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Prenatal restraint stress impairs recognition memory in adult male and female offspring

Published online by Cambridge University Press:  29 January 2020

Clarissa A. Moura ,
Matheus C. Oliveira ,
Layse F. Costa ,
Pamella R. F. Tiago ,
Victor A. D. Holanda ,
Ramon H. Lima ,
Fernanda C. Cagni ,
Bruno Lobão-Soares ,
Franscico Bolaños-Jiménez  and
Elaine C. Gavioli Open the ORCID record for Elaine C. Gavioli [Opens in a new window]
Clarissa A. Moura
Affiliation:
Department of Biophysics and Pharmacology, Federal University of Rio Grande do Norte, Natal, RN, Brazil
Matheus C. Oliveira
Affiliation:
Department of Biophysics and Pharmacology, Federal University of Rio Grande do Norte, Natal, RN, Brazil
Layse F. Costa
Affiliation:
Department of Biophysics and Pharmacology, Federal University of Rio Grande do Norte, Natal, RN, Brazil
Pamella R. F. Tiago
Affiliation:
Department of Biophysics and Pharmacology, Federal University of Rio Grande do Norte, Natal, RN, Brazil
Victor A. D. Holanda
Affiliation:
Department of Biophysics and Pharmacology, Federal University of Rio Grande do Norte, Natal, RN, Brazil
Ramon H. Lima
Affiliation:
Department of Biophysics and Pharmacology, Federal University of Rio Grande do Norte, Natal, RN, Brazil
Fernanda C. Cagni
Affiliation:
Department of Biophysics and Pharmacology, Federal University of Rio Grande do Norte, Natal, RN, Brazil
Bruno Lobão-Soares
Affiliation:
Department of Biophysics and Pharmacology, Federal University of Rio Grande do Norte, Natal, RN, Brazil
Franscico Bolaños-Jiménez
Affiliation:
UMR 1280 Physiologie des Adaptations Nutritionnelles, INRA-Université de Nantes, Nantes, France
Elaine C. Gavioli*
Affiliation:
Department of Biophysics and Pharmacology, Federal University of Rio Grande do Norte, Natal, RN, Brazil
*
Author for correspondence: Elaine C. Gavioli, Email: [email protected]
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Abstract

Objective:

Accumulating evidence from preclinical and clinical studies indicates that prenatal exposure to stress impairs the development of the offspring brain and facilitates the emergence of mental illness. This study aims to describe the impact of prenatal restraint stress on cognition and exploration to an unfamiliar environment at adulthood in an outbred strain of mice.

Methods:

Late pregnant mice were exposed to restraint stress and adult offspring (60 days of age) behaviours were assessed in the object recognition task and open field test.

Findings:

Prenatal stress (PNS) impaired new object recognition in male and female mice. Importantly, the learning deficits in female PNS mice were linked to their estrous cycle. Actually, PNS females in metestrus/diestrus but not in proestrus/estrus phases displayed recognition deficits compared to controls. Concerning locomotion in an unfamiliar environment, male but not female PNS mice displayed significant increase, but showed no differences in the distance travelled within the centre zone of the arena.

Conclusion:

Present findings support the view that maternal restraint-stress during late pregnancy impairs recognition memory in both male and female offspring, and in females, this cognitive deficit is dependent on the estrous cycle phase. Ultimately, these data reinforce that PNS is an aetiological component of psychiatric disorders associated with memory deficits.

Keywords

restraint prenatal stressrecognition object taskestrous cycleopen fieldmouse
Type
Original Article
Information
Acta Neuropsychiatrica , Volume 32 , Issue 3 , June 2020 , pp. 122 - 127
Copyright
© Scandinavian College of Neuropsychopharmacology 2020

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References

Abdul Aziz, NH, Kendall, DA and Pardon, MC (2012) Prenatal exposure to chronic mild stress increases corticosterone levels in the amniotic fluid and induces cognitive deficits in female offspring, improved by treatment with the antidepressant drug amitriptyline. Behavioural Brain Research 231(1), 29–39.CrossRefGoogle ScholarPubMed
Behan, AT, van den Hove, DL, Mueller, L, Jetten, MJ, Steinbusch, HW, Cotter, DR and Prickaerts, J (2011) Evidence of female-specific glial deficits in the hippocampus in a mouse model of prenatal stress. European Neuropsychopharmacology 21(1), 71–79.CrossRefGoogle Scholar
Benoit, JD, Rakic, P and Frick, KM (2015) Prenatal stress induces spatial memory deficits and epigenetic changes in the hippocampus indicative of heterochromatin formation and reduced gene expression. Behavioural Brain Research 281, 1–8.CrossRefGoogle ScholarPubMed
Bock, J, Wainstock, T, Braun, K and Segal, M (2015) Stress in utero: prenatal programming of brain plasticity and cognition. Biological Psychiatry 78(5), 315–326.CrossRefGoogle ScholarPubMed
Boersma, GJ and Tamashiro, KL (2014) Individual differences in the effects of prenatal stress exposure in rodents. Neurobiology of Stress 1, 100–108.CrossRefGoogle ScholarPubMed
Brannigan, R, Cannon, M, Tanskanen, A, Huttunen, MO, Leacy, FP and Clarke, MC (2019) The association between subjective maternal stress during pregnancy and offspring clinically diagnosed psychiatric disorders. Acta Psychiatrica Scandinavica 139(4), 304–310.CrossRefGoogle ScholarPubMed
Clarke, DJ, Sarkissian, L, Todd, SM, Suraev, AS, Bahceci, D, Brzozowska, N and Arnold, JC (2019) Nrg1 deficiency modulates the behavioural effects of prenatal stress in mice. Progress in Neuro-psychopharmacology & Biological Psychiatry 88, 86–95.CrossRefGoogle ScholarPubMed
Cohen, SJ and Stackman, RW Jr (2015) Assessing rodent hippocampal involvement in the novel object recognition task. A review. Behavioural Brain Research 285, 105–117.CrossRefGoogle ScholarPubMed
Contreras, CM, Molina, M, Saavedra, M and Martínez-Mota, L (2000) Lateral septal neuronal firing rate increases during proestrus-estrus in the rat. Physiology & Behavior 68, 279–284.CrossRefGoogle ScholarPubMed
Dong, E, Dzitoyeva, SG, Matrisciano, F, Tueting, P, Grayson, DR and Guidotti, A (2015) Brain-derived neurotrophic factor epigenetic modifications associated with schizophrenia-like phenotype induced by prenatal stress in mice. Biological Psychiatry 77, 589–596.CrossRefGoogle ScholarPubMed
Gur, TL, Shay, L, Palkar, AV, Fisher, S, Varaljay, VA, Dowd, S and Bailey, MT (2017) Prenatal stress affects placental cytokines and neurotrophins, commensal microbes, and anxiety-like behavior in adult female offspring. Brain, Behavior, and Immunity 64, 50–58.CrossRefGoogle ScholarPubMed
Hiroi, R, Carbone, DL, Zuloaga, DG, Bimonte-Nelson, HA and Handa, RJ (2016) Sex-dependent programming effects of prenatal glucocorticoid treatment on the developing serotonin system and stress-related behaviors in adulthood. Neuroscience 320, 43–56.CrossRefGoogle ScholarPubMed
Hollins, SL and Cairns, MJ (2016) MicroRNA: small RNA mediators of the brains genomic response to environmental stress. Progress in Neurobiology 143, 61–81.CrossRefGoogle ScholarPubMed
Kilkenny, C, Browne, W, Cuthill, IC, Emerson, M, Altman, DG and NC3Rs Reporting Guidelines Working Group (2010) Animal research: reporting in vivo experiments: the ARRIVE guidelines. British Journal of Pharmacology 160(7), 1577–1579.CrossRefGoogle ScholarPubMed
Kippin, TE, Szumlinski, KK, Kapasova, Z, Rezner, B and See, RE (2008) Prenatal stress enhances responsiveness to cocaine. Neuropsychopharmacology 33(4), 769–782.CrossRefGoogle ScholarPubMed
Kiryanova, V, Meunier, SJ, Vecchiarelli, HA, Hill, MN and Dyck, RH (2016) Effects of maternal stress and perinatal fluoxetine exposure on behavioral outcomes of adult male offspring. Neuroscience 320, 281–296.CrossRefGoogle ScholarPubMed
Lee, YA, Kim, YJ and Goto, Y (2016) Cognitive and affective alterations by prenatal and postnatal stress interaction. Physiology &Behavior 165, 146–153.CrossRefGoogle ScholarPubMed
Leger, M, Quiedeville, A, Bouet, V, Haelewyn, B, Boulouard, M, Schumann-Bard, P and Freret, T (2013) Object recognition test in mice. Nature Protocols 8(12), 2531–2537.CrossRefGoogle ScholarPubMed
Li, J, Yang, H, Guldin, MB, Vedsted, P and Vestergaard, M (2015) Increased utilisation of primary healthcare in persons exposed to severe stress in prenatal life: a national population-based study in Denmark. BMJ Open 5(1), e005657.CrossRefGoogle ScholarPubMed
Maccari, S and Morley-Fletcher, S (2007) Effects of prenatal restraint stress on the hypothalamus-pituitary-adrenal axis and related behavioural and neurobiological alterations. Psychoneuroendocrinology 32(S1), S10–S15.CrossRefGoogle ScholarPubMed
Miranda, A and Sousa, N (2018) Maternal hormonal milieu influence on fetal brain development. Brain Behaviour 8(2), e00920.CrossRefGoogle ScholarPubMed
Nakhjiri, E, Saboory, E, Roshan-Milani, S, Rasmi, Y and Khalafkhani, D (2017) Effect of prenatal restraint stress and morphine co-administration on plasma vasopressin concentration and anxiety behaviors in adult rat offspring. Stress 20(2), 205–211.CrossRefGoogle ScholarPubMed
Owen, D, Andrews, MH and Matthews, SG (2005) Maternal adversity, glucocorticoids and programming of neuroendocrine function and behavior. Neuroscience and Biobehavioral Reviews 29, 209–226.CrossRefGoogle Scholar
Pallarés, ME and Antonelli, MC (2017) Prenatal stress and neurodevelopmental plasticity: relevance to psychopathology. Advances in Experimental Medicine and Biology 1015, 117–129.CrossRefGoogle ScholarPubMed
Pugliese, V, Bruni, A, Carbone, EA, Calabrò, G, Cerminara, G, Sampogna, G, Luciano, M, Steardo, L Jr, Fiorillo, A, Garcia, CS and De Fazio, P (2019) Maternal stress, prenatal medical illnesses and obstetric complications: risk factors for schizophrenia spectrum disorder, bipolar disorder and major depressive disorder. Psychiatry Research 271, 23–30.CrossRefGoogle ScholarPubMed
Rosenqvist, MA, Sjölander, A, Ystrom, E, Larsson, H and Reichborn-Kjennerud, T (2018) Adverse family life events during pregnancy and ADHD symptoms in five-year-old offspring. Journal of Child Psychology and Psychiatry, and Allied Disciplines 60(6), 665–675.CrossRefGoogle ScholarPubMed
Schroeder, M, Sultany, T and Weller, A (2013). Prenatal stress effects on emotion regulation differ by genotype and sex in prepubertal rats. Developmental Psychobiology 55(2), 176–192.CrossRefGoogle ScholarPubMed
Seibenhener, ML and Wooten, MC (2015) Use of the open field maze to measure locomotor and anxiety-like behavior in mice. Journal of Visualized Experiments 96, e52434.Google Scholar
Singletary, SJ, Kirsch, AJ, Watson, J, Karim, BO, Huso, DL, Hurn, PD and Murphy, SJ (2005) Lack of correlation of vaginal impedance measurements with hormone levels in the rat. Contemporary Topics in Laboratory Animal Science 44(6), 37–42.Google ScholarPubMed
Son, GH, Chung, S, Geum, D, Kang, SS, Choi, WS, Kim, K, Choi, S (2007) Hyperactivity and alteration of the midbrain dopaminergic system in maternally stressed male mice offspring. Biochemical and Biophysical Research Communications 352(3), 823–829.CrossRefGoogle ScholarPubMed
Son, GH, Geum, D, Chung, S, Kim, EJ, Jo, JH, Kim, CM, Lee, KH, Kim, H, Choi, S, Kim, HT, Lee, CJ and Kim, K (2006) Maternal stress produces learning deficits associated with impairment of NMDA receptor-mediated synaptic plasticity. Journal of Neuroscience 26(12), 3309–3318.CrossRefGoogle ScholarPubMed
Van den Bergh, BRH, van den Heuvel, MI, Lahti, M, Braeken, M, de Rooij, SR, Entringer, S, Hoyer, D, Roseboom, T, Räikkönen, K, King, S and Schwab, M (2017) Prenatal developmental origins of behavior and mental health: the influence of maternal stress in pregnancy. Neuroscience and Biobehavioral Reviews, in press, doi: 10.1016/j.neubiorev.2017.07.003CrossRefGoogle ScholarPubMed
Van den Hove, DL, Blanco, CE, Aendekerk, B, Desbonnet, L, Bruschettini, M, Steinbusch, HP, Prickaerts, J and Steinbusch, HW (2005) Prenatal restraint stress and long-term affective consequences. Developmental Neuroscience 27(5), 313–320.CrossRefGoogle ScholarPubMed
Van Goethem, NP, Rutten, K, van der Staay, FJ, Jans, LA, Akkerman, S, Steinbusch, HW, Blokland, A, van’tKlooster, J and Prickaerts, J (2012) Object recognition testing: rodent species, strains, housing conditions, and estrous cycle. Behavioural Brain Research 232(2), 323–334.CrossRefGoogle ScholarPubMed
Varcin, KJ, Alvares, GA, Uljarević, M and Whitehouse, AJO (2017) Prenatal maternal stress events and phenotypic outcomes in Autism Spectrum Disorder. Autism Research 10(11), 1866–1877.CrossRefGoogle ScholarPubMed
Woolley, CS and McEwen, BS (1992) Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. Journal of Neuroscience 12, 2549–2554.CrossRefGoogle ScholarPubMed
Zhang, Y, Wang, R, Chen, R and Wang, L (2019) Changes of Wnt/β-catenin signaling pathway in the hippocampus caused by prenatal stress induce depression- and anxiety-like behaviors in rats. Nan fang yike da xuexuebao 39(2), 222–226.Google ScholarPubMed
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