. 159.

    & Changes in muopioid receptor expression and function in the mesolimbic system after long-term access to a palatable diet. Pharmacol. Ther. 154, 110–119 (2015).

  160. 160.

    Brown adipose tissue growth and development. Scientifica 2013, 305763 (2013).

  161. 161.

    & Effects of rearing temperature on body weight and abdominal fat in male and female rats. Am. J. Physiol. 274, R398–R405 (1998).

  162. 162.

    et al. Vagal tone dominates autonomic control of mouse heart rate at thermoneutrality. Am. J. Physiol. Heart Circ. Physiol. 294, H1581–H1588 (2008).

  163. 163.

    & Nonshivering thermogenesis and its adequate measurement in metabolic studies. J. Exp. Biol. 214, 242–253 (2011).

  164. 164.

    , , & Anti-obesity and metabolic efficacy of the beta3adrenergic agonist, CL316243, in mice at thermoneutrality compared to 22 degrees C. Obes. (Silver Spring) 23, 1450–1459 (2015).

  165. 165.

    et al. Anthropometric measures in middle age after exposure to famine during gestation: evidence from the Dutch famine. Am. J. Clin. Nutr. 85, 869–876 (2007).

  166. 166.

    et al. Perinatal undernutrition stimulates seeking food reward. Int. J. Dev. Neurosci. 31, 334–341 (2013).

  167. 167.

    , , , & Increased palatable food intake and response to food cues in intrauterine growth-restricted rats are related to tyrosine hydroxylase content in the orbitofrontal cortex and nucleus accumbens. Behav. Brain Res. 287, 73–81 (2015).

  168. 168.

    et al. Perinatal malnutrition stimulates motivation through reward and enhances drd(1a) receptor expression in the ventral striatum of adult mice. Pharmacol. Biochem. Behav. 134, 106–114 (2015).

  169. 169.

    et al. Intrauterine growth restriction increases the preference for palatable foods and affects sensitivity to food rewards in male and female adult rats. Brain Res. 1618, 41–49 (2015).

  170. 170.

    et al. Intrauterine growth restriction modifies the hedonic response to sweet taste in newborn pups - Role of the accumbal muopioid receptors. Neuroscience 322, 500–508 (2016).

  171. 171.

    et al. Suboptimal maternal diets alter mu opioid receptor and dopamine type 1 receptor binding but exert no effect on dopamine transporters in the offspring brain. Int. J. Dev. Neurosci. 64, 21–28 (2016).

  172. 172.

    , , & Dietary obesity and neonatal sympathectomy. I. Effects on body composition and brown adipose. Am. J. Physiol. 247, R979–R987 (1984).

  173. 173.

    et al. Perinatal elevation of hypothalamic insulin, acquired malformation of hypothalamic galaninergic neurons, and syndrome xlike alterations in adulthood of neonatally overfed rats. Brain Res. 836, 146–155 (1999).

  174. 174.

    & Meal parameters and vagal gastrointestinal afferents in mice that experienced early postnatal overnutrition. Physiol. Behav. 101, 184–191 (2010).

  175. 175.

    , & Early dietary intervention: long-term effects on blood pressure, brain neuropeptide Y, and adiposity markers. Am. J. Physiol. Endocrinol. Metab. 288, E1236–E1243 (2005).

  176. 176.

    et al. Perinatal overfeeding in rats results in increased levels of plasma leptin but unchanged cerebrospinal leptin in adulthood. Int. J. Obes. 31, 371–377 (2007).

  177. 177.

    , , & Factors predicting nongenetic variability in body weight gain induced by a high-fat diet in inbred C57BL/6J mice. Obesity 20, 1179–1188 (2012).

  178. 178.

    et al. Observations on the orexigenic hypothalamic neuropeptide Ysystem in neonatally overfed weanling rats. J. Neuroendocrinol. 11, 541–546 (1999).

  179. 179.

    et al. Hypothalamic neuropeptide Y levels in weaning offspring of low-protein malnourished mother rats. Neuropeptides 34, 1–6 (2000).

  180. 180.

    et al. Role of premature leptin surge in obesity resulting from intrauterine undernutrition. Cell Metab. 1, 371–378 (2005).

  181. 181.

    et al. Large litter rearing enhances leptin sensitivity and protects selectively bred diet-induced obese rats from becoming obese. Endocrinology 151, 4270–4279 (2010).

  182. 182.

    & Maternal “junk-food” feeding of rat dams alters food choices and development of the mesolimbic reward pathway in the offspring. FASEB J. 25, 2167–2179 (2011).

  183. 183.

    et al. Little appetite for obesity: meta-analysis of the effects of maternal obesogenic diets on offspring food intake and body mass in rodents. Int. J. Obes. 39, 1669–1678 (2015).

  184. 184.

    & Consuming a low-fat diet from weaning to adulthood reverses the programming of food preferences in male, but not in female, offspring of 'junk food'-fed rat dams. Acta Physiol. 210, 127–141 (2014).

  185. 185.

    , , , & Maternal high-fat diet alters methylation and gene expression of dopamine and opioid-related genes. Endocrinology 151, 4756–4764 (2010).

  186. 186.

    et al. Sex and age-dependent effects of a maternal junk food diet on the muopioid receptor in rat offspring. Behav. Brain Res. 301, 124–131 (2016).

  187. 187.

    et al. Obesity at conception programs the opioid system in the offspring brain. Neuropsychopharmacology 39, 801–810 (2014).

  188. 188.

    et al. Perinatal western diet consumption leads to profound plasticity and GABAergic phenotype changes within hypothalamus and reward pathway from birth to sexual maturity in rat. Front. Endocrinol. 8, 216 (2017).

  189. 189.

    , & Methyl donor supplementation blocks the adverse effects of maternal high fat diet on offspring physiology. PLOS ONE 8, e63549 (2013).

  190. 190.

    , & Naloxone treatment alters gene expression in the mesolimbic reward system in 'junk food' exposed offspring in a sex-specific manner but does not affect food preferences in adulthood. Physiol. Behav. 133, 14–21 (2014).

  191. 191.

    , & A maternal cafeteria diet during gestation and lactation promotes adiposity and impairs skeletal muscle development and metabolism in rat offspring at weaning. J. Physiol. 567, 951–961 (2005).

  192. 192.

    , , & Postnatal environment overrides genetic and prenatal factors influencing offspring obesity and insulin resistance. Am. J. Physiol. Regul. Integr. Comp. Physiol. 291, R768–R778 (2006).

  193. 193.

    , , & The effects of prenatal exposure to a 'junk food' diet on offspring food preferences and fat deposition can be mitigated by improved nutrition during lactation. J. Dev. Origins Health Dis. 4, 348–357 (2013).

  194. 194.

    et al. Neonatal insulin action impairs hypothalamic neurocircuit formation in response to maternal high-fat feeding. Cell 64, 21–28 (2014).

  195. 195.

    The first months of life: a critical period for development of obesity. Am. J. Clin. Nutr. 87, 1587–1589 (2008).

  196. 196.

    , , & Fetal growth restriction promotes physical inactivity and obesity in female mice. Int. J. Obes. 39, 98–104 (2015).

  197. 197.

    , , & Delemarre- Hypothalamic neuropeptide expression of juvenile and middle-aged rats after early postnatal food restriction. Endocrinology 149, 3617–3625 (2008).

  198. 198.

    , , , & Respective contributions of maternal insulin resistance and diet to metabolic and hypothalamic phenotypes of progeny. Obesity 19, 492–499 (2010).

  199. 199.

    et al. Hypothalamic neural projections are permanently disrupted in diet-induced obese rats. Cell Metab. 7, 179–185 (2008).

  200. 200.

    et al. Early overnutrition results in early-onset arcuate leptin resistance and increased sensitivity to high-fat diet. Endocrinology 151, 1598–1610 (2010).

  201. 201.

    et al. Maternal obesity induced by diet in rats permanently influences central processes regulating food intake in offspring. PLOS ONE 4, e5870 (2009).

  202. 202.

    & Maternal diabetes compromises the organization of hypothalamic feeding circuits and impairs leptin sensitivity in offspring. Endocrinology 152, 4171–4179 (2011).

  203. 203.

    , & Preferential fat intake of pups nursed by dams fed low fat diet during pregnancy and lactation is higher than that of pups nursed by dams fed control diet and high fat diet. J. Nutr. Sci. Vitaminol. 54, 215–222 (2008).

  204. 204.

    et al. Palatability can drive feeding independent of AgRP neurons. Cell Metab. 22, 646–657 (2015).

  205. 205.

    et al. AgRP neurons regulate development of dopamine neuronal plasticity and nonfood-associated behaviors. Nat. Neurosci. 5, 1108–1110 (2012).

  206. 206.

    , , & NPY/AgRP neurons are essential for feeding in adult mice but can be ablated in neonates. Science 310, 683–685 (2005).

  207. 207.

    et al. Maternal high-fat intake alters presynaptic regulation of dopamine in the nucleus accumbens and increases motivation for fat rewards in the offspring. Neuroscience 176, 225–236 (2011).

  208. 208.

    et al. Ghrelin mediates stress-induced food-reward behavior in mice. J. Clin. Invest. 121, 2684–2692 (2011).

  209. 209.

    et al. Structural and molecular interrogation of intact biological systems. Nature 497, 332–337 (2013).

  210. 210.

    et al. Long-term dynamics of CA1 hippocampal place codes. Nat. Neurosci. 16, 264–266 (2013).

  211. 211.

    et al. Natural neural projection dynamics underlying social behavior. Cell 157, 1535–1551 (2014).

Download references

Acknowledgements

This work was funded by the US National Institutes of Health (R01 DK089038), the Klarman Family Foundation for Eating Disorders Research and the American Diabetes Association (117IBS208).

Author information

Affiliations

  1. Naomi Berrie Diabetes Center, Columbia University, New York, NY, USA.

    • Lori M. Zeltser
  2. Department of Pathology and Cell Biology, Columbia University, New York, NY, USA.

    • Lori M. Zeltser

Authors

  1. Search for Lori M. Zeltser in:

Competing interests

The author declares no competing financial interests.

Corresponding author

Correspondence to Lori M. Zeltser.

Glossary

Dutch Hunger Winter

A famine that occurred in the Netherlands near the end of World War II. Epidemiological studies of children of pregnant women exposed to this famine provided some of the earliest evidence of maternal programming of disease risk.

Emotional eating

Eating to satisfy emotional needs rather than to satisfy hunger or homeostatic needs; a classic example is eating behaviour in response to stress.

Intrauterine growth restriction

(IUGR). A condition in which a baby is smaller than expected for its gestational age because it is not growing at the normal rate inside the uterus.

Maternal undernutrition

Insufficient food intake during pregnancy and/or lactation, usually resulting in growth restriction.

Metabolic status

The sum of short-term energy availability and long-term energy stores; this information is transmitted by a combination of nutrient (such as glucose), hormonal (such as insulin) and neural (such as vagus-mediated gastric distension or AGRP neuron) signals.

Pre-gravid

The time period before pregnancy.