Skip to main content

Perinatal Positive and Negative Influences on the Early Neurobehavioral Reflex and Motor Development

  • Chapter
  • First Online:
Perinatal Programming of Neurodevelopment

Abstract

Early life events are critical in the development of the central nervous system. Injuries in this period can cause severe damage with permanent disabilities. The early changes following a perinatal lesion have prognostic significance. The nervous system in young age has a potential for plasticity and regeneration, which can prevent the negative effects of neuronal damage, and the most important objective of rehabilitation is to enhance this inner potential of the developing brain. Experimental examination of the environmental factors affecting this regeneration and remodeling process is very important. Endogenous factors, such as neurotrophic factors, which play a role in neurogenesis, migration, and differentiation of neurons, and development of neuronal circuits, are also in the center of interest. Most studies concerning the effect of positive or negative perinatal treatments focus mainly on long-term effects, and most examinations are carried out on adult animals following perinatal injuries. Less data are available on short-term effects and early neurobehavioral changes. In the past several years, we have shown how different (positive or negative) perinatal events affect the early neuronal development. Applying different tests widely used for behavioral testing, we have established a standardized testing method. This includes measuring parameters of somatic growth and facial development, appearance of basic neurological reflexes and also reflex performance, more complex motor coordination tests, and open-field and novelty-seeking tests. In the present chapter, we summarize data on early neurobehavioral development of newborn rats subjected to negative (perinatal asphyxia, hypoxia, excitotoxic injury, stress) and positive (enriched environment, neurotrophic factor treatment) stimuli during early postnatal life.

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

  • Allais A, Burel D, Isaac ER, Gray SL, Basille M, Ravni A, Sherwood NM, Vaudry H, Gonzalez BJ (2007) Altered cerebellar development in mice lacking pituitary adenylate cyclase-activating polypeptide. Eur J Neurosci 25(9):2604–2618

    Article  PubMed  Google Scholar 

  • Allende-Castro C, Espina-Marchant P, Bustamante D, Rojas-Mancilla E, Neira T, Gutierrez-Hernandez MA, Esmar D, Valdes JL, Morales P, Gebicke-Haerter PJ, Herrera-Marschitz M (2012) Further studies on the hypothesis of PARP-1 inhibition as a strategy for lessening the long-term effects produced by perinatal asphyxia: effects of nicotinamide and theophylline on PARP-1 activity in brain and peripheral tissue: nicotinamide and theophylline on PARP-1 activity. Neurotox Res 22(1):79–90. doi: 10.1007/s12640-012-9310-2

    Article  CAS  PubMed  Google Scholar 

  • Altman J, Sudarshan K (1975) Postnatal development of locomotion in the laboratory rat. Anim Behav 23:896–920

    Article  CAS  PubMed  Google Scholar 

  • Andreazzi AE, Grassiolli S, Marangon PB, Martins AG, de Oliveira JC, Torrezan R, Gravena C, Garcia RM, Mathias PC (2011) Impaired sympathoadrenal axis function contributes to enhanced insulin secretion in prediabetic obese rats. Exp Diabetes Res 2011:947917. doi: 10.1155/2011/947917.

    Article  PubMed Central  PubMed  Google Scholar 

  • Atlasz T, Szabadfi K, Reglodi D, Kiss P, Tamas A, Toth G, Molnar A, Szabo K, Gabriel R (2009) Effects of pituitary adenylate cyclase activating polypeptide (PACAP1-38) and its fragments on retinal degeneration induced by neonatal MSG treatment. Ann NY Acad Sci 1163:348–352

    Article  CAS  PubMed  Google Scholar 

  • Archer T, Schroder N, Fredriksson A (2003) Neurobehavioural deficits following postnatal iron overload: II Instrumental learning performance. Neurotox Res 5:77–94

    Article  CAS  PubMed  Google Scholar 

  • Babai N, Atlasz T, Tamás A, Reglődi D, Kiss P, Gábriel R (2005) Degree of damage compensation by various PACAP treatments in monosodium glutamate-induced retina degeneration. Neurotox Res 8:227–233

    Article  CAS  PubMed  Google Scholar 

  • Baier CJ, Katunar MR, Adrover E, Pallarés ME, Antonelli MC (2012) Gestational restraint stress and the developing dopaminergic system: an overview. Neurotox Res 22(1):16–32. doi: 10.1007/s12640-011-9305-4

    Article  CAS  PubMed  Google Scholar 

  • Basille-Dugay M, Vaudry H, Fournier A, Gonzalez B, Vaudry D (2013) Activation of pac1 receptors in rat cerebellar granule cells stimulates both calcium mobilization from intracellular stores and calcium influx through n-type calcium channels. Front Endocrinol (Lausanne) 4:56. doi: 10.3389/fendo.2013.00056

    CAS  Google Scholar 

  • Beas-Zárate C, Sánchez-Ruíz MY, Ureña-Guerrero ME, Feria-Velasco A (1998) Effect of neonatal exposure to monosodium L-glutamate on regional GABA release during postnatal development. Neurochem Int 33(3):217–232

    Article  PubMed  Google Scholar 

  • Beas-Zarate C, Perez-Vega MI, Gonzalez-Burgos I (2002) Neonatal exposure to monosodium L-glutamate induces loss of neurons and cytoarchitectural alterations in hippocampal CA1 pyramidal neurons of adult rats. Brain Res 952:275–281

    Article  CAS  PubMed  Google Scholar 

  • Blutstein T, Castello MA, Viechweg SS, Hadjimarkou MM, McQuail JA, Holder M, Thompson LP, Mong JA (2013) Differential responses of hippocampal neurons and astrocytes to nicotine and hypoxia in the fetal Guinea pig. Neurotox Res 24(1):80–93. doi: 10.1007/s12640-012-9363-2

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bourgault S, Vaudry D, Dejda A, Doan ND, Vaudry H, Fournier A (2009) Pituitary adenylate cyclase-activating polypeptide: focus on structure-activity relationships of a neuroprotective peptide. Curr Med Chem 16(33):4462–4480

    Article  CAS  PubMed  Google Scholar 

  • Bobrovskaya L, Maniam J, Ong LK, Dunkley PR, Morris MJ (2013) Early life stress and post-weaning high fat diet alter tyrosine hydroxylase regulation and AT1 receptor expression in the adrenal gland in a sex dependent manner. Neurochem Res 38(4):826–833. doi: 10.1007/s11064-013-0985-4

    Article  CAS  PubMed  Google Scholar 

  • Bustamante D, Morales P, Pereyra JT, Goiny M, Herrera-Marschitz M (2007) Nicotinamide prevents the effect of perinatal asphyxia on dopamine release evaluated with in vivo microdialysis 3 months after birth. Exp Brain Res 177:358–369

    Article  CAS  PubMed  Google Scholar 

  • Chaparro-Huerta V, Rivera-Cervantes MC, Torres-Mendoza BM, Beas-Zarate C (2002) Neuronal death and tumor necrosis factor-α response to glutamate-induced excitotoxicity in the cerebral cortex of neonatal rats. Neurosci Lett 333:95–98

    Article  CAS  PubMed  Google Scholar 

  • Cheng J, Fujimura M, Zhao W, Wang W (2013) Neurobehavioral effects, c-Fos/Jun expression and tissue distribution in rat offspring prenatally co-exposed to mehg and PFOA: PFOA impairs Hg retention. Chemosphere 91(6):758–764. doi: 10.1016/j.chemosphere.2013.02.016

    Article  CAS  PubMed  Google Scholar 

  • De Jongh R, Geyer MA, Olivier B, Groenink L (2005) The effects of sex and neonatal maternal separation on fear-potentiated and light-enhanced startle. Behav Brain Res 161(2):190–196

    Article  PubMed  Google Scholar 

  • de Kloet ER (2008) About stress hormones and resilience to psychopathology. J Neuroendocrinol 20(6):885–892. doi: 10.1111/j.1365 − 2826.2008.01707.x

    Article  PubMed  Google Scholar 

  • Dunn AJ, Webster EL (1985) Neonatal treatment with monosodium glutamate does not alter grooming behavior induced by novelty or adrenocorticotropic hormone. Behav Neur Biol 44:80–89

    Article  CAS  Google Scholar 

  • Ellenbroek BA, Derks N, Park HJ (2005) Early maternal deprivation retards neurodevelopment in Wistar rats. Stress 8(4):247–257

    Article  PubMed  Google Scholar 

  • Falluel-Morel A, Tascau LI, Sokolowski K, Brabet P, DiCicco-Bloom E (2008) Granule cell survival is deficient in PAC1-/- mutant cerebellum. J Mol Neurosci 36(1–3):38–44

    Article  CAS  PubMed  Google Scholar 

  • Farkas J, Reglodi D, Gaszner B, Szogyi D, Horvath G, Lubics A, Tamas A, Falko F, Besirevic D, Kiss P (2009) Effects of maternal separation on the neurobehavioral development of newborn Wistar rats. Brain Res Bull 79:208–214

    Article  PubMed  Google Scholar 

  • Galeano P, Blanco Calvo E, Madureira de OD, Cuenya L, Kamenetzky GV, Mustaca AE, Barreto GE, Giraldez-Alvarez LD, Milei J, Capani F (2011) Long-lasting effects of perinatal asphyxia on exploration, memory and incentive downshift. Int J Dev Neurosci 29(6):609–619. doi: 10.1016/j.ijdevneu.2011.05.002

    Article  PubMed  Google Scholar 

  • Gaszner B, Kormos V, Kozicz T, Hashimoto H, Reglodi D, Helyes Z (2012) The behavioral phenotype of pituitary adenylate cyclase activating polypeptide deficient mice in anxiety and depression tests is accompanied by blunted c-Fos expression in the bed nucleus of the stria terminalis, central projecting Edinger Westphal nucleus, ventral lateral septum and dorsal raphe nucleus. Neuroscience 202:283–299

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez-Burgos I, Perez-Vega MI, Beas-Zarate C (2001) Neonatal exposure to monosodium glutamate induces cell death and dendritic hypotrophy in rat prefrontocortical pyramidal neurons. Neurosci Lett 297:69–72

    Article  CAS  PubMed  Google Scholar 

  • Gilbert ME, Llorens J (1993) Delay in the development of amygdala kindling following treatment with 3,3’-iminodipropionitrile. Neurotoxicol Teratol 15(4):243–250

    Article  CAS  PubMed  Google Scholar 

  • Grimaldi M, Romer I, de Apodaca MT, Iturbe L, Catania ID, González J, Kolliker-Fres R, Barreto G, Capani F (2012) Early changes in the synapses of the neostriatum induced by perinatal asphyxia. Nutr Neurosci 15(3):103–110. doi: 10.1179/1476830511Y.0000000026

    Article  CAS  PubMed  Google Scholar 

  • Grissom EM, Hawley WR, Bromley-Dulfano SS, Marino SE, Stathopoulos NG, Dohanich GP (2012) Learning strategy is influenced by trait anxiety and early rearing conditions in prepubertal male, but not prepubertal female rats. Neurobiol Learn Mem 98(2):174–181. doi: 10.1016/j.nlm.2012.06.001

    Article  PubMed  Google Scholar 

  • Harmar AJ, Fahrenkrug J, Gozes I, Laburthe M, May V, Pisegna JR, Vaudry D, Vaudry H, Waschek JA, Said SI (2012) Pharmacology and functions of receptors for vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide: IUPHAR review 1. Br J Pharmacol 166(1):4–17. doi: 10.1111/j.1476-5381.2012.01871.x

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hebb DO (1947) The effects of early experience on problem solving at maturity. Am Psychol 2:306–307

    Google Scholar 

  • Hill JM, Gozes I, Hill JL, Fridkin M, Brenneman DE (1991) Vasoactive intestinal peptide antagonist retards the development of neonatal behaviors in the rat. Peptides 12:187–192

    Article  CAS  PubMed  Google Scholar 

  • Holighaus Y, Weihe E, Eiden LE (2012) STC1 induction by PACAP is mediated through cAMP and ERK1/2 but not PKA in cultured cortical neurons. J Mol Neurosci 46(1):75–87

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hori M, Nakamachi T, Rakwal R, Shibato J, Ogawa T, Aiuchi T, Tsuruyama T, Tamaki K, Shioda S (2012) Transcriptomics and proteomics analyses of the PACAP38 influenced ischemic brain in permanent middle cerebral artery occlusion model mice. J Neuroinflammation 9:256. doi: 10.1186/1742-2094-9-256. Erratum in J Neuroinflammation 2013 10:18

    Google Scholar 

  • Ishihama T, Ago Y, Shintani N, Hashimoto H, Baba A, Takuma K, Matsuda T (2010) Environmental factors during early developmental period influence psychobehavioral abnormalities in adult PACAP-deficient mice. Behav Brain Res 209(2):274–280

    Article  CAS  PubMed  Google Scholar 

  • Jain V, Baitharu I, Prasad D, Ilavazhagan G (2013) Enriched environment prevents hypobaric hypoxia induced memory impairment and neurodegeneration: role of BDNF/PI3K/GSK3β pathway coupled with CREB activation. PLoS One 8(5):e62235

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Johnson EM, Traver KL, Hoffman SW, Harrison CR, Herman JP (2013) Environmental enrichment protects against functional deficits caused by traumatic brain injury. Front Behav Neurosci 7:44

    Article  PubMed Central  PubMed  Google Scholar 

  • Kambe Y, Miyata A (2012) Role of mitochondrial activation in PACAP dependent neurite outgrowth. J Mol Neurosci 48(3):550–557

    Article  CAS  PubMed  Google Scholar 

  • Karlen-Amarante M, da Cunha NV, de Andrade O, de Souza HC, Martins-Pinge MC (2012) Altered baroreflex and autonomic modulation in monosodium glutamate-induced hyperadipose rats. Metabolism 61(10):1435–1442

    Article  CAS  PubMed  Google Scholar 

  • Kiss P, Tamás A, Lubics A, Szalai M, Szalontay L, Lengvári I, Reglődi D (2005) Development of neurological reflexes and motor coordination in rats neonatally treated with monosodium glutamate. Neurotox Res 8:235–244

    Article  CAS  PubMed  Google Scholar 

  • Kiss P, Tamás A, Lubics A, Lengvári I, Szalai M, Hauser D, Horváth Z, Rácz B, Gábriel R, Babai N, Tóth G, Reglődi D (2006) Effects of systemic PACAP treatment in monosodium glutamate-induced behavioral changes and retinal degeneration. Ann NY Acad Sci 1070:365–370

    Article  CAS  PubMed  Google Scholar 

  • Kiss P, Szogyi D, Reglodi D, Horvath G, Farkas J, Lubics A, Tamas A, Atlasz T, Szabadfi K, Babai N, Gabriel R, Koppan M (2009) Effects of perinatal asphyxia on the neurobehavioral and retinal development of newborn rats. Brain Res 1255:42–50

    Article  CAS  PubMed  Google Scholar 

  • Kiss P, Atlasz T, Szabadfi K, Horvath G, Griecs M, Farkas J, Matkovits A, Toth G, Lubics A, Tamas A, Gabriel R, Reglodi D (2011) Comparison between PACAP- and enriched environment-induced retinal protection in MSG-treated newborn rats. Neurosci Lett 487:400–405

    Article  CAS  PubMed  Google Scholar 

  • Klingberg H, Brankack J, Klingberg F (1987) Long-term effects on behavior after postnatal treatment with monosodium-L-glutamate. Biomed Biochim Acta 46:705–711

    CAS  PubMed  Google Scholar 

  • Kubo T, Kohira R, Okano T, Ishikawa K (1993) Neonatal glutamate can destroy the hippocampal CA1 structure and impair discrimination learning in rats. Brain Res 616:311–314

    Article  CAS  PubMed  Google Scholar 

  • Lee MY, Yu JH, Kim JY, Seo JH, Park ES, Kim CH, Kim H, Cho SR (2013) Alteration of synaptic activity-regulating genes underlying functional improvement by long-term exposure to an enriched environment in the adult brain. Neurorehabil Neural Repair 27(6):561–574

    Article  PubMed  Google Scholar 

  • Leussis MP, Freund N, Brenhouse HC, Thompson BS, Andersen SL (2012) Depressive-like behavior in adolescents after maternal separation: sex differences, controllability, and GABA. Dev Neurosci 34(2–3):210–217

    Article  CAS  PubMed  Google Scholar 

  • Li M, Xue X, Shao S, Shao F, Wang W (2013) Cognitive, emotional and neurochemical effects of repeated maternal separation in adolescent rats. Brain Res 1518:82–90.

    Article  CAS  PubMed  Google Scholar 

  • Lubics A, Reglődi D, Tamás A, Kiss P, Szalai M, Szalontay L, Lengvári I (2005) Neurological reflexes and early motor behavior in rats subjected to neonatal hypoxic/ischemic injury. Behav Brain Res 157:157–165

    Article  PubMed  Google Scholar 

  • Marco EM, Macrì S, Laviola G (2011) Critical age windows for neurodevelopmental psychiatric disorders: evidence from animal models. Neurotox Res 19(2):286–307. doi:10.1007/s12640-010-9205-z

    Article  PubMed  Google Scholar 

  • Morales P, Fiedler JL, Andres S, Berrios C, Huaiquin P, Bustamante D, Cardenas S, Parra E, Herrera-Marschitz M (2008) Plasticity of hippocampus following perinatal asphyxia: effects on postnatal apoptosis and neurogenesis. J Neurosci Res 86:2650–2662

    Article  CAS  PubMed  Google Scholar 

  • Nasiraei-Moghadam S, Sherafat MA, Safari MS, Moradi F, Ahmadiani A, Dargahi L (2013) Reversal of prenatal morphine exposure-induced memory deficit in male but not female rats. J Mol Neurosci 50(1):58–69. doi:10.1007/s12031-012-9860-z

    Article  CAS  PubMed  Google Scholar 

  • Nakamachi T, Farkas J, Watanabe J, Ohtaki H, Dohi K, Arata S, Shioda S (2011) Role of PACAP in neural stem/progenitor cell and astrocyte-from neural development to neural repair. Curr Pharm Des 17(10):973–984

    Article  CAS  PubMed  Google Scholar 

  • Nakamachi T, Tsuchida M, Kagami N, Yofu S, Wada Y, Hori M, Tsuchikawa D, Yoshikawa A, Imai N, Nakamura K, Arata S, Shioda S (2012) IL-6 and PACAP receptor expression and localization after global brain ischemia in mice. J Mol Neurosci 48(3):518–525

    Article  CAS  PubMed  Google Scholar 

  • Reglodi D, Kiss P, Lubics A, Tamas A (2011) Review of the protective effects of PACAP in models of neurodegenerative diseases in vitro and in vivo. Curr Pharm Des 17:962–972

    Article  CAS  PubMed  Google Scholar 

  • Reglodi D, Kiss P, Szabadfi K, Atlasz T, Gabriel R, Horvath G, Szakaly P, Sandor B, Lubics A, Laszlo E, Farkas J, Matkovits A, Brubel R, Hashimoto H, Ferencz A, Vincze A, Helyes Z, Welke L, Lakatos A, Tamas A (2012) PACAP is an endogenous protective factor - insights from PACAP deficient mice. J Mol Neurosci 48:482–492

    Article  CAS  PubMed  Google Scholar 

  • Rousset CI, Kassem J, Aubert A, Planchenault D, Gressens P, Chalon S, Belzung C, Saliba E (2013) Maternal exposure to lipopolysaccharide leads to transient motor dysfunction in neonatal rats. Dev Neurosci 35(2–3):172–181. doi:10.1159/000346579 (Epub 2013 Feb 27)

    Article  CAS  PubMed  Google Scholar 

  • Saraceno GE, Castilla R, Barreto GE, Gonzalez J, Kölliker-Frers RA, Capani F (2012) Hippocampal dendritic spines modifications induced by perinatal asphyxia. Neural Plast 2012:873532. doi: 10.1155/2012/873532.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Schuck PF, Ferreira Gda C, Viegas CM, Tonin AM, Busanello EN, Pettenuzzo LF, Netto CA, Wajner M (2009) Chronic early postnatal administration of ethylmalonic acid to rats causes behavioral deficit. Behav Brain Res 197(2):364–370. doi: 10.1016/j.bbr.2008.09.031

    Article  CAS  PubMed  Google Scholar 

  • Slotten HA, Kalinichev M, Hagan JJ, Marsden CA, Fone KC (2006) Long-lasting changes in behavioural and neuroendocrine indices in the rat following neonatal maternal separation: gender-dependent effects. Brain Res 1097(1):123–132

    Article  CAS  PubMed  Google Scholar 

  • Simola N, Bustamante D, Pinna A, Pontis S, Morales P, Morelli M, Herrera-Marschitz M (2008) Acute perinatal asphyxia impairs non-spatial memory and alters motor coordination in adult male rats. Exp Brain Res 185:595–601

    Article  PubMed  Google Scholar 

  • Skultétyová I, Tokarev D, Jezová D (1998) Stress-induced increase in blood-brain barrier permeability in control and monosodium glutamate-treated rats. Brain Res Bull 45(2):175–178

    Article  PubMed  Google Scholar 

  • Smart JL, Dobbing J (1971a) Vulnerability of developing brain. II. Effects of early nutritional deprivation on reflex ontogeny and development on behavior in the rat. Brain Res 28:85–95

    Article  CAS  PubMed  Google Scholar 

  • Smart JL, Dobbing J (1971b) Vulnerability of developing brain. VI. Relative effects of foetal and early postnatal undernutrition on reflex ontogeny and development of behavior in the rat. Brain Res 33:303–314

    Article  CAS  PubMed  Google Scholar 

  • Souza SK, Martins TL, Ferreira GD, Vinagre AS, Silva RS, Frizzo ME (2013) Metabolic effects of perinatal asphyxia in the rat cerebral cortex. Metab Brain Dis 28(1):25–32. doi:10.1007/s11011-012-9367-x

    Article  CAS  PubMed  Google Scholar 

  • Swinny JD, O’Farrell E, Bingham BC, Piel DA, Valentino RJ, Beck SG (2010) Neonatal rearing conditions distinctly shape locus coeruleus neuronal activity, dendritic arborization, and sensitivity to corticotrophin-releasing factor. Int J Neuropsychopharmacol 13(4):515–525

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Szabadfi K, Atlasz T, Horvath G, Kiss P, Hamza L, Farkas J, Tamas A, Lubics A, Gabriel R, Reglodi D (2009) Early postnatal enriched environment decreases retinal degeneration induced by monosodium glutamate treatment. Brain Res 1259:107–112

    Article  CAS  PubMed  Google Scholar 

  • Tsuchikawa D, Nakamachi T, Tsuchida M, Wada Y, Hori M, Farkas J, Yoshikawa A, Kagami N, Imai N, Shintani N, Hashimoto H, Atsumi T, Shioda S (2012) Neuroprotective effect of endogenous pituitary adenylate cyclase-activating polypeptide on spinal cord injury. J Mol Neurosci 48(3):508–517

    Article  CAS  PubMed  Google Scholar 

  • Van de Berg WD, Blockland A, Cuello AC, Schmitz C, Vreuls W, Steinbusch HW, Blanco CE (2000) Perinatal asphyxia results in changes in presynaptic bouton number in striatum and cerebral cortex - a stereological and behavioral analysis. J Chem Neuroanat 20:71–82

    Article  PubMed  Google Scholar 

  • Van de Berg WD, Kwaijtaal M, de Louw AJ, Lissone NP, Schmitz C, Faull RL, Blokland A, Blanco CE, Steinbusch HW (2003) Impact of perinatal asphyxia on the GABAergic and locomotor system. Neuroscience 117:83–96

    Article  PubMed  Google Scholar 

  • Vannucci RC, Rossini A, Towfight J, Vannucci SJ (1997) Measuring the accentuation of the brain damage that arises from perinatal cerebral hypoxia-ischemia. Biol Neonate 72:187–191

    Article  CAS  PubMed  Google Scholar 

  • Vaudry D, Falluel-Morel A, Bourgault S, Basille M, Burel D, Wurtz O, Fournier A, Chow BK, Hashimoto H, Galas L, Vaudry H (2009) Pituitary adenylate cyclase-activating polypeptide and its receptors: 20 years after the discovery. Pharmacol Rev 61:283–357

    Article  CAS  PubMed  Google Scholar 

  • Vivinetto AL, Suarez MM, Rivarola MA (2013) Neurobiological effects of neonatal maternal separation and post-weaning environmental enrichment. Behav Brain Res 240:110–118

    Article  PubMed  Google Scholar 

  • Waschek J (2013) VIP and PACAP: neuropeptide modulators of CNS inflammation, injury, and repair. Br J Pharmacol 169(3):512–523. doi:10.1111/bph.12181

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wigger A, Neumann ID (1999) Periodic maternal deprivation induces gender-dependent alterations in behavioral and neuroendocrine responses to emotional stress in adult rats. Physiol Behav 66(2):293–302

    Article  CAS  PubMed  Google Scholar 

  • Williams AN, Woessner KM (2009) Monosodium glutamate ’allergy’: menace or myth? Clin Exp Allergy 39(5):640–646. doi:10.1111/j.1365 − 2222.2009.03221.x

    Article  CAS  PubMed  Google Scholar 

  • Wixey JA, Reinebrant HE, Buller KM (2011) Inhibition of neuroinflammation prevents injury to the serotonergic network after hypoxia-ischemia in the immature rat brain. J Neuropathol Exp Neurol 70(1):23–35. doi:10.1097/NEN.0b013e3182020b7b.

    Article  CAS  PubMed  Google Scholar 

  • Yan Y, Zhou X, Pan Z, Ma J, Waschek JA, DiCicco-Bloom E (2013) Pro- and anti-mitogenic actions of pituitary adenylate cyclase-activating polypeptide in developing cerebral cortex: potential mediation by developmental switch of PAC1 receptor mRNA isoforms. J Neurosci 33(9):3865–3878

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang L, Qu Y, Tang B, Zhao F, Xiong T, Ferriero D, Mu D (2012) Integrin β8 signaling in neonatal hypoxic-ischemic brain injury. Neurotox Res 22(4):280–291

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was supported by OTKA K104984, TAMOP (4.2.1.B-10/2/KONV-2010 − 002, 4.2.2.B-10/1 − 2010 − 0029, 4.2.2.A-11/1/KONV-2012 − 0024), Arimura Foundation, PTE-MTA “Lendület” Program.

Conflict of Interest

The authors declare no conflicts of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gabor Horvath MD .

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

Horvath, G. et al. (2015). Perinatal Positive and Negative Influences on the Early Neurobehavioral Reflex and Motor Development. 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_8

Download citation

Publish with us

Policies and ethics