Skip to main content

Role of Sensory, Social, and Hormonal Signals from the Mother on the Development of Offspring

  • Chapter
  • First Online:
Perinatal Programming of Neurodevelopment

Part of the book series: Advances in Neurobiology ((NEUROBIOL,volume 10))

Abstract

For mammals, sensory, social, and hormonal experience early in life is essential for the continuity of the infant’s development. These experiences come from the mother through maternal care, and have enduring effects on the physiology and behavior of the adult organism. Disturbing the mother–offspring interaction by maternal deprivation (neglect) or exposure to adverse events as chronic stress, maltreatment, or sexual abuse has negative effects on the mental, psychological, physiological, and behavioral health. Indeed, these kinds of negative experiences can be the source of some neuropsychiatric diseases as depression, anxiety, impulsive aggression, and antisocial behavior. The purpose of this chapter is to review the most relevant evidence that supports the participation of cues from the mother and/or littermates during the postnatal preweaning period for the development of nervous system of the offspring. These findings come from the most frequently utilized experimental paradigms used in animal models, such as natural variations in maternal behavior, handling, partial maternal deprivation, and total maternal deprivation and artificial rearing. Through the use of these experimental procedures, it is possible to positively (handling paradigm), or negatively (maternal deprivation paradigms), affect the offspring’s development. Finally, this chapter reviews the importance of the hormones that pups ingest through the maternal milk during early lactation on the development of several physiological systems, including the immune, endocrine systems, as well as on the adult behavior of the offspring.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Afonso VM, Grella SL, Chatterjee D, Fleming AS (2008) Previous maternal experience affects accumbal dopaminergic responses to pup-stimuli. Brain Res 1198:115–123

    CAS  PubMed  Google Scholar 

  • Alberts JR, Gubernick DJ (1983) Reciprocity and resource exchange: a symbiotic model of parent-offspring relation. In: Moltz H, Rosenblum L (eds) Symbiosis in parent-young interactions. Plenum, New York

    Google Scholar 

  • Almeida SS, Tonkiss J, Galler JR (1996) Prenatal protein malnutrition affects exploratory behavior of female rats in the elevated plus-maze test. Physiol Behav 60:675–680

    CAS  PubMed  Google Scholar 

  • Amarant T, Fridkin M, Koch Y (1982) Luteinizing hormone-releasing hormone and thyrotropin-releasing hormone in human and bovine milk. Euro J Biochem 127:647–650

    CAS  Google Scholar 

  • Angelucci L, Patacchioli FR, Chierechetti C, Laureti S (1983) Perinatal mother-offspring pituitary-adrenal interrelationship in rats: corticosterone in milk may affect adult life. Endocrinol Exp 17:191–205

    CAS  PubMed  Google Scholar 

  • Anisman H, Zaharia MD, Meaney MJ, Merali Z (1998) Do early life events permanently alter behavior and hormonal responses to stressors. Int J Dev Neurosci 16:149–164

    CAS  PubMed  Google Scholar 

  • Archibald JG (1945) Some effects of thyroprotein on the composition of milk. J Dairy Sci 51:1933–1935

    Google Scholar 

  • Avishai-Eliner S, Eghbal-Ahmadi M, Tabachnik E, Brunson KI, Baram TZ (2001) Dow-regulation of hypothalamic corticotropin releasing hormone messenger ribonucleic acid (mRNA) precedes early-life experience-induced changes in hippocampal glucocorticoid receptor mRNA. Endocrinology 142:89–97

    CAS  PubMed Central  PubMed  Google Scholar 

  • Aydin S, Ozkan Y, Kumru S (2006) Ghrelin is present in human colostrum, transitional and mature milk. Peptides 27 :878–882

    CAS  PubMed  Google Scholar 

  • Bales K, Carter CS (2002) Oxytocin facilitates parental care in female prairie voles (but not in males). Horm Behav 41:456

    Google Scholar 

  • Bales K, Abdelnabi M, Carter CS (2001) Neonatal injections affects reproductive parameters in male prairie voles. Horm Behav 39:324

    Google Scholar 

  • Ballard FJ, Nield MK, Francis GL, Dahlenburg GW, Wallace JC (1982) The relationship between the insulin content and inhibitory effects of bovine colostrums on protein breakdown in cultured cells. J Cell Physiol 110:249–254

    CAS  PubMed  Google Scholar 

  • Baram T, Koch Y, Hazum E, Fridkin M (1977) Gonadotropin-releasing hormone in milk. Science 198:300–302

    CAS  PubMed  Google Scholar 

  • Barret J, Fleming AS (2011) Annual research review: all mothers are not created equal: neural and psychobiological perspectives on mothering and the importance of individual differences. J Child Psychol Psychiatry 52:368–397

    Google Scholar 

  • Baumrucker CR, Magliaro-Macrina AL (2011) Hormones in milk. Encyclopedia of dairy sciences, 2nd edn. Academic, New York, pp 565–771

    Google Scholar 

  • Beane ML, Cole MA, Spencer RL, Rudy JW (2002) Neonatal handling enhances contextual fear conditioning and alters corticosterone stress responses in young rats. Horm Behav 41:33–40

    CAS  PubMed  Google Scholar 

  • Ben-Jonathan N, Arbogast LA, Hyde JF (1989) Neuroendocrine regulation of prolactin release. Prog Neurobiol 33:399–447

    CAS  PubMed  Google Scholar 

  • Benuck I, Rowe FA (1975) Centrally and peripherally induced anosmia: influences on maternal behavior in lactating female rats. Physiol Behav 14:439–447

    CAS  PubMed  Google Scholar 

  • Berczi I, Nagy E, Kovacs K, Horvath E (1981) Regulation of humoral immunitary in rats by pituitary hormones. Acta Endocrinol 98:506–513

    CAS  PubMed  Google Scholar 

  • Bielecki M, Przala F, Lazewska M (1972) Level of erythropoietin in the woman milk. Acta Physiol 23:435–439

    Google Scholar 

  • Boer GJ (1993) Chronic oxytocion treatment during late gestation and lactation impairs development of rat offspring. Neurotoxicol Teratol 15:383–389

    CAS  PubMed  Google Scholar 

  • Boer GJ, Quak, J, de Vries MC, Heinsbroek RPW (1994) Mild sustained effects of neonatal vasopressin and oxytocin treatment on brain growth and behavior of the rat. Peptides 15:229–236

    CAS  PubMed  Google Scholar 

  • Bohuslav D, Catherine SW, Debra L, McWilliam HS, Dominguez JA, McCuskey RS, Philipps ASF, Koldovsky O (2000) Milk-borne epidermal growth factor modulates intestinal transforming growth factor-α levels in neonatal rats. Pediatr Res 47:194–200

    Google Scholar 

  • Bosch OJ, Kromer SA, Neumann ID (2006) Prenatal stress: opposite effects on anxiety and hypothalamic expression of vasopressin and corticotropin-releasing hormone in rats selectively bred for high and low anxiety. Eur J Neurosci 23:541–551

    PubMed  Google Scholar 

  • Bour DS, Kacsoh B, Mastrol AM (1991) Effect of neonatal milk-prolactin deprivation on the ontogeny of the immune system. Endocr Regul 25:111–119

    PubMed  Google Scholar 

  • Bridges R (1996) Biochemical basis of parental behavior in the rat. Adv Stud Behav 25:215–242

    Google Scholar 

  • Brummelte S, Pawluski JL, Galea LA (2006) High post-partum levels of corticosterone given to dams influence postnatal hippocampal cell proliferation and behavior of offspring: a model of post-partum stress and possible depression. Horm Behav 50:370–382

    CAS  PubMed  Google Scholar 

  • Brummelte S, Schmidt KL, Taves MD, Soma KK, Galea LA (2010) Elevated corticosterone levels in stomach milk, serum, and brain of male and female offspring after maternal corticosterone treatment in the rat. Dev Neurobiol 70:714–725

    CAS  PubMed  Google Scholar 

  • Brummelte S, Lieblich SE, Galea LA (2012) Gestational and postpartum corticosterone exposure to the dam affects behavioral and endocrine outcome of the offspring in a sexual-dimorphic manner. Neuropharmacology 62:406–418

    CAS  PubMed  Google Scholar 

  • Burton C, Lovic V, Fleming AS (2006) Early adversity alters attention and locomotion in adults Sprague-Dawley rats. Behav Neurosci 120:665–675

    PubMed  Google Scholar 

  • Caldji C, Tannenbaum B, Sharma S, Francis D, Plotsky PM, Meaney MJ (1998) Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. Proc Natl Acad Sci U S A 95:5335–5340

    CAS  PubMed Central  PubMed  Google Scholar 

  • Caldji C, Diorio J, Meaney MJ (2000) Variations in maternal care in infancy regulate the development of stress reactivity. Biol Psychiatry 48:1164–1174

    CAS  PubMed  Google Scholar 

  • Carpenter G (1980) Epidermal growth factor is a major growth-promoting agent in human milk. Science 210:198–199

    CAS  PubMed  Google Scholar 

  • Carter CS (1992) Oxytocin and sexual behavior. Neurosci Biobehav Rev 16:131–144

    CAS  PubMed  Google Scholar 

  • Carter CS (2003) Developmental consequences of oxytocin. Physiol Behav 79:383–397

    CAS  PubMed  Google Scholar 

  • Carter CS, Altemus M (1997) Integrative functions of lactional hormones in social behavior and stress management. Ann N Y Acad Sci 807:164–174

    CAS  PubMed  Google Scholar 

  • Casolini P, Cigliana G, Alemán GS, Ruggiere V, Angelucci L, Catalani A (1997) Effect of increased maternal corticosterone during lactation on hippocampal corticosterone receptors, stress response and learning in offspring in the early stages of life. Neuroscience 79:1005–1012

    CAS  PubMed  Google Scholar 

  • Catalani A, Marinelli M, Scaccianoce S, Nicolai R, Muscolo LA, Porcu A, Korányi L, Piazza PV, Angelucci L (1993) Progeny of mothers drinking corticosterone during lactation has lower stress-induced corticosterone secretion and better congnitive performance. Brain Res 624:209–215

    CAS  PubMed  Google Scholar 

  • Catalani A, Casolini P, Scaccianoce S, Patacchioli FR, Spinozzi P, Angelucci L (2000) Maternal corticosterone during lactation permanently affects brain corticosteroid receptors, stress response and behaviour in rat progeny. Neuroscience 1000:319–325

    Google Scholar 

  • Cevreska S, Kovacev VP, Stankovski M, Kalamaras E (1975) The presence of immunologically reactive insulin in milk of women during the first week of lactation and its relation to changes in plasma insulin concentration. God Medicine Fak Skopje 21:35–41

    CAS  Google Scholar 

  • Champagne FA (2008) Epigenetic mechanisms and the transgenerational effects of maternal care. Front Neuroendocrinol 29:386–397

    CAS  PubMed Central  PubMed  Google Scholar 

  • Champagne FA, Meaney MJ (2001) Like mother, like daughter: evidence for non-genomic transmission of parental behavior and stress responsivity. Prog Brain Res 133:287–302

    CAS  PubMed  Google Scholar 

  • Champagne FA, Meaney MJ (2007) Transgenerational effects of social environment on variations in maternal care and behavior response to novelty. Behav Neurosci 121:1353–1363

    PubMed  Google Scholar 

  • Champagne FA, Francis DD, Mar A, Meaney MJ (2003) Variations in maternal care in the rat as a mediating influence for the effects of environment on development. Physiol Behavr 79:359–371

    CAS  Google Scholar 

  • Champagne FA, Weaver ICG, Diorio J, Dymov S, Szyf M, Meaney MJ (2006) Maternal care associated with methylation of the estrogen receptor-alpha1b promoter and estrogen receptor-alpha expression in the medial preoptic area of female offspring. Endocrinology 147:2909–2915

    CAS  PubMed  Google Scholar 

  • Chappell JE, Clandinin MT, Barbe GJ, Armstrong DT (1983) Prostanoid content of human milk: relationships to milk fatty acid content. Endocrinol Exp 17:351–358

    CAS  PubMed  Google Scholar 

  • Chirino R, González-Mariscal G, Beyer C (1999) Efecto de la lesión del bulbo olfatorio accesorio (BOA) sobre diferentes conductas reproductivas de la coneja. Congreso Nacional de Ciencias. Fisiológicas., 42nd, Zacatecas, México, p 0101

    Google Scholar 

  • Chirino R, Beyer C, Rosenblatt JS, González-Mariscal G (2000) Virgin female rabbits show pup-induced maternal behavior (MB) only after lesioning the accessory olfactory bulbs. Dev Psychobiol 36:248

    Google Scholar 

  • Chirino R, Beyer C, Rosenblatt JS, González-Mariscal G (2001) Intranasal zinc sulfate spray induces anosmia but not facilitate maternal behavior in estrous rabbits. Dev Psychobiol 38:197

    Google Scholar 

  • Cirulli F, Gottlieb S, Levine S (1992) Maternal factors regulate stress responsiveness in the neonatal rat. Psychobiology 20:143–152

    Google Scholar 

  • Cirulli F, Berry A, Alleva E (2003) Early disruption of the mother-infant relationship: effects on brain plasticity and implications for psychopathology. Neurosci Biobehav Rev 27:73–82

    CAS  PubMed  Google Scholar 

  • Costela C, Tejedor-Real P, Mico JA, Gilbert-Rahola J (1995) Effect of neonatal handling on learned helplessness model of depression. Physiol Behav 57:407–410

    CAS  PubMed  Google Scholar 

  • Cowie AT, Swinburne JK (1977) Hormones, drugs, metals and pesticides in milk: a guide to the literature. Dairy Sci Abstr 39:391–402

    Google Scholar 

  • Cox DB, Owens RA, Hartmann PE (1996) Blood and milk prolactin and the rate of milk synthesis in women. Exp Physiol 81:1007–1020

    CAS  PubMed  Google Scholar 

  • Crowley WR, Shah GV, Watanobe H, Grosvenor CE (1990) Effects of neonatal exposure to estradiol on prolactin secretion and activity of the tuberoinfundibular dopamine system in young adulthood: comparison with neonatal prolactin deficiency. J Neuroendocrinol 2:19–24

    CAS  PubMed  Google Scholar 

  • Darling J, Laing A, Harkness R (1974) A survey of the steroids in cow’s milk. J Endocrinol 62:291–297

    CAS  PubMed  Google Scholar 

  • Denenberg V, Smith WI, Ross S (1950) A preliminary study of individual and group hoarding in the white rat. J Genet Psychol 77:123–127

    PubMed  Google Scholar 

  • Diaz J, Moore E, Petracca F, Schacher J, Stamper C (1981) Artificial rearing of preweanling rat: the effectiveness of direct intragastric feeding. Physiol Behav 27:1103–1105

    CAS  PubMed  Google Scholar 

  • Diaz J, Moore E, Petracca F, Stamper C (1983) Somatic and central nervous system growth in artificially reared rat pups. Brain Res Bull 11:643–647

    CAS  PubMed  Google Scholar 

  • Dickson RB, Huff KK, Spencer EM, Lippman ME (1985) Induction of epidermal grow factor-related polypeptides by 17β-estradiol in human breast cancer cells. Endocrinology 118:138–142

    Google Scholar 

  • Donatelli AL, Seidman LJ, Goldstein JM, Tsuang MT, Buka SL (2010) Children of parents with affective and non-affective psychose: a longitudinal study of behavior problems. Am J Psychiatry 167:1331–1338

    PubMed Central  PubMed  Google Scholar 

  • Ellis LA, Picciano MF (1995) Bioactive and immunoreactive prolactin variants in human milk. Endocrinology 136:2711–2720

    CAS  PubMed  Google Scholar 

  • Ellis LA, Mastro AM, Picciano MF (1996) Milk-borne prolactin and neonatal development. J Mammary Gland Biol Neoplasia 1:259–269

    CAS  PubMed  Google Scholar 

  • Eriksson L, Valtonen M, Laitinen JT, Paananen M, Kaikkonen M (1998) Diurnal rhythm of melatonin in lactating cows and goats. Acta Vet Scand 39:310

    Google Scholar 

  • Faturi CB, Tiba PA, Kawakami SE, Catallani B, Kerstens M, Suchecki D (2010) Disruptions of the mother-infant relationship and stress-related behaviours: altered corticosterone secretion does not explain everything. Neurosci Biobehav Rev 34:821–834

    CAS  PubMed  Google Scholar 

  • Fleming AS, Luebke C (1981) Timidity prevents the nulliparous female from being a good mother. Physiol Behav 27:863–868

    CAS  PubMed  Google Scholar 

  • Fleming AS, Rosenblatt JS (1974) Olfactory regulation of maternal behavior in rats: I. Effects of olfactory bulb removal in experienced and inexperienced lactating and cycling females. J Comp Physiol 87:221–232

    Google Scholar 

  • Fleming AS, Vaccarino F, Tambosso L, Chee P (1979) Vomeronasal and olfactory system modulation of maternal behavior in the rat. Science 203:327–337

    Google Scholar 

  • Fleming AS, Kraemer GW, Gonzalez A, Lovic V, Ress A, Melo AI (2002) Mothering begets mothering: the transmission of behavior and its neurobiology across generation. Pharmacol Biochem Behav 73:61–75

    CAS  PubMed  Google Scholar 

  • Francis DD, Meaney MJ (1999) Maternal care and the development of stress responses. Curr Opin Neurobiol 9:128–134

    CAS  PubMed  Google Scholar 

  • Francis DD, Dioro J, Liu D, Meaney MJ (1999) Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 285:1155–1158

    Google Scholar 

  • Francis DD, Young LJ, Meaney MJ, Insel TR (2002) Naturally occurring differences in maternal care are associated with the expression of oxytocin and vasopressin (V1a) receptors: gender differences. J Neuroendocrinol 14:349–353

    CAS  PubMed  Google Scholar 

  • Fries AB, Pollak SD (2004) Emotion understanding in postinstitutionalized Eastern European children. Dev Psychopathol 16:355–369

    PubMed  Google Scholar 

  • Fritsche S, Steinhart H (1999) Occurrence of hormonally active compounds in food: a review. Eur Food Res Technol 209:153–179

    CAS  Google Scholar 

  • Gala RR, Singhakowinta A, Brennan MJ (1975) Studies on prolactin in human serum, urine and milk. Horm Res 6:310–320

    CAS  PubMed  Google Scholar 

  • Gala R, Forsyth I, Turvey A (1980) Milk prolactin is biologically active. Life Sci 26:987–993

    CAS  PubMed  Google Scholar 

  • Geschickter CF, Lewis D (1936) Lactogenic substance in the human breast: its use in experimental stimulation of mammary secretion and its assay in cases of cystic. Arch Surg 32:598–617

    Google Scholar 

  • Gimpl G, Fahrenholz F (2001) The oxytocin receptor system: structure, function and regulation. Physiol Behav 81:629–683

    CAS  Google Scholar 

  • Glaser D (2000) Child abuse and neglect and the brain-a review. J Child Psychol Psychiatry 41:97–116

    CAS  PubMed  Google Scholar 

  • Golden ES, Kehn LS, Rehnberg GL, Crofton KM (1995) Effects of developmental hypothyroidism on auditory and motor function in the rat. Toxicol Appl Pharmacol 135:67–76

    Google Scholar 

  • Goldman AS (1993) The immune system of human milk: antimicrobial, anti-inflammatory and immunomodulating properties. Pediatr Infect Dis J 12:664–671

    CAS  PubMed  Google Scholar 

  • Goldman AS, Frawley S (1996) Bioactive components of milk. J Mammary Gland Biol Neoplasia 3:241–242

    Google Scholar 

  • Gonella P, Harnatz P, Walker QA (1989) Prolactin is transported across the epithelium of the jejunum and ileum of suckling rat. J Cell Physiol 140:138–149

    Google Scholar 

  • Gonzalez A, Lovic V, Ward GR, Wainwright PE, Fleming AS (2001) Intergenerational effects of complete maternal deprivation and replacement stimulation on maternal behavior and emotionality in female rats. Dev Psychobiol 38:11–32

    CAS  PubMed  Google Scholar 

  • González-Mariscal G, Kinsley CH (2009) From indifference to ardor: the onset, maintenance, and meaning of the maternal brain. Horm Behav 1:109–136

    Google Scholar 

  • González-Mariscal G, Melo AI (2010) Communication by olfactory signals in rabbits: its role in reproduction. Vitam Horm 83:351–371

    PubMed  Google Scholar 

  • González-Mariscal G, Poindron P (2002) Parental care in mammals: immediate internal and sensory factors of control. Horm Brain Behav 1:215–298

    Google Scholar 

  • Grant WC (1952) Influence of anoxia of a lactating rat on the blood of normal baby rats. Am J Physiol 171:728–729

    Google Scholar 

  • Green JG, McLaughlin KA, Berglund PA, Gruber MJ, Sampson NA, Zaslavsky AM (2010) Childhood adversities and adult psychiatric disorders in the national comorbidity survey replication I: associations with first onset of DSM-IV disorders. Arch Gen Psychiatry 67:113–123

    PubMed Central  PubMed  Google Scholar 

  • Grosvenor CE, Whitworth NS (1976) Incorporation of rat prolactin into rat milk in vivo and in vitro. Endocrinology 70:71–79

    Google Scholar 

  • Grosvenor CE, Picciano MF, Baumrucker CR (1992) Hormones and growth factors in milk. Endocr Rev 14:710–728

    Google Scholar 

  • Grosvenor, CE, Picciano MF, Baumrucker CR (1993) Hormones and grow factors in milk. Endocr Rev 14:710–728

    CAS  PubMed  Google Scholar 

  • Gunnar MR, Nelson CA, Luciana M (2001) Effects of early deprivation: findings from orphanage-reared infants and children. In: Nelson CA, Luciana M (eds) Handbook of developmental cognitive neuroscience. The MIT Press, Massachusetts, pp 617–629

    Google Scholar 

  • Gutman DA, Nemeroff CB (2002) Neurobiology of early life stress: rodent studies. Semin Clin Neuropsychiatry 7:89–95

    PubMed  Google Scholar 

  • Hall WG (1975) Weaning and growth of artificially reared rats. Science 397:726–735

    Google Scholar 

  • Hall FS (1998) Social deprivation of neonatal, adolescent, and adults has distinct neurochemical and behavioral consequences. Crit Rev Neurobiol 2:129–162

    Google Scholar 

  • Hall FS, Wilkinson LS, Humby T, Robbins TW (1999) Maternal deprivation of neonatal rats produces enduring changes in dopamine function. Synapse 32:37–43

    CAS  PubMed  Google Scholar 

  • Haney PM, Estrin CR, Caliendo A, Patel MS (1986) Precocious induction of hepatic glucokinase and melic enzyme in artificially reared rat pups fed a high-carbohydrate diet. Arch Biochem Biophys 244:787–794

    CAS  PubMed  Google Scholar 

  • Harlow HF, Dodsworth RO, Harlow MK (1965) Total social isolation in monkeys. Proc Natl Acad Sci U S A 54:90–97

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hartman RD, Rosella-Dampman LM, Emmert SE, Summy-Long JY (1986) Ontogeny of opioid inhibition of vasopressin and oxytocin release in response to osmotic stimulation. Endocrinology 119:1–11

    CAS  PubMed  Google Scholar 

  • Hazum E, Sabatka JJ, Chang KJ, Brent DA, Findlay JW, Cuatrecasas P (1981) Morphine in cow and human milk: could dietary morphine constitute a ligand for specific morphine (mu) receptors? Science 213:1010–1012

    CAS  PubMed  Google Scholar 

  • Heap RB, Gwyn M, Laing J, Walters D (1973) Pregnancy diagnosis in cows: changes in milk progesterone, concentration during the oestrous cycle and pregnancy measured by rapid radioimmunoassay. J Agric Sci 81:151–159

    CAS  Google Scholar 

  • Heap RB, Hamon M, Fleet IR (1983) Factors affecting oestrone sulphate concentrations in milk. Br J Vet 39:79–88

    Google Scholar 

  • Henschen A, Lottspeich F, Branlt V, Teschemacher H (1979) Novel opioid peptides derived from casein (beta-casomorphins). II. Structure of active components from bovine casein peptone. Hoppe-Seyler´s Zeitschrift für Physiologische Chemie 360:1217–1224

    CAS  PubMed  Google Scholar 

  • Hess JL, Denenberg VH, Zarrow M, Peiffer WD (1969) Modification of the corticosterone response curve as a function of handling in infancy. Physiol Behav 4:102–109

    Google Scholar 

  • Hoeffler JP, Boockfor ER, Frawley LS (1985) Ontogeny of prolactin cells in neonatal rats: initial prolactin secretors also release growth hormone. Endocrinology 117:187–195

    CAS  PubMed  Google Scholar 

  • Hofer MA (1970) Physiological responses of in-cant rats to separation from their mothers. Science 168:871–873

    CAS  PubMed  Google Scholar 

  • Hofer MA (1972) Physiological and behavioral processes in early maternal deprivation, in physiology, emotions and psychosomatic illness, a CIBA foundation symposium, London, Amsterdam

    Google Scholar 

  • Hofer MA (1973a) The role of nutrition in the physiological and behavioral effects of early maternal separation on infant rats. Psychosom Med 35:350–359

    CAS  PubMed  Google Scholar 

  • Hofer MA (1973b) The effects of brief maternal separation on behavior and heart rates of two week old rat pups. Physiol Behav 10:423–427

    CAS  PubMed  Google Scholar 

  • Hoffmann B, Rattenberger E (1977) Testosterone concentrations in tissue from veal calves, bull and heifers and in milk samples. J Anim Sci 45:635–641

    CAS  PubMed  Google Scholar 

  • Holst N, Jenssen TG, Burhol PG (1990) A characterization of immunoreactivesomatostatin in human milk. J Ped Gastroenterol Nutr 10:47–52

    CAS  Google Scholar 

  • Hruska K, Veznik Z (1983) Significance of progesterone determination of milk. Endocrinol Exp (Bratisl) 17:207–211

    CAS  Google Scholar 

  • Huang XW, Zhao ZY, Ji C (2005) Effects of hypothyroidism on apoptosis and the expression of Bcl-2 and Bax gene in the neonatal rat hippocampus neurons. Zhonghua Er Ke Za Zhi 43:48–52

    PubMed  Google Scholar 

  • Insel TR, Winslow JT (1991) Central administration of oxytocin modulates the infant rat’s response to social isolation. Eur J Pharmacol 203:149–152

    CAS  PubMed  Google Scholar 

  • Jansen HT, Kirby JD, Cooke PS, Arambepola N, Iwamoto GA (2007) Impact of neonatal hypothyroidism on reproduction in the male hamster, Mesocricetus auratus. Physiol Behav 23:771–781

    Google Scholar 

  • Jonakait GM, Bohn MC, Black IB (1980) Maternal glucocorticoid hormones influence neurotransmitter phenotypic expression in embryos. Science 210:551–553

    CAS  PubMed  Google Scholar 

  • Kacsoh B, Toth B, Avery L, Deaver D, Baumrucker C, Grosvenor C (1991) Biological and immunological activities of glycosylated and molecular weigth variants of bovine prolactin in colostrums, and milk. J Anim Sci 69:456

    Google Scholar 

  • Kacsoh B, Veress Z, Toth BE, Avery LM, Grosvenor CE (1993) Bioactive and immunoreactive variants of prolactin in milk and serum of lactating rats and their pups. J Endocrinol 138:243–257

    CAS  PubMed  Google Scholar 

  • Kierson JA, Dimatteo DM, Locke RG, Mackley AB, Spear ML (2006) Ghrelin and cholecystokinin in term and preterm human breast milk. Acta Paediatr 95:991–995 (Oslo, Norway 1992)

    PubMed  Google Scholar 

  • Koch Y, Werner H, Fridkin M (1991) Hypothalamichormones in milk. Endocrinol Regulat 25:1–13

    CAS  Google Scholar 

  • Koldovsky O (1980) Hormones in milk. Life Sci 26:1833–1836

    CAS  PubMed  Google Scholar 

  • Koldovsky O (1989) Search for role of milk-borne biologically active peptides for the suckling. J Nutriol 119:1543–1551

    CAS  Google Scholar 

  • Koldovsky O (1996) The potential physiological significance of milk-borne hormonally active substances for the neonate. J Mammary Gland Biol Neoplasia 3:317–323

    Google Scholar 

  • Koldovsky O, Thornbug W (1987) Hormones in milk. J Pediatr Gastroenterol Nutriol 6:172–196

    CAS  Google Scholar 

  • Kosten T, Lee HJ, Kim JJ (2007) Neonatal handling alters learning in adult male and female rats in a task-specific manner. Res Rep 1154:144–153

    CAS  Google Scholar 

  • Kramer KM, Cushing BS, Carter CS (2003) Developmental effects of oxytocin on stress response: single versus repeated exposure. Physiol Behav 79:775–782

    CAS  PubMed  Google Scholar 

  • Krulich L, Koldovsky O, Jumawan J, Lau H, Horowitz C (1977) TSH in serum and milk of normal, thryoidectomized, and hyperthyroid lactating rats. Proc Soc Exp Biol Med 155:599–601

    CAS  PubMed  Google Scholar 

  • Kulski JK, Hartmann PE (1981) Changes in the concentrations of cortisol in milk during different stages of human lactation. Aust J Exp Biol Med Sci 59:769–778

    CAS  PubMed  Google Scholar 

  • Ladd CO, Owens MJ, Nemeroff CB (1996) Persistent changes in corticotrophin-releasing factor neuronal systems induced by maternal deprivation. Endocrinology 137:1212–1218

    CAS  PubMed  Google Scholar 

  • Lee MHS, Williams DI (1974) Changes in licking behavior following handling of young. Anim Behav 2:2679–2681

    Google Scholar 

  • Lehmann J, Feldon J (2000) Long-term biobehavioral effects of maternal separation in the rat: consistent or confusing? Rev Neurosci 11:383–408

    CAS  PubMed  Google Scholar 

  • Leigh H, Hofer M (1973) Behavioral and physiologic effects of littermate removal on the remaining single pup and mother during the pre-weaning period in rats. Psychosomatics 35:497–508

    CAS  Google Scholar 

  • Levine S (1957) Infantile experience and consummatory behavior in adulthood. J Comp Physiol Psychol 50:609–612

    CAS  PubMed  Google Scholar 

  • Levine S, Lewis GW (1959) Critical period for the effects of infantile experience on the maturation of a stress response. Science 129:42–43

    CAS  PubMed  Google Scholar 

  • Lévy F, Kendrick K, Keverne EB, Porter RH, Romeyer A (1996) Physiological, sensory and experiential factors of parental care in sheep. Adv Study Behav 25:385–473

    Google Scholar 

  • Lévy F, Melo AI, Gale Jr BG, Madden M, Fleming AS (2003) Complete maternal deprivation affects social, but not spatial, learning in adult rats. Dev Psychobiol 43:177–191

    PubMed  Google Scholar 

  • Liu D, Diorio J, Tannenbaum B, Caldji C, Francis D, Freedman A et al (1997) Maternal care, hippocampal glucocorticoid receptors and hypothalamic-pituitary-adrenal responses to stress. Science 227:1659–1662

    Google Scholar 

  • Liu D, Caldji C, Sharma S, Plotsky PM, Meaney MJ (2000) Influence of neonatal rearing conditions on stress-induced adrenocorticotropin responses and norepinepherine release in the hypothalamic paraventricular nucleus. J Neuroendocrinol 12:5–12

    PubMed  Google Scholar 

  • Lomanowska AM, Ammari N, Kraemer GW (2010) Interactions between the effects of early isolation rearing and complex housing on adult locomotor activity and sensitivity to amphetamine in rats involve noradrenergic neurotransmission. Pharmacol Biochem Behav 95:100–105

    CAS  PubMed  Google Scholar 

  • Lovic V, Fleming AS (2004) Artificially-reared female rats show reduced prepulse inhibition and deficits in the attentional set-shifting task-reversal of effects with maternal-like licking stimulation. Behav Brain Res 148:209–219

    PubMed  Google Scholar 

  • Lovic V, Fleming AS, Fletcher PJ (2006) Early life tactile stimulation changes adult rat responsiveness to amphetamine. Pharmacol Biochem Behav 84:497–503

    CAS  PubMed  Google Scholar 

  • Macri S, Mason GJ, Wurbel H (2004) Dissociation in the of neonatal maternal separations on maternal care and the offspring’s HPA and fear responses in rats. Eur J Neurosci 20:1017–1024

    PubMed  Google Scholar 

  • Macri S, Chiarotti F, Wurbel H (2008) Maternal separation and maternal care act independently on the development of HPA responses in male rats. Behav Brain Res 191:227–234

    CAS  PubMed  Google Scholar 

  • Malve P (1977) Prolactin and the hormones in milk. J Anim Sci 45:609–616

    Google Scholar 

  • Malve P, McMutry J (1974) Measurement of prolactin in milk by radio immunoassay. J Dairy Sci 57:411–415

    Google Scholar 

  • Malven PV, Head HH, Collier RJ, Buonomo FC (1987) Periparturient changes in secretion and mammary uptake of insulin and in concentrations of insulin and insulin-like growth factors in milk of dairy cows. J Dairy Sci 70:2254–2265

    CAS  PubMed  Google Scholar 

  • Markham JA, Koenig JI (2011) Prenatal stress: role in psychotic and depressive diseases. Psychopharmacology (Berl) 214:89–106

    CAS  Google Scholar 

  • Matthews K, Robbins TW (2003) Early experience as a determinant of adult behavioural responses to reward: the effects of repeated maternal separation in the rat. Neurosci Biobehav Rev 27:45–55

    PubMed  Google Scholar 

  • Matthews K, Wilkinson LS, Robbins TW (1996a) Repeated maternal separation of pre-weanling rats attenuates the behavioural responses to primary and conditioned incentives in adulthood. Physiol Behav 59:99–107

    CAS  PubMed  Google Scholar 

  • Matthews K, Hall FS, Wilkinson LS, Robbins TW (1996b) Retarded acquisition and reduced expression of conditioned locomotor activity in adult rats following repeated early maternal separation: effects of prefeeding, d-amphetamine, dopamine antagonists and clonidine. Psychopharmacology (Berl) 126:75–84

    CAS  Google Scholar 

  • Mayer AD, Rosenblatt JS (1977) Effects of intranasal zinc sulfate on open field and maternal behavior in female rats: experimental effects. J Comp Physiol 89:701–710

    Google Scholar 

  • McGarrigle HHC, Lachelin GCL (1983) Oestrone, oestradiol and oestriol glucosidurinates and sulphates in human puerperal plasma milk. J Steroid Biochem 18:607–611

    CAS  PubMed  Google Scholar 

  • McMurtry JP, Malven PV (1974a) Experimental alterations of prolactin levels in goat milk and plasma. Endocrinology 95:559–564

    CAS  PubMed  Google Scholar 

  • McMurtry JP, Malven PV (1974b) Radioimmunoassay of endogenous and exogenous prolactin in milk of rats. J Endocrinol 61:211–217

    CAS  PubMed  Google Scholar 

  • Meaney MJ (2001) Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu Rev Neurosci 24:1161–1192

    CAS  PubMed  Google Scholar 

  • Meaney MJ, Aitken DH (1985) The effects of early postnatal handling on hippocampal gluco-corticoid receptor concentration: temporal parameters. Dev Brain Res 22:301–304

    Google Scholar 

  • Meaney MJ, Aitken DH, Van Berkel C, Bhatnagar S, Sapolsky RM (1988) Effect of neonatal handling on age-related impairments associated with the hippocampus. Science 239:766–768

    CAS  PubMed  Google Scholar 

  • Meaney MJ, Aitken DH, Viau V, Sharma S, Sarrieau A (1989) Neonatal handling alters adrenocortical negative feedback sensitivity and hippocampal type II glucocorticoid receptor binding in the rat. Neuroendocrinology 50:597–604

    CAS  PubMed  Google Scholar 

  • Meaney MJ, Diorio J, Francis D, Widdowson J, LaPlante P, Caldji C, Sharma S, Seckl JR, Plotsky PM (1996) Early environmental regulation of forebrain glucocorticoid receptor gene expression: implications for adrenocortical responses to stress. Dev Neurosci 18:49–72

    CAS  PubMed  Google Scholar 

  • Meerlo P, Horvath KM, Luiten PG, Angelucci L, Catalani A, Koolhaas JM (2001) Increased maternal corticosterone levels in rats: effects on brain 5-HT1A receptors and behavioral coping with stress in adult offspring. Behav Neurosci 115:1111–1117

    CAS  PubMed  Google Scholar 

  • Melo AI, Lovic V, Gonzalez A, Madden M, Sinopoli K, Fleming AS (2006) Maternal and littermate deprivation disrupt maternal behavior and social-learning of food preference in adulthood: tactile stimulation, nest odor, and social rearing prevent these effects. Dev Psychobiol 48:209–219

    PubMed  Google Scholar 

  • Melo AI, Pérez-Ledezma M, Clapp C, Arnold E, Rivera JC, Fleming AS (2009) Effects of prolactin deficiency during the early postnatal period on the development of maternal behaviors in female rats: mother’s milk makes the difference. Horm Behav 56:281–291

    CAS  PubMed  Google Scholar 

  • Messer M, Thomas EB, Galofre A, Dallman T, Dallmen PR (1969) Artificial feeding of infants rats by continuous infusion. J Nutr 98:404–410

    CAS  PubMed  Google Scholar 

  • Monk EL, Erb RE, Mollet TA (1975) Relationships between immunoreactive estrone and estradiol in milk, blood, and urine of diary cows. J Dairy Sci 58:34–40

    CAS  PubMed  Google Scholar 

  • Moore CL (1984) Maternal contribution to the development of masculine sexual behavior in laboratory rats. Dev Psychobiol 17:347–356

    CAS  PubMed  Google Scholar 

  • Moore SD (2013) Current thinking about nature and nurture. Hist Philosophy Theory Life Sci 1:629–652

    Google Scholar 

  • Morreale de Escobar G, Obregón MJ, Calvo R, Escobar del Rey F (1987) Effects of iodine deficiency on thyroid hormone metabolism and the brain in fetal rats: the role of the maternal transfer of thyroxin. Horm Res 26:12–27

    CAS  PubMed  Google Scholar 

  • Nagano M, Chastre E, Choquet A, Bara J, Gespach C, Kelly PA (1995) Expression of prolactin and growth hormone receptor genes and their isoforms in the gastrointestinal tract. Am Physiol 268:431–442

    Google Scholar 

  • Nilsson S, Nygren K-G, Johansson EDB (1978) Ethinyl estradiol in human milk and plasma after oral administration. Contraception 17:131–139

    CAS  PubMed  Google Scholar 

  • Noonan LR, Continell G, Pedersen CA (1989) Neonatal administration of oxytocin Increases novelty-induced grooming in the adult rat. Pharmacol Biochem Behav 33:555–558

    CAS  PubMed  Google Scholar 

  • Numan M (2006) Hypothalamic neural circuits regulating maternal responsiveness toward infants. Behav Cogn Neurosci Rev 4:163–190

    Google Scholar 

  • Oberkotter LV (1986) Maternal hyperthyroidism during lactation influences thyroid function in suckling rat pups, Manuscript in preparation

    Google Scholar 

  • Ogawa J, Sasahara A, Yoshida T, Sira MM, Futatani T, Kanegane H, Miyawaki T (2004) Role of transforming growth factor-beta in breast milk for initiation of IgA production in newborn infants. Early Hum Dev 77:67–75

    CAS  PubMed  Google Scholar 

  • Olausson H, Uvnas-Moberg K, Sohlstrom A (2003) Postnatal oxytocin alleviates adverse effects in adult rat offspring caused by maternal malnutrition. Am J Physiol Endocrinol Metab 284:475–480

    Google Scholar 

  • Ollivier-Bousquet M, Kann G, Durand G (1993) Prolactin transit through mammary epithelial cells and appearance in milk. Endocr Regul 27:115–124

    CAS  PubMed  Google Scholar 

  • Ostrom KM (1990) A review of the hormone prolactin during lactation. Prog Food Nutr Sci 14:1–44

    CAS  PubMed  Google Scholar 

  • Peaker M, Neville MC (1991) Hormones in milk: chemical signals to the offspring? J Endocrinol 131:1–3

    CAS  PubMed  Google Scholar 

  • Pedersen CA, Boccia ML (2002) Oxytocin links mothering received, mothering bestowed and adult stress responses. Stress 5:259–267

    CAS  PubMed  Google Scholar 

  • Pfeifer L, Bale K, Carter CS (2001) Neonatal administration of oxytocin affects alloparental behavior in male prairie voles. Horm Behav 40:344

    Google Scholar 

  • Plotsky PM, Meaney MJ (1993) Early, postnatal experience alters hypothalamic corticotrophin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats. Mol Brain Res 18:195–200

    CAS  PubMed  Google Scholar 

  • Poindron P, Le Neindre P, Raksanyi I, Trillat G, Orgeur P (1980a) Importance of the characteristics of the young in the manifestation and establishment of maternal behavior in sheep. Reprod Nutr Dev 20:817–826

    CAS  PubMed  Google Scholar 

  • Polk DH (1992) Do breast milk derived hormones play a role in neonatal development? Early Hum Dev 29:329–331

    CAS  PubMed  Google Scholar 

  • Pollack EI, Sachs BD (1975) Male copulatory behavior and female maternal behavior in neonatally bulbectomized rats. Physiol Behav 14:337–343

    Google Scholar 

  • Pollack PF, Goda T, Colony PC, Edmond J, Thornburg W, Korc M, Koldovsky O (1987) Effects of enterally fed epidermal growth factor on the small and large intestine of the suckling rat. Regul Pept 17:121–132

    CAS  PubMed  Google Scholar 

  • Pryce CR, Feldon J (2003) Long-term neurobehavioral impact of the postnatal environments in rats: manipulations, effects and mediating mechanisms. Neurosci Biobehav Rev 27:57–71

    PubMed  Google Scholar 

  • Pryce CR, Bettschen D, Bahr NI, Feldon J (2001) Comparison of the effects of infant handling, isolation, and nonhandling on acoustic startle, prepulse inhibition, locomotion, and HPA activity in the adult rat. Behav Neurosci 115:71–83

    CAS  PubMed  Google Scholar 

  • Puccio F, Lehy T (1988) Oral administration of epidermal growth factor in suckling rats stimulates cell DNA synthesis in fundic and antral gastric mucosae as well as in intestinal mucosa and pancreas. Regul Pept 20:53–64

    CAS  PubMed  Google Scholar 

  • Ratsimamanga AR, Nigeon-Dureuil M, Rabinowicz M (1956) Presence d´hormone-type cortinique-das le lait de la vache gravide. Comptes Rendus de Societe Biologie (Paris) 150:2179–2182

    CAS  Google Scholar 

  • Rosenblatt JS (1965) The basis of synchrony in the behavioral interaction between the mother and her offspring in the laboratory rat. In: Fos BM (ed) Determinants of infant behavior, vol 3. Methuen, London, pp 6–41

    Google Scholar 

  • Rosenblatt JS (1967) Nonhormonal basis of maternal behavior in the rat. Science 156:1512–1514

    CAS  PubMed  Google Scholar 

  • Rosenblatt JS, Lehrman DS (1963) Maternal behavior in the laboratory rat. In: Rheingold HL (ed) Maternal behavior in mammals. Wiley, New York, pp 8–57

    Google Scholar 

  • Rosenblatt JS, Siegel HI, Mayer AD (1979) Progress in the study of maternal behavior in the rat: hormonal, non-hormonal, sensory, and developmental aspects. Adv Study Behav 10:225–311

    Google Scholar 

  • Rosenblatt JS, Mayer AD, Siegel HI (1985) Maternal behavior among the nonprimate mammals. In: Adler N, Pfaff D, Goy RW (eds) Handbook of behavioral neurobiology, vol 7. Plenum Press, New York, pp 229–298

    Google Scholar 

  • Rosenfeld P, Suchecki D, Levine S (1992) Multifactorial regulation of the hypothalamic-pituitary-adrenal axis during development. Neurosci Biobehav Rev 16:553–568

    CAS  PubMed  Google Scholar 

  • Russell DH, Mills KT, Talamantes FJ, Bern HA (1998) Neonatal administration of prolactin antiserum alters the developmental pattern of T- and B-lymphocytes in the thymus and spleen of BALB/c female mice. Proc Natl Acad Sci U S A 85:7404–7407

    Google Scholar 

  • Rutter M, O´Connor TG (2004) Are there biological programming effects for psychological development? Findings from a study of Romanian adoptess. Dev Psychol 40:81–94

    PubMed  Google Scholar 

  • Sapolsky RM, Krey L, McEwen BS (1984) Glococorticoid sensitive hippocampal neurons are involved in terminating the adrenocortical stress response. Proc Natl Acad Sci U S A 81:6174–6177

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sapolsky RM, Meaney MJ (1986) Maturation of the adrenocortical stress response: neuroendocrine control mechanisms and the stress hyporesponsive period. Brain Res 396:64–76

    CAS  PubMed  Google Scholar 

  • Sarda A, Nair RMG (1981) Elevated levels of LRH in human milk. J Clin Endocinol Metab 52:826–828

    CAS  Google Scholar 

  • Sawano S, Arimura A, Schally AV, Redding TW, Schapiro S (1969) Neonatal corticoid administration: effects upon adult pituitary growth hormone and hypothalamic growth hormone-releasing hormone activity. Acta Endocrinol 61:57–67

    CAS  PubMed  Google Scholar 

  • Sawchenko PE, Swanson LW (1985) Relationship of oxytocin pathways to the control of neuroendocrine and autonomic function. In: Amico JA, Robinson AG (eds) Oxytocin: clinical and laboratory studies. Elsevier Science Publishers B.V., Amsterdam, pp 87–103

    Google Scholar 

  • Schmidt MV, Enthoven L, Van Woezik JH, Levine S, De Kloet ER, Oitzl MS (2004) The dynamics of the hypothalamic-pituitary-adrenal axis during maternal deprivation. J Neuroendocrinol 16:52–57

    CAS  PubMed  Google Scholar 

  • Shah V, Shyr SW, Grosvenor CE, Crowley WR (1988) Hyperprolactinemia after neonatal prolactin (PRL) deficiency in rats: evidence for altered anterior pituitary regulation of PRL secretion. Endocrinology 182:1883–1889

    Google Scholar 

  • Shieh KR, Pan JT (1999) Stimulatory role of prolactin on the development of tuberoinfundibular dopaminergic neurons in prepubertal female rats: studies with cysteamine and somatostatin. J Neuroendocrinol 11:907–917

    CAS  PubMed  Google Scholar 

  • Shing YW, Klagsbrun M (1984) Human and bovine milk contain different sets of growth factors. Endocrinology 115:273–282

    CAS  PubMed  Google Scholar 

  • Shyr SW, Crowley WR, Grosvenor CE (1986) Effect of neonatal prolactin deficiency on prepubertal tuberoinfundibular and tuberohypophyseal dopaminergic neuronal activity. Endocrinology 119:1217–1221

    CAS  PubMed  Google Scholar 

  • Simmons KR, Moses SC, Perkins BL (1979) Prostaglandin in milk, days open, and estrus detection in dairy cows treated with prostaglandin F2 alpha. J Dairy Sci 62:1443–1448

    CAS  PubMed  Google Scholar 

  • Slebodzinski AB, Twardon J (2004) Thyroid hormones (TH) and 5′-monodeiodinase (5′-MD) activity in goat’s milk from the early, mid- and late lactation period. Acta Vet Hung 52:349–359

    CAS  PubMed  Google Scholar 

  • Slebodzinski AB, Nowak J, Gawecka H, Sechman A (1986) Thyroid hormones and insulin in milk: a comparative study. Endocrinol Exp 20:247–255

    CAS  PubMed  Google Scholar 

  • Smart JL, Tonkiss J, Massey RF (1986) A phenomenon: left-biassed asymmetrical eye-opening in artificially reared rat pups. Dev Brain Res 28:134–136

    Google Scholar 

  • Sohlström A, Carlsson C, Uvnas-Moberg K (2000) Effects of oxytocin treatment in early life on body weight and corticosterone in adult offspring from ad libitum-fed and food-restricted rats. Biol Neonate 78:33–40

    PubMed  Google Scholar 

  • Sohlström A, Olausson H, Brismar K, Uvnäs-Moberg K (2002) Oxytocin treatment during early life influences reproductive performance in ad libitum fed and food-restricted female rats. Biol Neonate 81:132–138

    PubMed  Google Scholar 

  • Spear LP, Specht SM, Kirstein CL, Kuhn CM (1989) Anterior and Posterior, but not cheek, intraoral cannulation procedures elevate serum corticosterone levels in neonatal rat pups. Dev Psychobiol 22:401–411

    CAS  PubMed  Google Scholar 

  • Stemberg W, Ridgway CG (2003) Effects of gestational stress and neonatal handling on pain, analgesia, and stress behavior of adult mice. Physiol Behav 78:375–383

    Google Scholar 

  • Strbak V (1985) The Role of maternal milk in endocrine regulation of sucklings. VEDA, Bratislava, pp 1–108

    Google Scholar 

  • Strbák V, Macho L, Skultétyová M, Michalicková J, Pohlová G (1983) Thyroid hormones in milk: physiological approach a review. Endocrinol Exp 4:219–235

    Google Scholar 

  • Sullivan EC, Hinde K, Mendoza SP, Capitanio JP (2001) Cortisol concentrations in the milk of rhesus monkey mothers are associated with confident temperament in sons, but not daughters. Dev Psychobiol 53:96–104

    Google Scholar 

  • Takeda S, Kuwabara Y, Mizuno M (1986) Concentrations and origin of oxytocin in breastmilk. Endocrinol Jan 33:821–826

    CAS  Google Scholar 

  • Tamasy V, Du J, Vallerga A, Meisami E, Timiras PS (1984) Suckling ability and maternal prolactin levels in hypothyroid rats. Horm Behav 18:457–464

    CAS  PubMed  Google Scholar 

  • Tamasy V, Meisami E, Du J-Z, Timiras PS (1986) Exploratory behavior, learning ability, and thyroid hormonal responses to stress in female rats rehabilitating from postnatal hypothyroidism. Dev Psychobiol 19:537–553

    CAS  PubMed  Google Scholar 

  • Teicher MH, Andersen SL, Polcari A, Anderson CM, Navalta CP, Kim DM (2003) The neurobiological consequences of early stress and childhood maltreatment. Neurosci Biobehav Rev 27:33–44

    PubMed  Google Scholar 

  • Teicher MH, Tomoda A, Susan L, Andersen SL (2006) Neurobiological consequences of early stress and childhood maltreatment: are results from human and animal studies comparable? Ann N Y Acad Sci 1071:313–323

    PubMed  Google Scholar 

  • Ternore A, Oberkotter LV, Koldovsky O, Parks JS, Vanderberg CM (1981) Thyrotropin in human breast milk. Horm Res 14:193–200

    Google Scholar 

  • Tucker HA, Schwalm JW (1977) Glucocorticoids mammary tissue and milk. J Anim Sci 46:627–634

    Google Scholar 

  • Uvnas-Moberg K, Alster P, Petersson M, Sohlstro¨m A, Bjorkstrand E (1998) Postnatal oxytocin injections cause sustained weight gain and increased nociceptive thresholds in male and female rats. Pediatr Rev 43:1–5

    Google Scholar 

  • Valtonen M, Kangas AP, Voutilainen M, Eriksson L (2003) Diurnal rhythm of melatonin in young calves and intake of melatonin in milk. Anim Sci 77:149–154

    CAS  Google Scholar 

  • van Ijzendoornd MH (1992) Intergenerational transmission of parenting: a review of studies in nonclinical populations. Dev Rev 12:76–99

    Google Scholar 

  • Viau V, Sharmas S, Plotsky PM, Meaney MJ (1993) The hypothalamic-pituitary adrenal response to stress in handled and non-handled rats: differences in stress-induced plasma ACTH secretion are not dependent upon increased corticosterone levels. J Neurosci 13:1097–1105

    CAS  PubMed  Google Scholar 

  • Vigouroux E, Rastoqui N, Fenerole JM (1980) Estimation of hormonal and nonhormonal iodine uptake from maternal milk in suckling rats. Acta Endocrinol 93:332–338

    CAS  PubMed  Google Scholar 

  • Vinici JL, Buonomo FC, Veenhuizen JJ, Miller MA, Cleammons DR, Collier RJ (1991) Nutrient balance and stage of lactation affect responses of insulin, insuli-like growth factors I and II, and ministration in dairy cows. J Nutr 121:1656–1664

    Google Scholar 

  • Weinberg J, Smotherman WP, Levine S (1978) Early handling effects on neophobia andconditioned taste aversion. Physiol Behav 5:589–596

    Google Scholar 

  • Weininger O (1954) Physiological damage under emotional stress as a function of early experience. Science 119:285–286

    CAS  PubMed  Google Scholar 

  • Weiss EL, Longhurst JG, Mazure CM (1999) Childhood sexual abuse as a risk factor for depression in women: psychosocial and neurobiological correlates. Am J Psychiatry 156:816–828

    CAS  PubMed  Google Scholar 

  • Werner S, Widstrom AM, Wahlberg V, Eneroth P, Winberg J (1982) Immunoreactive calcitonin in maternal milk and serum in relation to prolactin and neurotensin. Early Hum Dev 6:77–82

    CAS  PubMed  Google Scholar 

  • Werner H, Amarant T, Fridkin M, Koch Y (1986) Growth hormone releasing factor-like immunoreactivity in human milk. Biochem Biophys Res Commun 135:1084–1089

    CAS  PubMed  Google Scholar 

  • Werner H, Katz P, Fridkin M, Koch Y, Levine S (1988) Growth hormone releasing factor and somatostatin concentrations in the milk of lactating women. Eur J Pediatr 147:252–256

    CAS  PubMed  Google Scholar 

  • Wilson DA, Willner J, Kurz EM, Nadel L (1986) Early handling increases hippocampal long-term potentiation in young rats. Behav Brain Res 21:223–227

    CAS  PubMed  Google Scholar 

  • Witt DM (1997) Mechanisms of oxytocin-mediated sociosexual behavior. Ann N Y Acad Sci 807:287–301

    CAS  PubMed  Google Scholar 

  • Wolford ST, Argoudelis CJ (1979) Measurement of strogen in cow’s milk, human milk, and dietary products. J Dairy Sci 62:1458–1463

    CAS  PubMed  Google Scholar 

  • Zaied AA, Bierschwal CJ, Elmore RG, Youngquist RS, Sharp AJ, Garverick HA (1979) Concentrations of progesterone in milk as a monitor of early pregnancy diagnosis in dairy cows. Theriogenology 12:3–11

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The author thanks Prof. Alison S. Fleming for commenting and editing this work and Francisco Corona Land for his generous help in the preparation of the table and the references.

This study was supported by a CONACYT-Mon co grant to Angel I. Melo (CB-2010-01-156413).

Conflict of Interest

The authors declare no conflicts of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Angel I. Melo .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer Science+Business Media New York

About this chapter

Cite this chapter

Melo, A. (2015). Role of Sensory, Social, and Hormonal Signals from the Mother on the Development of Offspring. In: Antonelli, M. (eds) Perinatal Programming of Neurodevelopment. Advances in Neurobiology, vol 10. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-1372-5_11

Download citation

Publish with us

Policies and ethics