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Published in: Environmental Health and Preventive Medicine 1/2021

01-12-2021 | Insulins | Research article

The mechanism of enriched environment repairing the learning and memory impairment in offspring of prenatal stress by regulating the expression of activity-regulated cytoskeletal-associated and insulin-like growth factor-2 in hippocampus

Authors: Su-zhen Guan, You-juan Fu, Feng Zhao, Hong-ya Liu, Xiao-hui Chen, Fa-qiu Qi, Zhi-hong Liu, Tzi Bun Ng

Published in: Environmental Health and Preventive Medicine | Issue 1/2021

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Abstract

Background

Prenatal stress can cause neurobiological and behavioral defects in offspring; environmental factors play a crucial role in regulating the development of brain and behavioral; this study was designed to test and verify whether an enriched environment can repair learning and memory impairment in offspring rats induced by prenatal stress and to explore its mechanism involving the expression of insulin-like growth factor-2 (IGF-2) and activity-regulated cytoskeletal-associated protein (Arc) in the hippocampus of the offspring.

Methods

Rats were selected to establish a chronic unpredictable mild stress (CUMS) model during pregnancy. Offspring were weaned on 21st day and housed under either standard or an enriched environment. The learning and memory ability were tested using Morris water maze and Y-maze. The expression of IGF-2 and Arc mRNA and protein were respectively measured by using RT-PCR and Western blotting.

Results

There was an elevation in the plasma corticosterone level of rat model of maternal chronic stress during pregnancy. Maternal stress’s offspring exposed to an enriched environment could decrease their plasma corticosterone level and improve their weight. The offspring of maternal stress during pregnancy exhibited abnormalities in Morris water maze and Y-maze, which were improved in an enriched environment. The expression of IGF-2, Arc mRNA, and protein in offspring of maternal stress during pregnancy was boosted and some relationships existed between these parameters after being exposed enriched environment.

Conclusions

The learning and memory impairment in offspring of prenatal stress can be rectified by the enriched environment, the mechanism of which is related to the decreasing plasma corticosterone and increasing hippocampal IGF-2 and Arc of offspring rats following maternal chronic stress during pregnancy.
Literature
1.
go back to reference Hantsoo L, Kornfield S, Anguera MC, Epperson CN. Inflammation: a proposed intermediary between maternal stress and offspring neuropsychiatric risk. Biol Psychiatry. 2019;85:97–106.PubMedCrossRef Hantsoo L, Kornfield S, Anguera MC, Epperson CN. Inflammation: a proposed intermediary between maternal stress and offspring neuropsychiatric risk. Biol Psychiatry. 2019;85:97–106.PubMedCrossRef
2.
go back to reference Van den Bergh B, van den Heuvel MI, Lahti M, et al. Prenatal developmental origins of behavior and mental health: The influence of maternal stress in pregnancy. Neurosci Biobehav Rev. 2020;117:26-64. Van den Bergh B, van den Heuvel MI, Lahti M, et al. Prenatal developmental origins of behavior and mental health: The influence of maternal stress in pregnancy. Neurosci Biobehav Rev. 2020;117:26-64.
3.
go back to reference Londono TA, Diaz SA, Ross DA, Stevens HE. Effects of maternal prenatal stress: mechanisms, implications, and novel therapeutic interventions. Biol Psychiatry. 2016;80:e85–7.CrossRef Londono TA, Diaz SA, Ross DA, Stevens HE. Effects of maternal prenatal stress: mechanisms, implications, and novel therapeutic interventions. Biol Psychiatry. 2016;80:e85–7.CrossRef
4.
go back to reference Maccari S, Polese D, Reynaert ML, Amici T, Morley-Fletcher S, Fagioli F. Early-life experiences and the development of adult diseases with a focus on mental illness: the human birth theory. Neuroscience. 2017;342:232–51.PubMedCrossRef Maccari S, Polese D, Reynaert ML, Amici T, Morley-Fletcher S, Fagioli F. Early-life experiences and the development of adult diseases with a focus on mental illness: the human birth theory. Neuroscience. 2017;342:232–51.PubMedCrossRef
5.
go back to reference Simcock G, Elgbeili G, Laplante DP, Kildea S, Cobham V, Stapleton H, et al. The effects of prenatal maternal stress on early temperament: the 2011 queensland flood study. J Dev Behav Pediatr. 2017;38:310–21.PubMedCrossRef Simcock G, Elgbeili G, Laplante DP, Kildea S, Cobham V, Stapleton H, et al. The effects of prenatal maternal stress on early temperament: the 2011 queensland flood study. J Dev Behav Pediatr. 2017;38:310–21.PubMedCrossRef
6.
go back to reference Karam SM, Barros AJ, Matijasevich A, Dos SI, Anselmi L, Barros F, et al. Intellectual disability in a birth cohort: prevalence, etiology, and determinants at the age of 4 years. Public Health Genom. 2016;19:290–7.CrossRef Karam SM, Barros AJ, Matijasevich A, Dos SI, Anselmi L, Barros F, et al. Intellectual disability in a birth cohort: prevalence, etiology, and determinants at the age of 4 years. Public Health Genom. 2016;19:290–7.CrossRef
7.
go back to reference Kim DR, Bale TL, Epperson CN. Prenatal programming of mental illness: current understanding of relationship and mechanisms. Curr Psychiatry Rep. 2015;17:5.PubMedPubMedCentralCrossRef Kim DR, Bale TL, Epperson CN. Prenatal programming of mental illness: current understanding of relationship and mechanisms. Curr Psychiatry Rep. 2015;17:5.PubMedPubMedCentralCrossRef
8.
go back to reference Meyer JD, O'Campo P, Warren N, Muntaner C. Association of birthweight with maternal trajectories of effort-reward imbalance and demand-control across pregnancy. J Occup Environ Med. 2017;59:169–76.PubMedCrossRef Meyer JD, O'Campo P, Warren N, Muntaner C. Association of birthweight with maternal trajectories of effort-reward imbalance and demand-control across pregnancy. J Occup Environ Med. 2017;59:169–76.PubMedCrossRef
9.
go back to reference Maxwell SD, Fineberg AM, Drabick DA, Murphy SK, Ellman LM. Maternal prenatal stress and other developmental risk factors for adolescent depression: spotlight on sex differences. J Abnorm Child Psychol. 2018;46:381–97.PubMedPubMedCentralCrossRef Maxwell SD, Fineberg AM, Drabick DA, Murphy SK, Ellman LM. Maternal prenatal stress and other developmental risk factors for adolescent depression: spotlight on sex differences. J Abnorm Child Psychol. 2018;46:381–97.PubMedPubMedCentralCrossRef
10.
11.
go back to reference Zijlmans MA, Korpela K, Riksen-Walraven JM, de Vos WM, de Weerth C. Maternal prenatal stress is associated with the infant intestinal microbiota. Psychoneuroendocrino. 2015;53:233–45.CrossRef Zijlmans MA, Korpela K, Riksen-Walraven JM, de Vos WM, de Weerth C. Maternal prenatal stress is associated with the infant intestinal microbiota. Psychoneuroendocrino. 2015;53:233–45.CrossRef
12.
go back to reference Braeken MA, Jones A, Otte RA, Nyklicek I, Van den Bergh BR. Potential benefits of mindfulness during pregnancy on maternal autonomic nervous system function and infant development. Psychophysiology. 2017;54:279–88.PubMedCrossRef Braeken MA, Jones A, Otte RA, Nyklicek I, Van den Bergh BR. Potential benefits of mindfulness during pregnancy on maternal autonomic nervous system function and infant development. Psychophysiology. 2017;54:279–88.PubMedCrossRef
13.
go back to reference Molenaar NM, Tiemeier H, van Rossum E, Hillegers M, Bockting C, Hoogendijk W, et al. Prenatal maternal psychopathology and stress and offspring HPA axis function at 6 years. Psychoneuroendocrino. 2019;99:120–7.CrossRef Molenaar NM, Tiemeier H, van Rossum E, Hillegers M, Bockting C, Hoogendijk W, et al. Prenatal maternal psychopathology and stress and offspring HPA axis function at 6 years. Psychoneuroendocrino. 2019;99:120–7.CrossRef
14.
go back to reference Yang J, Han H, Cao J, Li L, Xu L. Prenatal stress modifies hippocampal synaptic plasticity and spatial learning in young rat offspring. Hippocampus. 2006;16:431–6.PubMedCrossRef Yang J, Han H, Cao J, Li L, Xu L. Prenatal stress modifies hippocampal synaptic plasticity and spatial learning in young rat offspring. Hippocampus. 2006;16:431–6.PubMedCrossRef
15.
go back to reference Glover V. Prenatal stress and its effects on the fetus and the child: Possible underlying biological mechanisms. Adv Neurobiol. 2015;10:269–83.PubMedCrossRef Glover V. Prenatal stress and its effects on the fetus and the child: Possible underlying biological mechanisms. Adv Neurobiol. 2015;10:269–83.PubMedCrossRef
16.
go back to reference Agis-Balboa RC, Arcos-Diaz D, Wittnam J, Govindarajan N, Blom K, Burkhardt S, et al. A hippocampal insulin-growth factor 2 pathway regulates the extinction of fear memories. Embo J. 2011;30:4071–83.PubMedPubMedCentralCrossRef Agis-Balboa RC, Arcos-Diaz D, Wittnam J, Govindarajan N, Blom K, Burkhardt S, et al. A hippocampal insulin-growth factor 2 pathway regulates the extinction of fear memories. Embo J. 2011;30:4071–83.PubMedPubMedCentralCrossRef
17.
go back to reference Chen DY, Stern SA, Garcia-Osta A, Saunier-Rebori B, Pollonini G, Bambah-Mukku D, et al. A critical role for IGF-II in memory consolidation and enhancement. Nature. 2011;469:491–7.PubMedPubMedCentralCrossRef Chen DY, Stern SA, Garcia-Osta A, Saunier-Rebori B, Pollonini G, Bambah-Mukku D, et al. A critical role for IGF-II in memory consolidation and enhancement. Nature. 2011;469:491–7.PubMedPubMedCentralCrossRef
18.
go back to reference Bracko O, Singer T, Aigner S, Knobloch M, Winner B, Ray J, et al. Gene expression profiling of neural stem cells and their neuronal progeny reveals IGF2 as a regulator of adult hippocampal neurogenesis. J Neurosci. 2012;32:3376–87.PubMedPubMedCentralCrossRef Bracko O, Singer T, Aigner S, Knobloch M, Winner B, Ray J, et al. Gene expression profiling of neural stem cells and their neuronal progeny reveals IGF2 as a regulator of adult hippocampal neurogenesis. J Neurosci. 2012;32:3376–87.PubMedPubMedCentralCrossRef
19.
go back to reference Schmeisser MJ, Baumann B, Johannsen S, Vindedal GF, Jensen V, Hvalby OC, et al. IkappaB kinase/nuclear factor kappaB-dependent insulin-like growth factor 2 (Igf2) expression regulates synapse formation and spine maturation via Igf2 receptor signaling. J Neurosci. 2012;32:5688–703.PubMedPubMedCentralCrossRef Schmeisser MJ, Baumann B, Johannsen S, Vindedal GF, Jensen V, Hvalby OC, et al. IkappaB kinase/nuclear factor kappaB-dependent insulin-like growth factor 2 (Igf2) expression regulates synapse formation and spine maturation via Igf2 receptor signaling. J Neurosci. 2012;32:5688–703.PubMedPubMedCentralCrossRef
20.
21.
go back to reference Noe E, Bonneau N, Fournier ML, Caille S, Cador M, Le Moine C. Arc reactivity in accumbens nucleus, amygdala and hippocampus differentiates cue over context responses during reactivation of opiate withdrawal memory. Neurobiol Learn Mem. 2019;159:24–35.PubMedCrossRef Noe E, Bonneau N, Fournier ML, Caille S, Cador M, Le Moine C. Arc reactivity in accumbens nucleus, amygdala and hippocampus differentiates cue over context responses during reactivation of opiate withdrawal memory. Neurobiol Learn Mem. 2019;159:24–35.PubMedCrossRef
22.
go back to reference Ratajczak P, Nowakowska E, Kus K, Danielewicz R, Herman S, Wozniak A. Neuroleptics and enrichment environment treatment in memory disorders and other central nervous system function observed in prenatally stressed rats. Hum Exp Toxicol. 2015;34:526–37.PubMedCrossRef Ratajczak P, Nowakowska E, Kus K, Danielewicz R, Herman S, Wozniak A. Neuroleptics and enrichment environment treatment in memory disorders and other central nervous system function observed in prenatally stressed rats. Hum Exp Toxicol. 2015;34:526–37.PubMedCrossRef
23.
go back to reference Nithianantharajah J, Hannan AJ. Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nat Rev Neurosci. 2006;7:697–709.PubMedCrossRef Nithianantharajah J, Hannan AJ. Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nat Rev Neurosci. 2006;7:697–709.PubMedCrossRef
24.
go back to reference Garrido-Garcia A, de Andres R, Jimenez-Pompa A, Soriano P, Sanz-Fuentes D, Martinez-Blanco E, et al. Neurogranin expression is regulated by synaptic activity and promotes synaptogenesis in cultured hippocampal neurons. Mol Neurobiol. 2019;56:7321–37.PubMedCrossRef Garrido-Garcia A, de Andres R, Jimenez-Pompa A, Soriano P, Sanz-Fuentes D, Martinez-Blanco E, et al. Neurogranin expression is regulated by synaptic activity and promotes synaptogenesis in cultured hippocampal neurons. Mol Neurobiol. 2019;56:7321–37.PubMedCrossRef
25.
go back to reference Wei Z, Meng X, El FR, Sun B, Mai D, Zhang J, et al. Environmental enrichment prevents Abeta oligomer-induced synaptic dysfunction through mirna-132 and hdac3 signaling pathways. Neurobiol Dis. 2020;134:104617.PubMedCrossRef Wei Z, Meng X, El FR, Sun B, Mai D, Zhang J, et al. Environmental enrichment prevents Abeta oligomer-induced synaptic dysfunction through mirna-132 and hdac3 signaling pathways. Neurobiol Dis. 2020;134:104617.PubMedCrossRef
26.
go back to reference Willner P. Validity, reliability and utility of the chronic mild stress model of depression: a 10-year review and evaluation. Psychopharmacology (Berl). 1997;134:319–29.CrossRef Willner P. Validity, reliability and utility of the chronic mild stress model of depression: a 10-year review and evaluation. Psychopharmacology (Berl). 1997;134:319–29.CrossRef
27.
go back to reference Liu XH, Qian LJ, Gong JB, Shen J, Zhang XM, Qian XH. Proteomic analysis of mitochondrial proteins in cardiomyocytes from chronic stressed rat. Proteomics. 2004;4:3167–76.PubMedCrossRef Liu XH, Qian LJ, Gong JB, Shen J, Zhang XM, Qian XH. Proteomic analysis of mitochondrial proteins in cardiomyocytes from chronic stressed rat. Proteomics. 2004;4:3167–76.PubMedCrossRef
28.
go back to reference Lui CC, Wang JY, Tain YL, Chen YC, Chang KA, Lai MC, et al. Prenatal stress in rat causes long-term spatial memory deficit and hippocampus MRI abnormality: differential effects of postweaning enriched environment. Neurochem Int. 2011;58:434–41.PubMedCrossRef Lui CC, Wang JY, Tain YL, Chen YC, Chang KA, Lai MC, et al. Prenatal stress in rat causes long-term spatial memory deficit and hippocampus MRI abnormality: differential effects of postweaning enriched environment. Neurochem Int. 2011;58:434–41.PubMedCrossRef
29.
go back to reference Kapoor A, Kostaki A, Janus C, Matthews SG. The effects of prenatal stress on learning in adult offspring is dependent on the timing of the stressor. Behav Brain Res. 2009;197:144–9.PubMedCrossRef Kapoor A, Kostaki A, Janus C, Matthews SG. The effects of prenatal stress on learning in adult offspring is dependent on the timing of the stressor. Behav Brain Res. 2009;197:144–9.PubMedCrossRef
30.
go back to reference Hauer D, Kaufmann I, Strewe C, Briegel I, Campolongo P, Schelling G. The role of glucocorticoids, catecholamines and endocannabinoids in the development of traumatic memories and posttraumatic stress symptoms in survivors of critical illness. Neurobiol Learn Mem. 2014;112:68–74.PubMedCrossRef Hauer D, Kaufmann I, Strewe C, Briegel I, Campolongo P, Schelling G. The role of glucocorticoids, catecholamines and endocannabinoids in the development of traumatic memories and posttraumatic stress symptoms in survivors of critical illness. Neurobiol Learn Mem. 2014;112:68–74.PubMedCrossRef
31.
go back to reference Hartman S, Eilertsen EM, Ystrom E, Belsky J, Gjerde LC. Does prenatal stress amplify effects of postnatal maternal depressive and anxiety symptoms on child problem behavior? Dev Psychol. 2020;56:128–37.PubMedCrossRef Hartman S, Eilertsen EM, Ystrom E, Belsky J, Gjerde LC. Does prenatal stress amplify effects of postnatal maternal depressive and anxiety symptoms on child problem behavior? Dev Psychol. 2020;56:128–37.PubMedCrossRef
32.
go back to reference Simons S, Zijlmans M, Cillessen A, de Weerth C. Maternal prenatal and early postnatal distress and child stress responses at age 6. Stress. 2019;22:654–63.PubMedCrossRef Simons S, Zijlmans M, Cillessen A, de Weerth C. Maternal prenatal and early postnatal distress and child stress responses at age 6. Stress. 2019;22:654–63.PubMedCrossRef
33.
go back to reference Iturra-Mena AM, Arriagada-Solimano M, Luttecke-Anders A, Dagnino-Subiabre A. Effects of prenatal stress on anxiety- and depressive-like behaviours are sex-specific in prepubertal rats. J Neuroendocrinol. 2018;30:e12609.PubMedCrossRef Iturra-Mena AM, Arriagada-Solimano M, Luttecke-Anders A, Dagnino-Subiabre A. Effects of prenatal stress on anxiety- and depressive-like behaviours are sex-specific in prepubertal rats. J Neuroendocrinol. 2018;30:e12609.PubMedCrossRef
34.
go back to reference Tang X, Lu Z, Hu D, Zhong X. Influencing factors for prenatal stress, anxiety and depression in early pregnancy among women in Chongqing, China. J Affect Disord. 2019;253:292–302.PubMedCrossRef Tang X, Lu Z, Hu D, Zhong X. Influencing factors for prenatal stress, anxiety and depression in early pregnancy among women in Chongqing, China. J Affect Disord. 2019;253:292–302.PubMedCrossRef
35.
go back to reference Suzuki A, Iinuma M, Hayashi S, Sato Y, Azuma K, Kubo KY. Maternal chewing during prenatal stress ameliorates stress-induced hypomyelination, synaptic alterations, and learning impairment in mouse offspring. Brain Res. 2016;1651:36–43.PubMedCrossRef Suzuki A, Iinuma M, Hayashi S, Sato Y, Azuma K, Kubo KY. Maternal chewing during prenatal stress ameliorates stress-induced hypomyelination, synaptic alterations, and learning impairment in mouse offspring. Brain Res. 2016;1651:36–43.PubMedCrossRef
36.
go back to reference Zhang H, Shang Y, Xiao X, Yu M, Zhang T. Prenatal stress-induced impairments of cognitive flexibility and bidirectional synaptic plasticity are possibly associated with autophagy in adolescent male-offspring. Exp Neurol. 2017;298:68–78.PubMedCrossRef Zhang H, Shang Y, Xiao X, Yu M, Zhang T. Prenatal stress-induced impairments of cognitive flexibility and bidirectional synaptic plasticity are possibly associated with autophagy in adolescent male-offspring. Exp Neurol. 2017;298:68–78.PubMedCrossRef
37.
go back to reference Bruel-Jungerman E, Laroche S, Rampon C. New neurons in the dentate gyrus are involved in the expression of enhanced long-term memory following environmental enrichment. Eur J Neurosci. 2005;21:513–21.PubMedCrossRef Bruel-Jungerman E, Laroche S, Rampon C. New neurons in the dentate gyrus are involved in the expression of enhanced long-term memory following environmental enrichment. Eur J Neurosci. 2005;21:513–21.PubMedCrossRef
38.
go back to reference Kapoor A, Dunn E, Kostaki A, Andrews MH, Matthews SG. Fetal programming of hypothalamo-pituitary-adrenal function: prenatal stress and glucocorticoids. J Physiol. 2006;572:31–44.PubMedPubMedCentralCrossRef Kapoor A, Dunn E, Kostaki A, Andrews MH, Matthews SG. Fetal programming of hypothalamo-pituitary-adrenal function: prenatal stress and glucocorticoids. J Physiol. 2006;572:31–44.PubMedPubMedCentralCrossRef
39.
go back to reference Doreste-Mendez R, Rios-Ruiz EJ, Rivera-Lopez LL, Gutierrez A, Torres-Reveron A. Effects of environmental enrichment in maternally separated rats: age and sex-specific outcomes. Front Behav Neurosci. 2019;13:198.PubMedPubMedCentralCrossRef Doreste-Mendez R, Rios-Ruiz EJ, Rivera-Lopez LL, Gutierrez A, Torres-Reveron A. Effects of environmental enrichment in maternally separated rats: age and sex-specific outcomes. Front Behav Neurosci. 2019;13:198.PubMedPubMedCentralCrossRef
40.
go back to reference Machida M, Fujimaki S, Hidaka R, Asashima M, Kuwabara T. The insulin regulatory network in adult hippocampus and pancreatic endocrine system. Stem Cells Int. 2012;2012:959737.PubMedPubMedCentralCrossRef Machida M, Fujimaki S, Hidaka R, Asashima M, Kuwabara T. The insulin regulatory network in adult hippocampus and pancreatic endocrine system. Stem Cells Int. 2012;2012:959737.PubMedPubMedCentralCrossRef
41.
go back to reference Marrocco J, Gray JD, Kogan JF, Einhorn NR, O'Cinneide EM, Rubin TG, et al. Early life stress restricts translational reactivity in CA3 neurons associated with altered stress responses in adulthood. Front Behav Neurosci. 2019;13:157.PubMedPubMedCentralCrossRef Marrocco J, Gray JD, Kogan JF, Einhorn NR, O'Cinneide EM, Rubin TG, et al. Early life stress restricts translational reactivity in CA3 neurons associated with altered stress responses in adulthood. Front Behav Neurosci. 2019;13:157.PubMedPubMedCentralCrossRef
42.
go back to reference Hermes M, Antonow-Schlorke I, Hollstein D, Kuehnel S, Rakers F, Frauendorf V, et al. Maternal psychosocial stress during early gestation impairs fetal structural brain development in sheep. Stress. 2020;23:233–42.PubMedCrossRef Hermes M, Antonow-Schlorke I, Hollstein D, Kuehnel S, Rakers F, Frauendorf V, et al. Maternal psychosocial stress during early gestation impairs fetal structural brain development in sheep. Stress. 2020;23:233–42.PubMedCrossRef
43.
go back to reference Stern SA, Kohtz AS, Pollonini G, Alberini CM. Enhancement of memories by systemic administration of insulin-like growth factor II. Neuropsychopharmacol. 2014;39:2179–90.CrossRef Stern SA, Kohtz AS, Pollonini G, Alberini CM. Enhancement of memories by systemic administration of insulin-like growth factor II. Neuropsychopharmacol. 2014;39:2179–90.CrossRef
44.
go back to reference Taubenfeld SM, Milekic MH, Monti B, Alberini CM. The consolidation of new but not reactivated memory requires hippocampal C/EBPbeta. Nat Neurosci. 2001;4:813–8.PubMedCrossRef Taubenfeld SM, Milekic MH, Monti B, Alberini CM. The consolidation of new but not reactivated memory requires hippocampal C/EBPbeta. Nat Neurosci. 2001;4:813–8.PubMedCrossRef
45.
go back to reference Steward O, Worley PF. Selective targeting of newly synthesized Arc mRNA to active synapses requires NMDA receptor activation. Neuron. 2001;30:227–40.PubMedCrossRef Steward O, Worley PF. Selective targeting of newly synthesized Arc mRNA to active synapses requires NMDA receptor activation. Neuron. 2001;30:227–40.PubMedCrossRef
46.
go back to reference Cho KK, Khibnik L, Philpot BD, Bear MF. The ratio of NR2A/B NMDA receptor subunits determines the qualities of ocular dominance plasticity in visual cortex. Proc Natl Acad Sci U S A. 2009;106:5377–82.PubMedPubMedCentralCrossRef Cho KK, Khibnik L, Philpot BD, Bear MF. The ratio of NR2A/B NMDA receptor subunits determines the qualities of ocular dominance plasticity in visual cortex. Proc Natl Acad Sci U S A. 2009;106:5377–82.PubMedPubMedCentralCrossRef
47.
go back to reference Chowdhury S, Shepherd JD, Okuno H, Lyford G, Petralia RS, Plath N, et al. Arc/Arg3.1 interacts with the endocytic machinery to regulate AMPA receptor trafficking. Neuron. 2006;52:445–59.PubMedPubMedCentralCrossRef Chowdhury S, Shepherd JD, Okuno H, Lyford G, Petralia RS, Plath N, et al. Arc/Arg3.1 interacts with the endocytic machinery to regulate AMPA receptor trafficking. Neuron. 2006;52:445–59.PubMedPubMedCentralCrossRef
48.
go back to reference Rial VE, Lee-Osbourne J, Worley PF, Malinow R, Cline HT. Increased expression of the immediate-early gene arc/arg3.1 reduces AMPA receptor-mediated synaptic transmission. Neuron. 2006;52:461–74.CrossRef Rial VE, Lee-Osbourne J, Worley PF, Malinow R, Cline HT. Increased expression of the immediate-early gene arc/arg3.1 reduces AMPA receptor-mediated synaptic transmission. Neuron. 2006;52:461–74.CrossRef
49.
go back to reference Dikkes P, Jaffe DB, Guo WH, Chao C, Hemond P, Yoon K, et al. IGF2 knockout mice are resistant to kainic acid-induced seizures and neurodegeneration. Brain Res. 2007;1175:85–95.PubMedCrossRef Dikkes P, Jaffe DB, Guo WH, Chao C, Hemond P, Yoon K, et al. IGF2 knockout mice are resistant to kainic acid-induced seizures and neurodegeneration. Brain Res. 2007;1175:85–95.PubMedCrossRef
50.
go back to reference Fumagalli F, Franchi C, Caffino L, Racagni G, Riva MA, Cervo L. Single session of cocaine intravenous self-administration shapes goal-oriented behaviours and up-regulates Arc mRNA levels in rat medial prefrontal cortex. Int J Neuropsychopharmacol. 2009;12:423–9.PubMedCrossRef Fumagalli F, Franchi C, Caffino L, Racagni G, Riva MA, Cervo L. Single session of cocaine intravenous self-administration shapes goal-oriented behaviours and up-regulates Arc mRNA levels in rat medial prefrontal cortex. Int J Neuropsychopharmacol. 2009;12:423–9.PubMedCrossRef
Metadata
Title
The mechanism of enriched environment repairing the learning and memory impairment in offspring of prenatal stress by regulating the expression of activity-regulated cytoskeletal-associated and insulin-like growth factor-2 in hippocampus
Authors
Su-zhen Guan
You-juan Fu
Feng Zhao
Hong-ya Liu
Xiao-hui Chen
Fa-qiu Qi
Zhi-hong Liu
Tzi Bun Ng
Publication date
01-12-2021
Publisher
BioMed Central
Keywords
Insulins
Insulins
Published in
Environmental Health and Preventive Medicine / Issue 1/2021
Print ISSN: 1342-078X
Electronic ISSN: 1347-4715
DOI
https://doi.org/10.1186/s12199-020-00929-7

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