Early life adversities or high fat diet intake reduce cognitive function and alter BDNF signaling in adult rats: Interplay of these factors changes these effects
Corresponding Author
Danusa Mar Arcego
Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, UFRGS, Porto Alegre, Rio Grande do Sul, Brazil
Corresponding author at: Departamento de Bioquímica, ICBS, UFRGS, Ramiro Barcelos, 2600 (Anexo) Lab. 37, 90035-003 Porto Alegre, RS, Brazil. Fax: +55 51 3308 5535.
E-mail address: [email protected] (D.M. Arcego).
Search for more papers by this authorRachel Krolow
Programa de Pós-Graduação em Saúde e Comportamento, Universidade Católica de Pelotas (UCPel), Pelotas, RS, Brazil
Search for more papers by this authorCarine Lampert
Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, UFRGS, Porto Alegre, Rio Grande do Sul, Brazil
Search for more papers by this authorAna Paula Toniazzo
Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, UFRGS, Porto Alegre, Rio Grande do Sul, Brazil
Search for more papers by this authorCarolina Berlitz
Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, UFRGS, Porto Alegre, Rio Grande do Sul, Brazil
Search for more papers by this authorCamilla Lazzaretti
Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, UFRGS, Porto Alegre, Rio Grande do Sul, Brazil
Search for more papers by this authorFelipe Schmitz
Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, UFRGS, Porto Alegre, Rio Grande do Sul, Brazil
Search for more papers by this authorAndré Felipe Rodrigues
Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, UFRGS, Porto Alegre, Rio Grande do Sul, Brazil
Search for more papers by this authorAngela T.S. Wyse
Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, UFRGS, Porto Alegre, Rio Grande do Sul, Brazil
Search for more papers by this authorCarla Dalmaz
Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, UFRGS, Porto Alegre, Rio Grande do Sul, Brazil
Search for more papers by this authorCorresponding Author
Danusa Mar Arcego
Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, UFRGS, Porto Alegre, Rio Grande do Sul, Brazil
Corresponding author at: Departamento de Bioquímica, ICBS, UFRGS, Ramiro Barcelos, 2600 (Anexo) Lab. 37, 90035-003 Porto Alegre, RS, Brazil. Fax: +55 51 3308 5535.
E-mail address: [email protected] (D.M. Arcego).
Search for more papers by this authorRachel Krolow
Programa de Pós-Graduação em Saúde e Comportamento, Universidade Católica de Pelotas (UCPel), Pelotas, RS, Brazil
Search for more papers by this authorCarine Lampert
Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, UFRGS, Porto Alegre, Rio Grande do Sul, Brazil
Search for more papers by this authorAna Paula Toniazzo
Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, UFRGS, Porto Alegre, Rio Grande do Sul, Brazil
Search for more papers by this authorCarolina Berlitz
Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, UFRGS, Porto Alegre, Rio Grande do Sul, Brazil
Search for more papers by this authorCamilla Lazzaretti
Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, UFRGS, Porto Alegre, Rio Grande do Sul, Brazil
Search for more papers by this authorFelipe Schmitz
Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, UFRGS, Porto Alegre, Rio Grande do Sul, Brazil
Search for more papers by this authorAndré Felipe Rodrigues
Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, UFRGS, Porto Alegre, Rio Grande do Sul, Brazil
Search for more papers by this authorAngela T.S. Wyse
Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, UFRGS, Porto Alegre, Rio Grande do Sul, Brazil
Search for more papers by this authorCarla Dalmaz
Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, UFRGS, Porto Alegre, Rio Grande do Sul, Brazil
Search for more papers by this authorAbstract
Environmental factors, like early exposure to stressors or high caloric diets, can alter the early programming of central nervous system, leading to long-term effects on cognitive function, increased vulnerability to cognitive decline and development of psychopathologies later in life. The interaction between these factors and their combined effects on brain structure and function are still not completely understood. In this study, we evaluated long-term effects of social isolation in the prepubertal period, with or without chronic high fat diet access, on memory and on neurochemical markers in the prefrontal cortex of rats. We observed that early social isolation led to impairment in short-term and working memory in adulthood, and to reductions of Na+,K+-ATPase activity and the immunocontent of phospho-AKT, in prefrontal cortex. Chronic exposure to a high fat diet impaired short-term memory (object recognition), and decreased BDNF levels in that same brain area. Remarkably, the association of social isolation with chronic high fat diet rescued the memory impairment on the object recognition test, as well as the changes in BDNF levels, Na+,K+-ATPase activity, MAPK, AKT and phospho-AKT to levels similar to the control-chow group. In summary, these findings showed that a brief social isolation period and access to a high fat diet during a sensitive developmental period might cause memory deficits in adulthood. On the other hand, the interplay between isolation and high fat diet access caused a different brain programming, preventing some of the effects observed when these factors are separately applied.
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References
- F.H. Abdalla, R. Schmatz, A.M. Cardoso, F.B. Carvalho, J. Baldissarelli, J.S. de Oliveira, M.M. Rosa, M.A. Goncalves Nunes, M.A. Rubin, I.B. da Cruz, F. Barbisan, V.L. Dressler, L.B. Pereira, M.R. Schetinger, V.M. Morsch, J.F. Goncalves, C.M. Mazzanti. Quercetin protects the impairment of memory and anxiogenic-like behavior in rats exposed to cadmium: possible involvement of the acetylcholinesterase and Na(+), K(+)-ATPase activities. Physiol. Behav. 135: 2014; 152–167
- A. Abildgaard, S. Lund, K.S. Hougaard. Chronic high-fat diet increases acute neuroendocrine stress response independently of prenatal dexamethasone treatment in male rats. Acta Neuropsychiatr. 26: 2014; 8–18
- T.C. Adam, E.S. Epel. Stress, eating and the reward system. Physiol. Behav. 91: 2007; 449–458
- R. Andero, D.C. Choi, K.J. Ressler. BDNF-TrkB receptor regulation of distributed adult neural plasticity, memory formation, and psychiatric disorders. Prog. Mol. Biol. Transl. Sci. 122: 2014; 169–192
- D.M. Arcego, R. Krolow, C. Lampert, C. Noschang, A.G. Ferreira, E. Scherer, A.T. Wyse, C. Dalmaz. Isolation during the prepubertal period associated with chronic access to palatable diets: effects on plasma lipid profile and liver oxidative stress. Physiol. Behav. 124: 2014; 23–32
- K. Arvaniti, Q. Huang, D. Richard. Effects of leptin and corticosterone on the expression of corticotropin-releasing hormone, agouti-related protein, and proopiomelanocortin in the brain of ob/ob mouse. Neuroendocrinology. 73: 2001; 227–236
- H.E. Auvinen, J.A. Romijn, N.R. Biermasz, H. Pijl, L.M. Havekes, J.W. Smit, P.C. Rensen, A.M. Pereira. The effects of high fat diet on the basal activity of the hypothalamus-pituitary-adrenal axis in mice. J. Endocrinol. 214: 2012; 191–197
- R. Bakker, P. Tiesinga, R. Kotter. The scalable brain atlas: instant web-based access to public brain atlases and related content. Neuroinformatics. 13: 2015; 353–366
- G.R. Barker, F. Bird, V. Alexander, E.C. Warburton. Recognition memory for objects, place, and temporal order: a disconnection analysis of the role of the medial prefrontal cortex and perirhinal cortex. J. Neurosci. 27: 2007; 2948–2957
- M.R. Bennett, J. Lagopoulos. Stress and trauma: bDNF control of dendritic-spine formation and regression. Prog. Neurobiol. 112: 2014; 80–99
- S.J. Blakemore, S. Choudhury. Development of the adolescent brain: implications for executive function and social cognition. J. Child Psychol. Psychiatry. 47: 2006; 296–312
- M.M. Bradford. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 1976; 248–254
- W.W. Burggren, C.A. Mueller. Developmental critical windows and sensitive periods as three-dimensional constructs in time and space *. Physiol. Biochem. Zool. 88: 2015; 91–102
- B. Buwalda, W.A. Blom, J.M. Koolhaas, G. van Dijk. Behavioral and physiological responses to stress are affected by high-fat feeding in male rats. Physiol. Behav. 73: 2001; 371–377
- E. Calabrese, A. Badea, C. Watson, G.A. Johnson. A quantitative magnetic resonance histology atlas of postnatal rat brain development with regional estimates of growth and variability. Neuroimage. 71: 2013; 196–206
- D. Camer, Y. Yu, A. Szabo, F. Fernandez, C.H. Dinh, X.F. Huang. Bardoxolone methyl prevents high-fat diet-induced alterations in prefrontal cortex signalling molecules involved in recognition memory. Prog. Neuropsychopharmacol. Biol. Psychiatry. 59: 2015; 68–75
- K.M. Chan, D. Delfert, K.D. Junger. A direct colorimetric assay for Ca2+ −stimulated ATPase activity. Anal. Biochem. 157: 1986; 375–380
- K.H. Choy, Y. de Visser, N.R. Nichols, M. van den Buuse. Combined neonatal stress and young-adult glucocorticoid stimulation in rats reduce BDNF expression in hippocampus: effects on learning and memory. Hippocampus. 18: 2008; 655–667
- E.A. Crone. Executive functions in adolescence: inferences from brain and behavior. Dev. Sci. 12: 2009; 825–830
- Y. Cui, Y. Shu, Y. Zhu, Y. Shi, G. Le. High-fat diets impair spatial learning of mice in the Y-maze paradigm: ameliorative potential of alpha-lipoic acid. J. Med. Food. 15: 2012; 713–717
- L.A. Douglas, E.I. Varlinskaya, L.P. Spear. Rewarding properties of social interactions in adolescent and adult male and female rats: impact of social versus isolate housing of subjects and partners. Dev. Psychobiol. 45: 2004; 153–162
- A. Ennaceur, J. Delacour. A new one-trial test for neurobiological studies of memory in rats. 1 Behavioral data. Behav. Brain Res. 31: 1988; 47–59
- K. Fabricius, L. Helboe, A. Fink-Jensen, G. Wortwein, B. Steiniger-Brach. Pharmacological characterization of social isolation-induced hyperactivity. Psychopharmacology (Berl.). 215: 2011; 257–266
- H.M. Francis, R.J. Stevenson. Higher reported saturated fat and refined sugar intake is associated with reduced hippocampal-dependent memory and sensitivity to interoceptive signals. Behav. Neurosci. 125: 2011; 943–955
- S. Fujisawa, G. Buzsaki. A 4Hz oscillation adaptively synchronizes prefrontal, VTA, and hippocampal activities. Neuron. 72: 2011; 153–165
- P.L. Gaskin, S.P. Alexander, K.C. Fone. Neonatal phencyclidine administration and post-weaning social isolation as a dual-hit model of ‘schizophrenia-like’ behaviour in the rat. Psychopharmacology (Berl.). 231: 2014; 2533–2545
- N. Gogtay, J.N. Giedd, L. Lusk, K.M. Hayashi, D. Greenstein, A.C. Vaituzis, T.F. Nugent 3rd, D.H. Herman, L.S. Clasen, A.W. Toga, J.L. Rapoport, P.M. Thompson. Dynamic mapping of human cortical development during childhood through early adulthood. Proc. Natl. Acad. Sci. U. S. A. 101: 2004; 8174–8179
- P.S. Goldman-Rakic. Cellular basis of working memory. Neuron. 14: 1995; 477–485
- B. Gonzalez, M. Raineri, J.L. Cadet, E. Garcia-Rill, F.J. Urbano, V. Bisagno. Modafinil improves methamphetamine-induced object recognition deficits and restores prefrontal cortex ERK signaling in mice. Neuropharmacology. 87: 2014; 188–197
- A.C. Granholm, H.A. Bimonte-Nelson, A.B. Moore, M.E. Nelson, L.R. Freeman, K. Sambamurti. Effects of a saturated fat and high cholesterol diet on memory and hippocampal morphology in the middle-aged rat. J. Alzheimers Dis. 14: 2008; 133–145
- F.L. Groeneweg, H. Karst, E.R. de Kloet, M. Joels. Mineralocorticoid and glucocorticoid receptors at the neuronal membrane, regulators of nongenomic corticosteroid signalling. Mol. Cell. Endocrinol. 350: 2012; 299–309
- M.L. Heiman, R.S. Ahima, L.S. Craft, B. Schoner, T.W. Stephens, J.S. Flier. Leptin inhibition of the hypothalamic-pituitary-adrenal axis in response to stress. Endocrinology. 138: 1997; 3859–3863
- J. Hernandez-Rapp, P.Y. Smith, M. Filali, C. Goupil, E. Planel, S.T. Magill, R.H. Goodman, S.S. Hebert. Memory formation and retention are affected in adult miR-132/212 knockout mice. Behav. Brain Res. 287: 2015; 15–26
- L. Hoeijmakers, P.J. Lucassen, A. Korosi. The interplay of early-life stress, nutrition, and immune activation programs adult hippocampal structure and function. Front. Mol. Neurosc. 7: 2014; 103
- S. Hong, B. Flashner, M. Chiu, E. ver Hoeve, S. Luz, S. Bhatnagar. Social isolation in adolescence alters behaviors in the forced swim and sucrose preference tests in female but not in male rats. Physiol. Behav. 105: 2012; 269–275
- Q. Huang, R. Rivest, D. Richard. Effects of leptin on corticotropin-releasing factor (CRF) synthesis and CRF neuron activation in the paraventricular hypothalamic nucleus of obese (ob/ob) mice. Endocrinology. 139: 1998; 1524–1532
- R.N. Hughes. The value of spontaneous alternation behavior (SAB) as a test of retention in pharmacological investigations of memory. Neurosci. Biobehav. Rev. 28: 2004; 497–505
- J.A. Jaques, P.H. Doleski, L.G. Castilhos, M.M. da Rosa, C. Souza Vdo, F.B. Carvalho, P. Marisco, M.L. Thorstenberg, J.F. Rezer, J.B. Ruchel, K. Coradini, R.C. Beck, M.A. Rubin, M.R. Schetinger, D.B. Leal. Free and nanoencapsulated curcumin prevents cigarette smoke-induced cognitive impairment and redox imbalance. Neurobiol. Learn. Mem. 100: 2013; 98–107
10.1016/j.nlm.2012.12.007 Google Scholar
- C.A. Jones, A.M. Brown, D.P. Auer, K.C. Fone. The mGluR2/3 agonist LY379268 reverses post-weaning social isolation-induced recognition memory deficits in the rat. Psychopharmacology (Berl.). 214: 2011; 269–283
- M.M. Kaczmarczyk, A.S. Machaj, G.S. Chiu, M.A. Lawson, S.J. Gainey, J.M. York, D.D. Meling, S.A. Martin, K.A. Kwakwa, A.F. Newman, J.A. Woods, K.W. Kelley, Y. Wang, M.J. Miller, G.G. Freund. Methylphenidate prevents high-fat diet (HFD)-induced learning/memory impairment in juvenile mice. Psychoneuroendocrinology. 38: 2013; 1553–1564
- A. Kamal, G.M. Ramakers, B. Altinbilek, M.J. Kas. Social isolation stress reduces hippocampal long-term potentiation: effect of animal strain and involvement of glucocorticoid receptors. Neuroscience. 256: 2014; 262–270
- S.E. Kanoski, R.L. Meisel, A.J. Mullins, T.L. Davidson. The effects of energy-rich diets on discrimination reversal learning and on BDNF in the hippocampus and prefrontal cortex of the rat. Behav. Brain Res. 182: 2007; 57–66
- E.I. Knudsen. Sensitive periods in the development of the brain and behavior. J. Cogn. Neurosci. 16: 2004; 1412–1425
- B. Kolb, R. Mychasiuk, A. Muhammad, Y. Li, D.O. Frost, R. Gibb. Experience and the developing prefrontal cortex. Proc. Natl. Acad. Sci. U. S. A. 109(Suppl 2): 2012; 17186–17193
- S. Kosari, E. Badoer, J.C. Nguyen, A.S. Killcross, T.A. Jenkins. Effect of western and high fat diets on memory and cholinergic measures in the rat. Behav. Brain Res. 235: 2012; 98–103
- R. Krolow, C. Noschang, S.N. Weis, L.F. Pettenuzzo, A.P. Huffell, D.M. Arcego, M. Marcolin, C.S. Mota, J. Kolling, E.B. Scherer, A.T. Wyse, C. Dalmaz. Isolation stress during the prepubertal period in rats induces long-lasting neurochemical changes in the prefrontal cortex. Neurochem. Res. 37: 2012; 1063–1073
- K. Kunisawa, N. Nakashima, M. Nagao, T. Nomura, S. Kinoshita, M. Hiramatsu. Betaine prevents homocysteine-induced memory impairment via matrix metalloproteinase-9 in the frontal cortex. Behav. Brain Res. 292: 2015; 36–43
10.1016/j.bbr.2015.06.004 Google Scholar
- F. Lante, M.C. de Jesus Ferreira, J. Guiramand, M. Recasens, M. Vignes. Low-frequency stimulation induces a new form of LTP, metabotropic glutamate (mGlu5) receptor- and PKA-dependent, in the CA1 area of the rat hippocampus. Hippocampus. 16: 2006; 345–360
- M.D. Lapiz, A. Fulford, S. Muchimapura, R. Mason, T. Parker, C.A. Marsden. Influence of postweaning social isolation in the rat on brain development, conditioned behavior, and neurotransmission. Neurosci. Behav. Physiol. 33: 2003; 13–29
- G. Laryea, M. Arnett, L.J. Muglia. Ontogeny of hypothalamic glucocorticoid receptor-mediated inhibition of the hypothalamic-pituitary-adrenal axis in mice. Stress. 2015; 1–8
- O.H. Lowry, N.J. Rosebrough, A.L. Farr, R.J. Randall. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193: 1951; 265–275
- E.M. Marco, S. Macri, G. Laviola. Critical age windows for neurodevelopmental psychiatric disorders: evidence from animal models. Neurotox. Res. 19: 2011; 286–307
- C.M. McCormick, I.Z. Mathews. HPA function in adolescence: role of sex hormones in its regulation and the enduring consequences of exposure to stressors. Pharmacol. Biochem. Behav. 86: 2007; 220–233
- B.S. McEwen. Central effects of stress hormones in health and disease: understanding the protective and damaging effects of stress and stress mediators. Eur. J. Pharmacol. 583: 2008; 174–185
- A.L. McIntosh, T.M. Ballard, L.J. Steward, P.M. Moran, K.C. Fone. The atypical antipsychotic risperidone reverses the recognition memory deficits induced by post-weaning social isolation in rats. Psychopharmacology (Berl.). 228: 2013; 31–42
10.1007/s00213-013-3011-2 Google Scholar
- A.D. McNeilly, C.A. Stewart, C. Sutherland, D.J. Balfour. High fat feeding is associated with stimulation of the hypothalamic-pituitary-adrenal axis and reduced anxiety in the rat. Psychoneuroendocrinology. 52: 2015; 272–280
- M.C. Morris, D.A. Evans, J.L. Bienias, C.C. Tangney, R.S. Wilson. Dietary fat intake and 6-year cognitive change in an older biracial community population. Neurology. 62: 2004; 1573–1579
- E.F. Naninck, L. Hoeijmakers, N. Kakava-Georgiadou, A. Meesters, S.E. Lazic, P.J. Lucassen, A. Korosi. Chronic early life stress alters developmental and adult neurogenesis and impairs cognitive function in mice. Hippocampus. 25: 2015; 309–328
- C. Noschang, R. Krolow, D.M. Arcego, D. Laureano, L.D. Fitarelli, A.P. Huffell, A.G. Ferreira, A.A. da Cunha, F.R. Machado, A.T. Wyse, C. Dalmaz. The influence of early life interventions on olfactory memory related to palatable food, and on oxidative stress parameters and Na+/K+-ATPase activity in the hippocampus and olfactory bulb of female adult rats. Neurochem. Res. 37: 2012; 1801–1810
10.1007/s11064-012-0793-2 Google Scholar
- M. Oates, B. Woodside, C.D. Walker. Chronic leptin administration in developing rats reduces stress responsiveness partly through changes in maternal behavior. Horm. Behav. 37: 2000; 366–376
- C.L. Ogden, M.D. Carroll, B.K. Kit, K.M. Flegal. Prevalence of obesity and trends in body mass index among US children and adolescents, 1999–2010. JAMA. 307: 2012; 483–490
- C.A. Oomen, H. Soeters, N. Audureau, L. Vermunt, F.N. van Hasselt, E.M. Manders, M. Joels, P.J. Lucassen, H. Krugers. Severe early life stress hampers spatial learning and neurogenesis, but improves hippocampal synaptic plasticity and emotional learning under high-stress conditions in adulthood. J. Neurosci. 30: 2010; 6635–6645
- H. Ouchi, K. Ono, Y. Murakami, K. Matsumoto. Social isolation induces deficit of latent learning performance in mice: a putative animal model of attention deficit/hyperactivity disorder. Behav. Brain Res. 238: 2013; 146–153
- A. Patapoutian, L.F. Reichardt. Trk receptors: mediators of neurotrophin action. Curr. Opin. Neurobiol. 11: 2001; 272–280
- G.W.C. Paxinos. The Rat Brain in Stereotaxic Coordinates. 1998; Academic Press: San Diego
- P. Pervanidou, G.P. Chrousos. Post-traumatic stress disorder in children and adolescents: from Sigmund Freud's trauma to psychopathology and the (Dys) metabolic syndrome. Horm. Metab. Res. 39: 2007; 413–419
- A. Petzold, L. Psotta, T. Brigadski, T. Endres, V. Lessmann. Chronic BDNF deficiency leads to an age-dependent impairment in spatial learning. Neurobiol. Learn. Mem. 120: 2015; 52–60
- M.A. Pezze, H.J. Marshall, K.C. Fone, H.J. Cassaday. Dopamine D1 receptor stimulation modulates the formation and retrieval of novel object recognition memory: role of the prelimbic cortex. Eur. Neuropsychopharmacol. 25: 2015; 2145–2156
- A. Pfefferbaum, J.E. Desmond, C. Galloway, V. Menon, G.H. Glover, E.V. Sullivan. Reorganization of frontal systems used by alcoholics for spatial working memory: an fMRI study. Neuroimage. 14: 2001; 7–20
- M.N. Quan, Y.T. Tian, K.H. Xu, T. Zhang, Z. Yang. Post weaning social isolation influences spatial cognition, prefrontal cortical synaptic plasticity and hippocampal potassium ion channels in Wistar rats. Neuroscience. 169: 2010; 214–222
- R. Rodrigo, A. Miranda-Merchak, R. Valenzuela Grau, J.P. Bachler, L. Vergara. Modulation of (Na,K)-ATPase activity by membrane fatty acid composition: therapeutic implications in human hypertension. Clin. Exp. Hypertens. 36: 2014; 17–26
10.3109/10641963.2013.783048 Google Scholar
- T.L. Roth, J.D. Sweatt. Epigenetic marking of the BDNF gene by early-life adverse experiences. Horm. Behav. 59: 2011; 315–320
- T. Sato, K. Tanaka, Y. Ohnishi, T. Teramoto, M. Irifune, T. Nishikawa. Effects of steroid hormones on (Na+, K+)-ATPase activity inhibition-induced amnesia on the step-through passive avoidance task in gonadectomized mice. Pharmacol. Res. 49: 2004; 151–159
- L.E. Sherman, J.D. Rudie, J.H. Pfeifer, C.L. Masten, K. McNealy, M. Dapretto. Development of the default mode and central executive networks across early adolescence: a longitudinal study. Dev. Cogn. Neurosci. 10: 2014; 148–159
- P.P. Silveira, A.K. Portella, S. Benetti Cda, A.I. Zugno, E.B. Scherer, C.B. Mattos, A.T. Wyse, A.B. Lucion, C. Dalmaz. Association between Na(+), K(+)-ATPase activity and the vulnerability/resilience to mood disorders induced by early life experience. Neurochem. Res. 36: 2011; 2075–2082
10.1007/s11064-011-0531-1 Google Scholar
- A.E. Takesian, T.K. Hensch. Balancing plasticity/stability across brain development. Prog. Brain Res. 207: 2013; 3–34
- L. Tapia-Arancibia, F. Rage, L. Givalois, S. Arancibia. Physiology of BDNF: focus on hypothalamic function. Front. Neuroendocrinol. 25: 2004; 77–107
- G.Z. Tau, B.S. Peterson. Normal development of brain circuits. Neuropsychopharmacology. 35: 2010; 147–168
- S. Tsakiris, G. Deliconstantinos. Influence of phosphatidylserine on (Na++K+)-stimulated ATPase and acetylcholinesterase activities of dog brain synaptosomal plasma membranes. Biochem. J. 220: 1984; 301–307
- L.M. Valentim, A.B. Geyer, A. Tavares, H. Cimarosti, P.V. Worm, R. Rodnight, C.A. Netto, C.G. Salbego. Effects of global cerebral ischemia and preconditioning on heat shock protein 27 immunocontent and phosphorylation in rat hippocampus. Neuroscience. 107: 2001; 43–49
- I. Valladolid-Acebes, P. Stucchi, V. Cano, M.S. Fernandez-Alfonso, B. Merino, M. Gil-Ortega, A. Fole, L. Morales, M. Ruiz-Gayo, N. Del Olmo. High-fat diets impair spatial learning in the radial-arm maze in mice. Neurobiol. Learn. Mem. 95: 2011; 80–85
- M.H. Vickers. Early life nutrition, epigenetics and programming of later life disease. Nutrients. 6: 2014; 2165–2178
- X.D. Wang, G. Rammes, I. Kraev, M. Wolf, C. Liebl, S.H. Scharf, C.J. Rice, W. Wurst, F. Holsboer, J.M. Deussing, T.Z. Baram, M.G. Stewart, M.B. Muller, M.V. Schmidt. Forebrain CRF(1) modulates early-life stress-programmed cognitive deficits. J. Neurosci. 31: 2011; 13625–13634
- D. Wang, J. Yan, J. Chen, W. Wu, X. Zhu, Y. Wang. Naringin improves neuronal insulin signaling, brain mitochondrial function, and cognitive function in high-Fat diet-Induced obese mice. Cell. Mol. Neurobiol. 2015
- E.C. Warburton, M.W. Brown. Neural circuitry for rat recognition memory. Behav. Brain Res. 285: 2015; 131–139
- D.J. Watson, C.A. Marsden, M.J. Millan, K.C. Fone. Blockade of dopamine D(3) but not D(2) receptors reverses the novel object discrimination impairment produced by post-weaning social isolation: implications for schizophrenia and its treatment. Int. J. Neuropsychopharmacol. 15: 2012; 471–484
- I.C. Weiss, C.R. Pryce, A.L. Jongen-Relo, N.I. Nanz-Bahr, J. Feldon. Effect of social isolation on stress-related behavioural and neuroendocrine state in the rat. Behav. Brain Res. 152: 2004; 279–295
- G. Winocur, C.E. Greenwood. Studies of the effects of high fat diets on cognitive function in a rat model. Neurobiol. Aging. 26(Suppl 1): 2005; 46–49
- A.T. Wyse, C.S. Bavaresco, E.A. Reis, A.I. Zugno, B. Tagliari, T. Calcagnotto, C.A. Netto. Training in inhibitory avoidance causes a reduction of Na+,K+-ATPase activity in rat hippocampus. Physiol. Behav. 80: 2004; 475–479
- A.T. de Souza Wyse, E.L. Streck, P. Worm, A. Wajner, F. Ritter, C.A. Netto. Preconditioning prevents the inhibition of Na+,K+-ATPase activity after brain ischemia. Neurochem. Res. 25: 2000; 971–975