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Current Neuropharmacology

Editor-in-Chief

ISSN (Print): 1570-159X
ISSN (Online): 1875-6190

Review Article

Pharmacological and Physiological Correlates of the Bidirectional Fear Phenotype of the Carioca Rats and Other Bidirectionally Selected Lines

Author(s): Yury V. Lages, Laura Balthazar, Thomas. E. Krahe and J. Landeira-Fernandez*

Volume 21, Issue 9, 2023

Published on: 18 May, 2023

Page: [1864 - 1883] Pages: 20

DOI: 10.2174/1570159X20666221012121534

Price: $65

Abstract

The Carioca rat lines originated from the selective bidirectional breeding of mates displaying extreme defense responses to contextual conditioned fear. After three generations, two distinct populations could be distinguished: the Carioca High- and Low-conditioned Freezing rats, CHF, and CLF, respectively. Later studies identified strong anxiety-like behaviors in the CHF line, while indications of impulsivity and hyperactivity were prominent in the CLF animals. The present review details the physiological and pharmacological-related findings obtained from these lines. The results discussed here point towards a dysfunctional fear circuitry in CHF rats, including alterations in key brain structures and the serotoninergic system. Moreover, data from these animals highlight important alterations in the stress-processing machinery and its associated systems, such as energy metabolism and antioxidative defense. Finally, evidence of an alteration in the dopaminergic pathway in CLF rats is also debated. Thus, accumulating data gathered over the years, place the Carioca lines as significant animal models for the study of psychiatric disorders, especially fear-related ones like anxiety.

Graphical Abstract

[1]
Jacobson, L.H.; Cryan, J.F. Genetic Approaches to Modeling Anxiety in Animals. In: Behavioral Neurobiology of Anxiety and Its Treatment; Stein, M.B.; Steckler, T., Eds.; Springer Berlin Heidelberg: Berlin, Heidelberg, 2010; pp. 161-201.
[2]
Bourin, M.; Petit-Demoulière, B.; Nic Dhonnchadha, B.; Hascöet, M. Animal models of anxiety in mice. Fundam. Clin. Pharmacol., 2007, 21(6), 567-574.
[http://dx.doi.org/10.1111/j.1472-8206.2007.00526.x] [PMID: 18034657]
[3]
World Health Organization. Depression and Other Common Mental Disorders; Geneva, 2017, p. 24.
[4]
Hall, C.S. Emotional behavior in the rat. I. Defecation and urination as measures of individual differences in emotionality. J. Comp. Psychol., 1934, 18(3), 385-403.
[http://dx.doi.org/10.1037/h0071444]
[5]
Stead, J.D.H.; Clinton, S.; Neal, C.; Schneider, J.; Jama, A.; Miller, S.; Vazquez, D.M.; Watson, S.J.; Akil, H. Selective breeding for divergence in novelty-seeking traits: heritability and enrichment in spontaneous anxiety-related behaviors. Behav. Genet., 2006, 36(5), 697-712.
[http://dx.doi.org/10.1007/s10519-006-9058-7] [PMID: 16502134]
[6]
Gomes, V.C.; Hassan, W.; Maisonnette, S.; Johnson, L.R.; Ramos, A.; Landeira-Fernandez, J. Behavioral evaluation of eight rat lines selected for high and low anxiety-related responses. Behav. Brain Res., 2013, 257(257), 39-48.
[http://dx.doi.org/10.1016/j.bbr.2013.09.028] [PMID: 24070856]
[7]
Padurariu, M.; Antioch, I.; Balmus, I.; Ciobica, A.; El-Lethey, H.S.; Kamel, M.M. Describing some behavioural animal models of anxiety and their mechanistics with special reference to oxidative stress and oxytocin relevance. Int. J. Vet. Sci. Med., 2017, 5(2), 98-104.
[http://dx.doi.org/10.1016/j.ijvsm.2017.08.003] [PMID: 30255057]
[8]
Ohl, F. Animal Models of Anxiety. In: Anxiety and Anxiolytic Drugs; Holsboer, F.; Ströhle, A., Eds.; Springer Berlin Heidelberg: Berlin, Heidelberg, 2005; pp. 35-69.
[http://dx.doi.org/10.1007/3-540-28082-0_2]
[9]
Calhoon, G.G.; Tye, K.M. Resolving the neural circuits of anxiety. Nat. Neurosci., 2015, 18(10), 1394-1404.
[http://dx.doi.org/10.1038/nn.4101] [PMID: 26404714]
[10]
File, S.E. Behavioral detection of anxiolytic action. Experimental Approaches to Anxiety and Depression; Elliot, J.M.; Heal, D.J.; Mardsen, C.A., Eds.; John Wiley: Chichester, 1992, pp. 25-44.
[11]
Perez, J.A.; Clinton, S.M.; Turner, C.A.; Watson, S.J.; Akil, H. A new role for FGF2 as an endogenous inhibitor of anxiety. J. Neurosci., 2009, 29(19), 6379-6387.
[http://dx.doi.org/10.1523/JNEUROSCI.4829-08.2009] [PMID: 19439615]
[12]
Prater, K.E.; Aurbach, E.L.; Larcinese, H.K.; Smith, T.N.; Turner, C.A.; Blandino, P.; Watson, S.J.; Maren, S.; Akil, H. Selectively bred rats provide a unique model of vulnerability to PTSD-Like behavior and respond differentially to FGF2 augmentation early in life. Neuropsychopharmacology, 2017, 42(8), 1706-1714.
[http://dx.doi.org/10.1038/npp.2017.37] [PMID: 28205604]
[13]
Fanselow, M.S. Neural organization of the defensive behavior system responsible for fear. Psychon. Bull. Rev., 1994, 1(4), 429-438.
[http://dx.doi.org/10.3758/BF03210947] [PMID: 24203551]
[14]
Gray, J.A.; McNaughton, N. The Neuropsychology of Anxiety: An Enquiry into the Function of the Septo-Hippocampal System; Oxford University Press: New York, 2000.
[15]
Lee, Y.; Davis, M. Role of the hippocampus, the bed nucleus of the stria terminalis, and the amygdala in the excitatory effect of corticotropin-releasing hormone on the acoustic startle reflex. J. Neurosci., 1997, 17(16), 6434-6446.
[http://dx.doi.org/10.1523/JNEUROSCI.17-16-06434.1997] [PMID: 9236251]
[16]
Walker, D.L.; Davis, M. Double dissociation between the involvement of the bed nucleus of the stria terminalis and the central nucleus of the amygdala in startle increases produced by conditioned versus unconditioned fear. J. Neurosci., 1997, 17(23), 9375-9383.
[http://dx.doi.org/10.1523/JNEUROSCI.17-23-09375.1997] [PMID: 9364083]
[17]
Davis, M.; Walker, D.L.; Lee, Y. Roles of the amygdala and bed nucleus of the stria terminalis in fear and anxiety measured with the acoustic startle reflex. Possible relevance to PTSD. Ann. N. Y. Acad. Sci., 1997, 821(1 Psychobiology), 305-331.
[http://dx.doi.org/10.1111/j.1749-6632.1997.tb48289.x] [PMID: 9238214]
[18]
Campos, A.C.; Fogaça, M.V.; Aguiar, D.C.; Guimarães, F.S. Animal models of anxiety disorders and stress. Br. J. Psychiatry, 2013, 35(Suppl. 2), S101-S111.
[http://dx.doi.org/10.1590/1516-4446-2013-1139] [PMID: 24271222]
[19]
Fanselow, M.S.; Wassum, K.M. The origins and organization of vertebrate pavlovian conditioning. Cold Spring Harb. Perspect. Biol., 2016, 8(1), a021717.
[http://dx.doi.org/10.1101/cshperspect.a021717] [PMID: 26552417]
[20]
Landeira-Fernandez, J. Context and Pavlovian conditioning. Braz. J. Med. Biol. Res., 1996, 29(2), 149-173.
[PMID: 8731345]
[21]
de Castro Gomes, V.; Landeira-Fernandez, J. Amygdaloid lesions produced similar contextual fear conditioning disruption in the Carioca high- and low-conditioned freezing rats. Brain Res., 2008, 1233, 137-145.
[http://dx.doi.org/10.1016/j.brainres.2008.07.044] [PMID: 18691560]
[22]
Gomes, V.C.; Silva, C.E.B.; Landeira-Fernandez, J. The carioca high and low conditioned freezing lines: a new animal model of generalized anxiety disorder. In: Anxiety Disorders; Kalinin, V., Ed.; IntechOpen, 2011.
[23]
Lages, Y.V.; Maisonnette, S.S.; Rosseti, F.P.; Landeira-Fernandez, J. Acquisition and extinction of contextual fear conditioning in Carioca high- and low-conditioned freezing rats. Learn. Motiv., 2021, 75, 101744.
[http://dx.doi.org/10.1016/j.lmot.2021.101744]
[24]
Macêdo-Souza, C.; Maisonnette, S.S.; Filgueiras, C.C.; Landeira-Fernandez, J.; Krahe, T.E. Cued fear conditioning in Carioca High- and Low-conditioned Freezing rats. Front. Behav. Neurosci., 2020, 13, 285.
[http://dx.doi.org/10.3389/fnbeh.2019.00285] [PMID: 32038188]
[25]
Cavaliere, D.R.; Maisonnette, S.; Krahe, T.E.; Landeira-Fernandez, J.; Cruz, A.P.M. High- and Low-conditioned Behavioral effects of midazolam in Carioca high- and low-conditioned freezing rats in an ethologically based test. Neurosci. Lett., 2020, 715, 134632.
[http://dx.doi.org/10.1016/j.neulet.2019.134632] [PMID: 31790719]
[26]
Lages, Y.V.; Maisonnette, S.S.; Rosseti, F.P.; Krahe, T.E.; Landeira-Fernandez, J. High-sugar/high-fat diet modulates the effects of chronic stress in cariocas high- and low-conditioned freezing rats. Physiol. Behav., 2022, 248, 113742.
[http://dx.doi.org/10.1016/j.physbeh.2022.113742] [PMID: 35172192]
[27]
Willner, P. The validity of animal models of depression. Psychopharmacology (Berl.), 1984, 83(1), 1-16.
[http://dx.doi.org/10.1007/BF00427414] [PMID: 6429692]
[28]
Lydiard, R.B. The role of GABA in anxiety disorders. J. Clin. Psychiatry, 2003, 64(Suppl. 3), 21-27.
[PMID: 12662130]
[29]
Bandelow, B.; Michaelis, S.; Wedekind, D. Treatment of anxiety disorders. Dialogues Clin. Neurosci., 2017, 19(2), 93-107.
[http://dx.doi.org/10.31887/DCNS.2017.19.2/bbandelow] [PMID: 28867934]
[30]
Sigel, E.; Ernst, M. The benzodiazepine binding sites of GABAA receptors. Trends Pharmacol. Sci., 2018, 39(7), 659-671.
[http://dx.doi.org/10.1016/j.tips.2018.03.006] [PMID: 29716746]
[31]
Kumar, V.; Bhat, Z.A.; Kumar, D. Animal models of anxiety: A comprehensive review. J. Pharmacol. Toxicol. Methods, 2013, 68(2), 175-183.
[http://dx.doi.org/10.1016/j.vascn.2013.05.003] [PMID: 23684951]
[32]
León, L.A.; Castro-Gomes, V.; Zárate-Guerrero, S.; Corredor, K.; Mello Cruz, A.P.; Brandão, M.L.; Cardenas, F.P.; Landeira-Fernandez, J. Behavioral effects of systemic, infralimbic and prelimbic injections of a serotonin 5-HT2A antagonist in Carioca high- and low-conditioned freezing rats. Front. Behav. Neurosci., 2017, 11, 117.
[http://dx.doi.org/10.3389/fnbeh.2017.00117] [PMID: 28736518]
[33]
Dias, G.P.; Bevilaqua, M.C.N.; Silveira, A.C.D.; Landeira-Fernandez, J.; Gardino, P.F. Behavioral profile and dorsal hippocampal cells in Carioca high-conditioned freezing rats. Behav. Brain Res., 2009, 205(2), 342-348.
[http://dx.doi.org/10.1016/j.bbr.2009.06.038] [PMID: 19583984]
[34]
Hassan, W.; de Castro Gomes, V.; Pinton, S.; Batista Teixeira da Rocha, J.; Landeira-Fernandez, J. Association between oxidative stress and contextual fear conditioning in Carioca high- and low-conditioned freezing rats. Brain Res., 2013, 1512, 60-67.
[http://dx.doi.org/10.1016/j.brainres.2013.03.039] [PMID: 23566816]
[35]
Salviano, M.; Ferreira, G.; Greidinger, M.; Couto, K.; Landeira-Fernandez, J.; Cruz, A. Behavioral evaluation of male and female carioca high-and low-freezing rats. Trends Psychol., 2014, 22, 663-675.
[36]
Prut, L.; Belzung, C. The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Eur. J. Pharmacol., 2003, 463(1-3), 3-33.
[http://dx.doi.org/10.1016/S0014-2999(03)01272-X] [PMID: 12600700]
[37]
Lages, Y.V.; Maisonnette, S.S.; Marinho, B.; Rosseti, F.P.; Krahe, T.E.; Landeira-Fernandez, J. Behavioral effects of chronic stress in Carioca high- and low-conditioned freezing rats. Stress, 2021, 24(5), 602-611.
[http://dx.doi.org/10.1080/10253890.2021.1934445] [PMID: 34030584]
[38]
Goulart, V.G.; Rocha-Mendonça, H.; Maisonnette, S.; Pandolfo, P.; Landeira-Fernandez, J.; Campello-Costa, P. Differential expression of glutamatergic receptor subunits in the hippocampus in carioca high- and low-conditioned freezing rats. Mol. Cell. Neurosci., 2021, 116, 103666.
[http://dx.doi.org/10.1016/j.mcn.2021.103666] [PMID: 34464708]
[39]
Bignami, G. Selection for high rates and low rates of avoidance conditioning in the rat. Anim. Behav., 1965, 13(2-3), 221-227.
[http://dx.doi.org/10.1016/0003-3472(65)90038-2] [PMID: 5835838]
[40]
Driscoll, P.; Ferré, P.; Fernández-Teruel, A.; Tobeña, A.; Escorihuela, R.M.; Levi de Stein, M.; Wolfman, C.; Medina, J. Effects of prenatal diazepam on two-way avoidance behavior, swimming navigation and brain levels of benzodiazepine-like molecules in male roman high- and low-avoidance rats. Psychopharmacology (Berl.), 1995, 122(1), 51-57.
[http://dx.doi.org/10.1007/BF02246441] [PMID: 8711064]
[41]
Gentsch, C.; Lichtsteiner, M.; Feer, H. 3H-Diazepam binding sites in roman high- and low-avoidance rats. Experientia, 1981, 37(12), 1315-1316.
[http://dx.doi.org/10.1007/BF01948382] [PMID: 6276220]
[42]
Bentareha, R.; Araujo, F.; Ruano, D.; Driscoll, P.; Escorihuela, R.M.; Tobeña, A.; Fernández-Teruel, A.; Vitorica, J. Pharmacological properties of the GABAA receptor complex from brain regions of (hypoemotional) Roman high- and (hyperemotional) low-avoidance rats. Eur. J. Pharmacol., 1998, 354(1), 91-97.
[http://dx.doi.org/10.1016/S0014-2999(98)00428-2] [PMID: 9726635]
[43]
Liebsch, G.; Montkowski, A.; Holsboer, F.; Landgraf, R. Behavioural profiles of two Wistar rat lines selectively bred for high or low anxiety-related behaviour. Behav. Brain Res., 1998, 94(2), 301-310.
[http://dx.doi.org/10.1016/S0166-4328(97)00198-8] [PMID: 9722280]
[44]
Liebsch, G.; Linthorst, A.C.; Neumann, I.D.; Reul, J.M.; Holsboer, F.; Landgraf, R. Behavioral, physiological, and neuroendocrine stress responses and differential sensitivity to diazepam in two Wistar rat lines selectively bred for high- and low-anxiety-related behavior. Neuropsychopharmacology, 1998, 19(5), 381-396.
[http://dx.doi.org/10.1016/S0893-133X(98)00042-6] [PMID: 9778660]
[45]
Beiderbeck, D.I.; Lukas, M.; Neumann, I.D. Anti-aggressive effects of neuropeptide S independent of anxiolysis in male rats. Front. Behav. Neurosci., 2014, 8, 185.
[http://dx.doi.org/10.3389/fnbeh.2014.00185] [PMID: 24910598]
[46]
Jochum, T.; Boettger, M.; Wigger, A.; Beiderbeck, D.; Neumann, I.; Landgraf, R.; Sauer, H.; Bär, K. Decreased sensitivity to thermal pain in rats bred for high anxiety-related behaviour is attenuated by citalopram or diazepam treatment. Behav. Brain Res., 2007, 183(1), 18-24.
[http://dx.doi.org/10.1016/j.bbr.2007.05.022] [PMID: 17599477]
[47]
Hermann, B.; Landgraf, R.; Keck, M.E.; Wigger, A.; Morrow, A.L.; Ströhle, A.; Holsboer, F.; Rupprecht, R. Pharmacological characterisation of cortical gamma-aminobutyric acid type A (GABAA) receptors in two Wistar rat lines selectively bred for high and low anxiety-related behaviour. World J. Biol. Psychiatry, 2000, 1(3), 137-143.
[http://dx.doi.org/10.3109/15622970009150581] [PMID: 12607222]
[48]
Krystal, J.H.; Stossel, S.; Krystal, A.D. Restricting Benzodiazepines to Short-Term Prescription. JAMA Psychiatry, 2015, 72(7), 734-735.
[http://dx.doi.org/10.1001/jamapsychiatry.2015.0351] [PMID: 25923129]
[49]
Olfson, M.; King, M.; Schoenbaum, M. Benzodiazepine Use in the United States. JAMA Psychiatry, 2015, 72(2), 136-142.
[http://dx.doi.org/10.1001/jamapsychiatry.2014.1763] [PMID: 25517224]
[50]
Fenton, M.C. Keyes, K. M.; Martins, S. S.; Hasin, D. S. Role of a Prescription in Anxiety Medication Use, Abuse, and Dependence., 2010, 167(10), 1247-1253.
[51]
Rickels, K.; Schweizer, E.; Case, W.G.; Greenblatt, D.J. Long-term therapeutic use of benzodiazepines. I. Effects of abrupt discontinuation. Arch. Gen. Psychiatry, 1990, 47(10), 899-907.
[http://dx.doi.org/10.1001/archpsyc.1990.01810220015002] [PMID: 2222129]
[52]
Gray, S.L.; Dublin, S.; Yu, O.; Walker, R.; Anderson, M.; Hubbard, R.A.; Crane, P.K.; Larson, E.B. Benzodiazepine use and risk of incident dementia or cognitive decline: prospective population based study. BMJ, 2016, 352, i90.
[http://dx.doi.org/10.1136/bmj.i90] [PMID: 26837813]
[53]
Pollack, M.H.; Van Ameringen, M.; Simon, N.M.; Worthington, J.W.; Hoge, E.A.; Keshaviah, A.; Stein, M.B. A double-blind randomized controlled trial of augmentation and switch strategies for refractory social anxiety disorder. Am. J. Psychiatry, 2014, 171(1), 44-53.
[http://dx.doi.org/10.1176/appi.ajp.2013.12101353] [PMID: 24399428]
[54]
Villas-Boas, G.R.; Lavorato, S.N.; Paes, M.M.; de Carvalho, P.M.G.; Rescia, V.C.; Cunha, M.S.; de Magalhães-Filho, M.F.; Ponsoni, L.F.; de Carvalho, A.A.V.; de Lacerda, R.B. da S Leite, L.; da S Tavares-Henriques, M.; Lopes, L.A.F.; Oliveira, L.G.R.; Silva-Filho, S.E.; da Silveira, A.P.S.; Cuman, R.K.N.; de S Silva-Comar, F.M.; Comar, J.F.; do A Brasileiro, L.; Dos Santos, J.N.; de Freitas, W.R.; Leão, K.V.; da Silva, J.G.; Klein, R.C.; Klein, M.H.F.; da S Ramos, B.H.; Fernandes, C.K.C.; de L Ribas, D.G.; Oesterreich, S.A. Modulation of the serotonergic receptosome in the treatment of anxiety and depression: a narrative review of the experimental evidence. Pharmaceuticals (Basel), 2021, 14(2), 148.
[http://dx.doi.org/10.3390/ph14020148] [PMID: 33673205]
[55]
Goodwin, G.M. Revisiting treatment options for depressed patients with generalised anxiety disorder. Adv. Ther., 2021, 38(S2)(Suppl. 2), 61-68.
[http://dx.doi.org/10.1007/s12325-021-01861-0] [PMID: 34417993]
[56]
Hillhouse, T.M.; Porter, J.H. A brief history of the development of antidepressant drugs: From monoamines to glutamate. Exp. Clin. Psychopharmacol., 2015, 23(1), 1-21.
[http://dx.doi.org/10.1037/a0038550] [PMID: 25643025]
[57]
Johansen, J.P.; Tarpley, J.W.; LeDoux, J.E.; Blair, H.T. Neural substrates for expectation-modulated fear learning in the amygdala and periaqueductal gray. Nat. Neurosci., 2010, 13(8), 979-986.
[http://dx.doi.org/10.1038/nn.2594] [PMID: 20601946]
[58]
Grahn, R.E.; Will, M.J.; Hammack, S.E.; Maswood, S.; McQueen, M.B.; Watkins, L.R.; Maier, S.F. Activation of serotonin-immunoreactive cells in the dorsal raphe nucleus in rats exposed to an uncontrollable stressor. Brain Res., 1999, 826(1), 35-43.
[http://dx.doi.org/10.1016/S0006-8993(99)01208-1] [PMID: 10216194]
[59]
Ressler, K.J.; Nemeroff, C.B. Role of serotonergic and noradrenergic systems in the pathophysiology of depression and anxiety disorders. Depress. Anxiety, 2000, 12(S1)(Suppl. 1), 2-19.
[http://dx.doi.org/10.1002/1520-6394(2000)12:1+<2:AID-DA2>3.0.CO;2-4] [PMID: 11098410]
[60]
Hale, M.W.; Shekhar, A.; Lowry, C.A. Stress-related serotonergic systems: implications for symptomatology of anxiety and affective disorders. Cell. Mol. Neurobiol., 2012, 32(5), 695-708.
[http://dx.doi.org/10.1007/s10571-012-9827-1] [PMID: 22484834]
[61]
Maswood, S.; Barter, J.E.; Watkins, L.R.; Maier, S.F. Exposure to inescapable but not escapable shock increases extracellular levels of 5-HT in the dorsal raphe nucleus of the rat. Brain Res., 1998, 783(1), 115-120.
[http://dx.doi.org/10.1016/S0006-8993(97)01313-9] [PMID: 9479059]
[62]
Marcinkiewcz, C.A.; Mazzone, C.M.; D’Agostino, G.; Halladay, L.R.; Hardaway, J.A.; DiBerto, J.F.; Navarro, M.; Burnham, N.; Cristiano, C.; Dorrier, C.E.; Tipton, G.J.; Ramakrishnan, C.; Kozicz, T.; Deisseroth, K.; Thiele, T.E.; McElligott, Z.A.; Holmes, A.; Heisler, L.K.; Kash, T.L. Serotonin engages an anxiety and fear-promoting circuit in the extended amygdala. Nature, 2016, 537(7618), 97-101.
[http://dx.doi.org/10.1038/nature19318] [PMID: 27556938]
[63]
Mongeau, R.; Martin, C.B.P.; Chevarin, C.; Maldonado, R.; Hamon, M.; Robledo, P.; Lanfumey, L. 5-HT2C receptor activation prevents stress-induced enhancement of brain 5-HT turnover and extracellular levels in the mouse brain: modulation by chronic paroxetine treatment. J. Neurochem., 2010, 115(2), 438-449.
[http://dx.doi.org/10.1111/j.1471-4159.2010.06932.x] [PMID: 20796171]
[64]
Meyer, J.H.; Kapur, S.; Eisfeld, B.; Brown, G.M.; Houle, S.; DaSilva, J.; Wilson, A.A.; Rafi-Tari, S.; Mayberg, H.S.; Kennedy, S.H. The effect of paroxetine on 5-HT(2A) receptors in depression: an [(18)F]setoperone PET imaging study. Am. J. Psychiatry, 2001, 158(1), 78-85.
[http://dx.doi.org/10.1176/appi.ajp.158.1.78] [PMID: 11136637]
[65]
Szabo, S.T.; de Montigny, C.; Blier, P. Progressive attenuation of the firing activity of locus coeruleus noradrenergic neurons by sustained administration of selective serotonin reuptake inhibitors. Int. J. Neuropsychopharmacol., 2000, 3(1), S1461145700001772.
[http://dx.doi.org/10.1017/S1461145700001772] [PMID: 11343573]
[66]
Dremencov, E.; El Mansari, M.; Blier, P. Effects of sustained serotonin reuptake inhibition on the firing of dopamine neurons in the rat ventral tegmental area. J. Psychiatry Neurosci., 2009, 34(3), 223-229.
[PMID: 19448853]
[67]
Likhtik, E.; Stujenske, J.M.A.; Topiwala, M.; Harris, A.Z.; Gordon, J.A. Prefrontal entrainment of amygdala activity signals safety in learned fear and innate anxiety. Nat. Neurosci., 2014, 17(1), 106-113.
[http://dx.doi.org/10.1038/nn.3582] [PMID: 24241397]
[68]
McDonald, A.J. Cortical pathways to the mammalian amygdala. Prog. Neurobiol., 1998, 55(3), 257-332.
[http://dx.doi.org/10.1016/S0301-0082(98)00003-3] [PMID: 9643556]
[69]
Vertes, R.P. Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse, 2004, 51(1), 32-58.
[http://dx.doi.org/10.1002/syn.10279] [PMID: 14579424]
[70]
Quirk, G.J.; Russo, G.K.; Barron, J.L.; Lebron, K. The role of ventromedial prefrontal cortex in the recovery of extinguished fear. J. Neurosci., 2000, 20(16), 6225-6231.
[http://dx.doi.org/10.1523/JNEUROSCI.20-16-06225.2000] [PMID: 10934272]
[71]
Laurent, V.; Westbrook, R.F. Inactivation of the infralimbic but not the prelimbic cortex impairs consolidation and retrieval of fear extinction. Learn. Mem., 2009, 16(9), 520-529.
[http://dx.doi.org/10.1101/lm.1474609] [PMID: 19706835]
[72]
Corcoran, K.A.; Quirk, G.J. Activity in prelimbic cortex is necessary for the expression of learned, but not innate, fears. J. Neurosci., 2007, 27(4), 840-844.
[http://dx.doi.org/10.1523/JNEUROSCI.5327-06.2007] [PMID: 17251424]
[73]
Umriukhin, A.E.; Wigger, A.; Singewald, N.; Landgraf, R. Hypothalamic and hippocampal release of serotonin in rats bred for hyper- or hypo-anxiety. Stress, 2002, 5(4), 299-305.
[http://dx.doi.org/10.1080/1025389021000061200] [PMID: 12475735]
[74]
Keck, M.E.; Sartori, S.B.; Welt, T.; Müller, M.B.; Ohl, F.; Holsboer, F.; Landgraf, R.; Singewald, N. Differences in serotonergic neurotransmission between rats displaying high or low anxiety/depression-like behaviour: effects of chronic paroxetine treatment. J. Neurochem., 2005, 92(5), 1170-1179.
[http://dx.doi.org/10.1111/j.1471-4159.2004.02953.x] [PMID: 15715667]
[75]
Kulikov, A.; Castanon, N.; Mormède, P.; Chaouloff, F. Cerebral tryptophan hydroxylase activity, and 5-HT1A receptor, 5-HT2A receptor, and 5-HT transporter binding in grouped and isolated Roman RHA and RLA rats: relationships with behaviours in two models of anxiety. Psychopharmacology (Berl.), 1995, 121(3), 385-395.
[http://dx.doi.org/10.1007/BF02246079] [PMID: 8584622]
[76]
Visser, A.K.D.; Ettrup, A.; Klein, A.B.; van Waarde, A.; Bosker, F.J.; Meerlo, P.; Knudsen, G.M.; de Boer, S.F. Similar serotonin-2A receptor binding in rats with different coping styles or levels of aggression. Synapse, 2015, 69(4), 226-232.
[http://dx.doi.org/10.1002/syn.21810] [PMID: 25684736]
[77]
Fomsgaard, L.; Moreno, J.L.; de la Fuente Revenga, M.; Brudek, T.; Adamsen, D.; Rio-Alamos, C.; Saunders, J.; Klein, A.B.; Oliveras, I.; Cañete, T.; Blazquez, G.; Tobeña, A.; Fernandez-Teruel, A.; Gonzalez-Maeso, J.; Aznar, S. Differences in 5-HT2A and mGlu2 receptor expression levels and repressive epigenetic modifications at the 5-HT2A promoter region in the roman low- (RLA-I) and high- (RHA-I) avoidance rat strains. Mol. Neurobiol., 2018, 55(3), 1998-2012.
[http://dx.doi.org/10.1007/s12035-017-0457-y] [PMID: 28265857]
[78]
Liang, F.; Feng, R.; Gu, S.; Jiang, S.; Zhang, X.; Li, N.; Xu, M.; Tang, Y.; Wang, F. Neurotransmitters and electrophysiological changes might work as biomarkers for diagnosing affective disorders. Dis. Markers, 2021, 2021, 1-12.
[http://dx.doi.org/10.1155/2021/9116502] [PMID: 34589159]
[79]
de Almeida Silva, M.; de Toledo, T.S.; de Figueiredo, R.M.; Leite-Panissi, C.R.A.; Huston, J.P.; Coimbra, N.C.; Mattern, C.; de Carvalho, M.C. The activation of D2-like receptors by intranasal dopamine facilitates the extinction of contextual fear and prevents conditioned fear-induced antinociception. Behav. Brain Res., 2022, 417, 113611.
[http://dx.doi.org/10.1016/j.bbr.2021.113611] [PMID: 34592376]
[80]
Sagvolden, T.; Pettersen, M.B.; Larsen, M.C. Spontaneously hypertensive rats (SHR) as a putative animal model of childhood hyperkinesis: SHR behavior compared to four other rat strains. Physiol. Behav., 1993, 54(6), 1047-1055.
[http://dx.doi.org/10.1016/0031-9384(93)90323-8] [PMID: 8295939]
[81]
Lago, T.; Davis, A.; Grillon, C.; Ernst, M. Striatum on the anxiety map: small detours into adolescence. Brain Res., 2017, 1654(Pt B), 177-184.
[http://dx.doi.org/10.1016/j.brainres.2016.06.006] [PMID: 27276526]
[82]
Ernst, M.; Zametkin, A.J.; Matochik, J.A.; Pascualvaca, D.; Jons, P.H.; Cohen, R.M. High midbrain [18F]DOPA accumulation in children with attention deficit hyperactivity disorder. Am. J. Psychiatry, 1999, 156(8), 1209-1215.
[http://dx.doi.org/10.1176/ajp.156.8.1209] [PMID: 10450262]
[83]
Ernst, M.; Lago, T.; Davis, A.; Grillon, C. The effects of methylphenidate and propranolol on the interplay between induced-anxiety and working memory. Psychopharmacology (Berl.), 2016, 233(19-20), 3565-3574.
[http://dx.doi.org/10.1007/s00213-016-4390-y] [PMID: 27492789]
[84]
Lages, Y.V.; Maisonnette, S.S.; Rosseti, F.P.; Galvão, B.O.; Landeira-Fernandez, J. Haloperidol and methylphenidate alter motor behavior and responses to conditioned fear of Carioca Low-conditioned Freezing rats. Pharmacol. Biochem. Behav., 2021, 211, 173296.
[http://dx.doi.org/10.1016/j.pbb.2021.173296] [PMID: 34752797]
[85]
World Health Organization model list of essential medicines: 21st list 2019; World Health Organization: Geneva, 2019.
[86]
Stevens, T.; Sangkuhl, K.; Brown, J.T.; Altman, R.B.; Klein, T.E. PharmGKB summary. Pharmacogenet. Genomics, 2019, 29(6), 136-154.
[http://dx.doi.org/10.1097/FPC.0000000000000376] [PMID: 30950912]
[87]
Drerup, J.M.; Hayashi, K.; Cui, H.; Mettlach, G.L.; Long, M.A.; Marvin, M.; Sun, X.; Goldberg, M.S.; Lutter, M.; Bibb, J.A. Attention-deficit/hyperactivity phenotype in mice lacking the cyclin-dependent kinase 5 cofactor p35. Biol. Psychiatry, 2010, 68(12), 1163-1171.
[http://dx.doi.org/10.1016/j.biopsych.2010.07.016] [PMID: 20832057]
[88]
Fernández, G.; Krapacher, F.; Ferreras, S.; Quassollo, G.; Mari, M.M.; Pisano, M.V.; Montemerlo, A.; Rubianes, M.D.; Bregonzio, C.; Arias, C.; Paglini, M.G. Lack of Cdk5 activity is involved on dopamine transporter expression and function: Evidences from an animal model of attention-deficit hyperactivity disorder. Exp. Neurol., 2021, 346, 113866.
[http://dx.doi.org/10.1016/j.expneurol.2021.113866] [PMID: 34537209]
[89]
Krapacher, F.A.; Mlewski, E.C.; Ferreras, S.; Pisano, V.; Paolorossi, M.; Hansen, C.; Paglini, G. Mice lacking p35 display hyperactivity and paradoxical response to psychostimulants. J. Neurochem., 2010, 114(1) no.
[http://dx.doi.org/10.1111/j.1471-4159.2010.06748.x] [PMID: 20403084]
[90]
Fan, X.; Xu, M.; Hess, E.J. D2 dopamine receptor subtype-mediated hyperactivity and amphetamine responses in a model of ADHD. Neurobiol. Dis., 2010, 37(1), 228-236.
[http://dx.doi.org/10.1016/j.nbd.2009.10.009] [PMID: 19840852]
[91]
Ruocco, L.A.; de Souza Silva, M.A.; Topic, B.; Mattern, C.; Huston, J.P.; Sadile, A.G. Intranasal application of dopamine reduces activity and improves attention in Naples High Excitability rats that feature the mesocortical variant of ADHD. Eur. Neuropsychopharmacol., 2009, 19(10), 693-701.
[http://dx.doi.org/10.1016/j.euroneuro.2009.02.005] [PMID: 19328660]
[92]
Leffa, D.T.; Panzenhagen, A.C.; Salvi, A.A.; Bau, C.H.D.; Pires, G.N.; Torres, I.L.S.; Rohde, L.A.; Rovaris, D.L.; Grevet, E.H. Systematic review and meta-analysis of the behavioral effects of methylphenidate in the spontaneously hypertensive rat model of attention-deficit/hyperactivity disorder. Neurosci. Biobehav. Rev., 2019, 100, 166-179.
[http://dx.doi.org/10.1016/j.neubiorev.2019.02.019] [PMID: 30826386]
[93]
Leo, D.; Sorrentino, E.; Volpicelli, F.; Eyman, M.; Greco, D.; Viggiano, D.; di Porzio, U.; Perrone-Capano, C. Altered midbrain dopaminergic neurotransmission during development in an animal model of ADHD. Neurosci. Biobehav. Rev., 2003, 27(7), 661-669.
[http://dx.doi.org/10.1016/j.neubiorev.2003.08.009] [PMID: 14624810]
[94]
Perusini, J.N.; Fanselow, M.S. Neurobehavioral perspectives on the distinction between fear and anxiety. Learn. Mem., 2015, 22(9), 417-425.
[http://dx.doi.org/10.1101/lm.039180.115] [PMID: 26286652]
[95]
Maren, S.; Phan, K.L.; Liberzon, I. The contextual brain: implications for fear conditioning, extinction and psychopathology. Nat. Rev. Neurosci., 2013, 14(6), 417-428.
[http://dx.doi.org/10.1038/nrn3492] [PMID: 23635870]
[96]
Galvão, B.O.; Gomes, V.C.; Maisonnette, S.; Landeira-Fernandez, J. Panic-like behaviors in Carioca high-and low-conditioned freezing rats. Psychol. Neurosci., 2011, 4(2), 205-210.
[http://dx.doi.org/10.3922/j.psns.2011.2.005]
[97]
Brandão, M.L.; De Aguiar, J.C.; Graeff, F.G. GABA mediation of the anti-aversive action of minor tranquilizers. Pharmacol. Biochem. Behav., 1982, 16(3), 397-402.
[http://dx.doi.org/10.1016/0091-3057(82)90441-5] [PMID: 6123116]
[98]
Oliveira, L.C.; Nobre, M.J.; Brandão, M.L.; Landeira-Fernández, J. Role of amygdala in conditioned and unconditioned fear generated in the periaqueductal gray. Neuroreport, 2004, 15(14), 2281-2285.
[http://dx.doi.org/10.1097/00001756-200410050-00028] [PMID: 15371750]
[99]
Ruiz Martinez, R.C.; Ribeiro de Oliveira, A.; Brandão, M.L. Conditioned and unconditioned fear organized in the periaqueductal gray are differentially sensitive to injections of muscimol into amygdaloid nuclei. Neurobiol. Learn. Mem., 2006, 85(1), 58-65.
[http://dx.doi.org/10.1016/j.nlm.2005.08.007] [PMID: 16198609]
[100]
de Carvalho, M.R.; Dias, G.P.; Cosci, F.; de-Melo-Neto, V.L.; Bevilaqua, M.C.N.; Gardino, P.F.; Nardi, A.E. Current findings of fMRI in panic disorder: contributions for the fear neurocircuitry and CBT effects. Expert Rev. Neurother., 2010, 10(2), 291-303.
[http://dx.doi.org/10.1586/ern.09.161] [PMID: 20136384]
[101]
Mobbs, D.; Marchant, J.L.; Hassabis, D.; Seymour, B.; Tan, G.; Gray, M.; Petrovic, P.; Dolan, R.J.; Frith, C.D. From threat to fear: the neural organization of defensive fear systems in humans. J. Neurosci., 2009, 29(39), 12236-12243.
[http://dx.doi.org/10.1523/JNEUROSCI.2378-09.2009] [PMID: 19793982]
[102]
Kim, E.J.; Horovitz, O.; Pellman, B.A.; Tan, L.M.; Li, Q.; Richter-Levin, G.; Kim, J.J. Dorsal periaqueductal gray-amygdala pathway conveys both innate and learned fear responses in rats. Proc. Natl. Acad. Sci. USA, 2013, 110(36), 14795-14800.
[http://dx.doi.org/10.1073/pnas.1310845110] [PMID: 23959880]
[103]
Adolphs, R. The biology of fear. Curr. Biol., 2013, 23(2), R79-R93.
[http://dx.doi.org/10.1016/j.cub.2012.11.055] [PMID: 23347946]
[104]
Gómez, M.J.; Morón, I.; Torres, C.; Esteban, F.J.; de la Torre, L.; Cándido, A.; Maldonado, A.; Fernández-Teruel, A.; Tobeña, A.; Escarabajal, M.D. One-way avoidance acquisition and cellular density in the basolateral amygdala: Strain differences in Roman high- and low-avoidance rats. Neurosci. Lett., 2009, 450(3), 317-320.
[http://dx.doi.org/10.1016/j.neulet.2008.10.112] [PMID: 19056466]
[105]
Río-Álamos, C.; Piludu, M.A.; Gerbolés, C.; Barroso, D.; Oliveras, I.; Sánchez-González, A.; Cañete, T.; Tapias-Espinosa, C.; Sampedro-Viana, D.; Torrubia, R.; Tobeña, A.; Fernández-Teruel, A. Volumetric brain differences between the Roman rat strains: Neonatal handling effects, sensorimotor gating and working memory. Behav. Brain Res., 2019, 361, 74-85.
[http://dx.doi.org/10.1016/j.bbr.2018.12.033] [PMID: 30576720]
[106]
Río-Álamos, C.; Oliveras, I.; Piludu, M.A.; Gerbolés, C.; Cañete, T.; Blázquez, G.; Lope-Piedrafita, S.; Martínez-Membrives, E.; Torrubia, R.; Tobeña, A.; Fernández-Teruel, A. Neonatal handling enduringly decreases anxiety and stress responses and reduces hippocampus and amygdala volume in a genetic model of differential anxiety: Behavioral-volumetric associations in the Roman rat strains. Eur. Neuropsychopharmacol., 2017, 27(2), 146-158.
[http://dx.doi.org/10.1016/j.euroneuro.2016.12.003] [PMID: 28049558]
[107]
Morón, I.; Gómez, M.J.; Escarabajal, M.D.; de la Torre, L.; Cándido, A.; Maldonado, A.; Tobeña, A.; Fernández-Teruel, A.; Torres, C. One-way avoidance learning in female inbred Roman high- and low-avoidance rats: Effects of bilateral electrolytic central amygdala lesions. Neurosci. Lett., 2010, 474(1), 32-36.
[http://dx.doi.org/10.1016/j.neulet.2010.03.001] [PMID: 20211695]
[108]
McDonald, J.W.; Johnston, M.V. Physiological and pathophysiological roles of excitatory amino acids during central nervous system development. Brain Res. Brain Res. Rev., 1990, 15(1), 41-70.
[http://dx.doi.org/10.1016/0165-0173(90)90011-C] [PMID: 2163714]
[109]
Riaza Bermudo-Soriano, C.; Perez-Rodriguez, M.M.; Vaquero-Lorenzo, C.; Baca-Garcia, E. New perspectives in glutamate and anxiety. Pharmacol. Biochem. Behav., 2012, 100(4), 752-774.
[http://dx.doi.org/10.1016/j.pbb.2011.04.010] [PMID: 21569789]
[110]
Donner, J.; Sipilä, T.; Ripatti, S.; Kananen, L.; Chen, X.; Kendler, K.S.; Lönnqvist, J.; Pirkola, S.; Hettema, J.M.; Hovatta, I. Support for involvement of glutamate decarboxylase 1 and neuropeptide y in anxiety susceptibility. Am. J. Med. Genet. B. Neuropsychiatr. Genet., 2012, 159B(3), 316-327.
[http://dx.doi.org/10.1002/ajmg.b.32029] [PMID: 22328461]
[111]
Mitani, H.; Shirayama, Y.; Yamada, T.; Maeda, K.; Ashby, C.R., Jr; Kawahara, R. Correlation between plasma levels of glutamate, alanine and serine with severity of depression. Prog. Neuropsychopharmacol. Biol. Psychiatry, 2006, 30(6), 1155-1158.
[http://dx.doi.org/10.1016/j.pnpbp.2006.03.036] [PMID: 16707201]
[112]
Hashimoto, K.; Yoshida, T.; Ishikawa, M.; Fujita, Y.; Niitsu, T.; Nakazato, M.; Watanabe, H.; Sasaki, T.; Shiina, A.; Hashimoto, T.; Kanahara, N.; Hasegawa, T.; Enohara, M.; Kimura, A.; Iyo, M. Increased serum levels of serine enantiomers in patients with depression. Acta Neuropsychiatr., 2016, 28(3), 173-178.
[http://dx.doi.org/10.1017/neu.2015.59] [PMID: 26512905]
[113]
Kim, J.S.; Schmid-Burgk, W.; Claus, D.; Kornhuber, H.H. Increased serum glutamate in depressed patients. Arch. Psychiatr. Nervenkr., 1982, 232(4), 299-304.
[http://dx.doi.org/10.1007/BF00345492] [PMID: 6133511]
[114]
Yadav, R.; Gupta, S.C.; Hillman, B.G.; Bhatt, J.M.; Stairs, D.J.; Dravid, S.M. Deletion of glutamate delta-1 receptor in mouse leads to aberrant emotional and social behaviors. PLoS One, 2012, 7(3), e32969.
[http://dx.doi.org/10.1371/journal.pone.0032969] [PMID: 22412961]
[115]
Réus, G.Z.; Abaleira, H.M.; Michels, M.; Tomaz, D.B.; Santos, M.A.B.; Carlessi, A.S.; Matias, B.I.; Leffa, D.D.; Damiani, A.P.; Gomes, V.C.; Andrade, V.M.; Dal-Pizzol, F.; Landeira-Fernadez, J.; Quevedo, J. Anxious phenotypes plus environmental stressors are related to brain DNA damage and changes in NMDA receptor subunits and glutamate uptake. Mutat. Res., 2015, 772, 30-37.
[http://dx.doi.org/10.1016/j.mrfmmm.2014.12.005] [PMID: 25772108]
[116]
Williams, K. Modulation and block of ion channels: a new biology of polyamines. Cell. Signal., 1997, 9(1), 1-13.
[http://dx.doi.org/10.1016/S0898-6568(96)00089-7] [PMID: 9067625]
[117]
Andreasen, J.T.; Fitzpatrick, C.M.; Larsen, M.; Skovgaard, L.; Nielsen, S.D.; Clausen, R.P.; Troelsen, K.; Pickering, D.S. Differential role of AMPA receptors in mouse tests of antidepressant and anxiolytic action. Brain Res., 2015, 1601, 117-126.
[http://dx.doi.org/10.1016/j.brainres.2015.01.001] [PMID: 25578259]
[118]
Paoletti, P.; Bellone, C.; Zhou, Q. NMDA receptor subunit diversity: impact on receptor properties, synaptic plasticity and disease. Nat. Rev. Neurosci., 2013, 14(6), 383-400.
[http://dx.doi.org/10.1038/nrn3504] [PMID: 23686171]
[119]
Sun, H.; Guan, L.; Zhu, Z.; Li, H. Reduced levels of NR1 and NR2A with depression-like behavior in different brain regions in prenatally stressed juvenile offspring. PLoS One, 2013, 8(11), e81775.
[http://dx.doi.org/10.1371/journal.pone.0081775] [PMID: 24278457]
[120]
Dias, G.P.; Bevilaqua, M.C.N.; da Luz, A.C.D.S.; Fleming, R.L.; de Carvalho, L.A.; Cocks, G.; Beckman, D.; Hosken, L.C.; de Sant’Anna Machado, W.; Corrêa-e-Castro, A.C.; Mousovich-Neto, F.; de Castro Gomes, V.; Bastos, G.N.T.; Kubrusly, R.C.C.; da Costa, V.M.C.; Srivastava, D.; Landeira-Fernandez, J.; Nardi, A.E.; Thuret, S.; Gardino, P.F. Hippocampal biomarkers of fear memory in an animal model of generalized anxiety disorder. Behav. Brain Res., 2014, 263, 34-45.
[http://dx.doi.org/10.1016/j.bbr.2014.01.012] [PMID: 24462725]
[121]
Allaman, I.; Fiumelli, H.; Magistretti, P.J.; Martin, J.L. Fluoxetine regulates the expression of neurotrophic/growth factors and glucose metabolism in astrocytes. Psychopharmacology (Berl.), 2011, 216(1), 75-84.
[http://dx.doi.org/10.1007/s00213-011-2190-y] [PMID: 21301813]
[122]
Quesseveur, G.; David, D.J.; Gaillard, M.C.; Pla, P.; Wu, M.V.; Nguyen, H.T.; Nicolas, V.; Auregan, G.; David, I.; Dranovsky, A.; Hantraye, P.; Hen, R.; Gardier, A.M.; Déglon, N.; Guiard, B.P. BDNF overexpression in mouse hippocampal astrocytes promotes local neurogenesis and elicits anxiolytic-like activities. Transl. Psychiatry, 2013, 3(4), e253.
[http://dx.doi.org/10.1038/tp.2013.30] [PMID: 23632457]
[123]
Malberg, J.E.; Eisch, A.J.; Nestler, E.J.; Duman, R.S. Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J. Neurosci., 2000, 20(24), 9104-9110.
[http://dx.doi.org/10.1523/JNEUROSCI.20-24-09104.2000] [PMID: 11124987]
[124]
Ghasemi, M.; Navidhamidi, M.; Rezaei, F.; Azizikia, A.; Mehranfard, N. Anxiety and hippocampal neuronal activity: Relationship and potential mechanisms. Cogn. Affect. Behav. Neurosci., 2022, 22(3), 431-449.
[PMID: 34873665]
[125]
Samuels, B.A.; Hen, R. Neurogenesis and affective disorders. Eur. J. Neurosci., 2011, 33(6), 1152-1159.
[http://dx.doi.org/10.1111/j.1460-9568.2011.07614.x] [PMID: 21395859]
[126]
Banasr, M.; Hery, M.; Printemps, R.; Daszuta, A. Serotonin-induced increases in adult cell proliferation and neurogenesis are mediated through different and common 5-HT receptor subtypes in the dentate gyrus and the subventricular zone. Neuropsychopharmacology, 2004, 29(3), 450-460.
[http://dx.doi.org/10.1038/sj.npp.1300320] [PMID: 14872203]
[127]
Soumier, A.; Banasr, M.; Lortet, S.; Masmejean, F.; Bernard, N.; Kerkerian-Le-Goff, L.; Gabriel, C.; Millan, M.J.; Mocaer, E.; Daszuta, A. Mechanisms contributing to the phase-dependent regulation of neurogenesis by the novel antidepressant, agomelatine, in the adult rat hippocampus. Neuropsychopharmacology, 2009, 34(11), 2390-2403.
[http://dx.doi.org/10.1038/npp.2009.72] [PMID: 19571795]
[128]
Jha, S.; Rajendran, R.; Fernandes, K.A.; Vaidya, V.A. 5-HT2A/2C receptor blockade regulates progenitor cell proliferation in the adult rat hippocampus. Neurosci. Lett., 2008, 441(2), 210-214.
[http://dx.doi.org/10.1016/j.neulet.2008.06.028] [PMID: 18603367]
[129]
Qi, X.; Lin, W.; Li, J.; Li, H.; Wang, W.; Wang, D.; Sun, M. Fluoxetine increases the activity of the ERK-CREB signal system and alleviates the depressive-like behavior in rats exposed to chronic forced swim stress. Neurobiol. Dis., 2008, 31(2), 278-285.
[http://dx.doi.org/10.1016/j.nbd.2008.05.003] [PMID: 18586506]
[130]
Lucassen, P.J.; Bosch, O.J.; Jousma, E.; Krömer, S.A.; Andrew, R.; Seckl, J.R.; Neumann, I.D. Prenatal stress reduces postnatal neurogenesis in rats selectively bred for high, but not low, anxiety: possible key role of placental 11β-hydroxysteroid dehydrogenase type 2. Eur. J. Neurosci., 2009, 29(1), 97-103.
[http://dx.doi.org/10.1111/j.1460-9568.2008.06543.x] [PMID: 19032587]
[131]
Müller, C.P.; Reichel, M.; Mühle, C.; Rhein, C.; Gulbins, E.; Kornhuber, J. Brain membrane lipids in major depression and anxiety disorders. Biochim. Biophys. Acta Mol. Cell Biol. Lipids, 2015, 1851(8), 1052-1065.
[http://dx.doi.org/10.1016/j.bbalip.2014.12.014] [PMID: 25542508]
[132]
Zoicas, I.; Mühle, C.; Schmidtner, A.K.; Gulbins, E.; Neumann, I.D.; Kornhuber, J. Anxiety and depression are related to higher activity of sphingolipid metabolizing enzymes in the rat brain. Cells, 2020, 9(5), 1239.
[133]
Carboni, L.; El Khoury, A.; Beiderbeck, D.I.; Neumann, I.D.; Mathé, A.A.; Neuropeptide, Y. Neuropeptide Y, calcitonin gene-related peptide, and neurokinin A in brain regions of HAB rats correlate with anxiety-like behaviours. Eur. Neuropsychopharmacol., 2022, 57, 1-14.
[http://dx.doi.org/10.1016/j.euroneuro.2021.12.011] [PMID: 35008014]
[134]
Kovács, A.; Telegdy, G.; Tóth, G.; Penke, B. Neurotransmitter-mediated open-field behavioral action of CGRP. Life Sci., 1999, 64(9), 733-740.
[http://dx.doi.org/10.1016/S0024-3205(99)00002-8] [PMID: 10075105]
[135]
Poore, L.H.; Helmstetter, F.J. The effects of central injections of calcitonin gene-related peptide on fear-related behavior. Neurobiol. Learn. Mem., 1996, 66(2), 241-245.
[http://dx.doi.org/10.1006/nlme.1996.0065] [PMID: 8946417]
[136]
Sink, K.S.; Walker, D.L.; Yang, Y.; Davis, M. Calcitonin gene-related peptide in the bed nucleus of the stria terminalis produces an anxiety-like pattern of behavior and increases neural activation in anxiety-related structures. J. Neurosci., 2011, 31(5), 1802-1810.
[http://dx.doi.org/10.1523/JNEUROSCI.5274-10.2011] [PMID: 21289190]
[137]
León, L.A.; Brandão, M.L.; Cardenas, F.P.; Parra, D.; Krahe, T.E.; Cruz, A.P.M.; Landeira-Fernandez, J. Distinct patterns of brain Fos expression in Carioca High- and Low-conditioned Freezing rats. PLoS One, 2020, 15(7), e0236039.
[http://dx.doi.org/10.1371/journal.pone.0236039] [PMID: 32702030]
[138]
Herman, J.P.; Tasker, J.G. Paraventricular hypothalamic mechanisms of chronic stress adaptation. Front. Endocrinol. (Lausanne), 2016, 7, 137.
[http://dx.doi.org/10.3389/fendo.2016.00137] [PMID: 27843437]
[139]
Jankord, R.; Herman, J.P. Limbic regulation of hypothalamo-pituitary-adrenocortical function during acute and chronic stress. Ann. N. Y. Acad. Sci., 2008, 1148(1), 64-73.
[http://dx.doi.org/10.1196/annals.1410.012] [PMID: 19120092]
[140]
Ziegler, D.R.; Cass, W.A.; Herman, J.P. Excitatory influence of the locus coeruleus in hypothalamic-pituitary-adrenocortical axis responses to stress. J. Neuroendocrinol., 1999, 11(5), 361-369.
[http://dx.doi.org/10.1046/j.1365-2826.1999.00337.x] [PMID: 10320563]
[141]
Herman, J.P.; McKlveen, J.M.; Ghosal, S.; Kopp, B.; Wulsin, A.; Makinson, R.; Scheimann, J.; Myers, B. Regulation of the hypothalamic-pituitary-adrenocortical stress response. In: Comprehensive Physiology; , 2016; pp. 603-621.
[http://dx.doi.org/10.1002/cphy.c150015]
[142]
Graeff, F.G.; Zangrossi, H., Jr The hypothalamic-pituitary-adrenal axis in anxiety and panic. Psychol. Neurosci., 2010, 3(1), 3-8.
[http://dx.doi.org/10.3922/j.psns.2010.1.002]
[143]
Balthazar, L.; Lages, Y.V.M.; Romano, V.C.; Landeira-Fernandez, J.; Krahe, T.E. The association between the renin-angiotensin system and the hypothalamic-pituitary-adrenal axis in anxiety disorders: A systematic review of animal studies. Psychoneuroendocrinology, 2021, 132, 105354.
[http://dx.doi.org/10.1016/j.psyneuen.2021.105354] [PMID: 34329905]
[144]
Samuels, E.; Szabadi, E. Functional neuroanatomy of the noradrenergic locus coeruleus: its roles in the regulation of arousal and autonomic function part I: principles of functional organisation. Curr. Neuropharmacol., 2008, 6(3), 235-253.
[http://dx.doi.org/10.2174/157015908785777229] [PMID: 19506723]
[145]
Calandreau, L.; Jaffard, R.; Desmedt, A. Dissociated roles for the lateral and medial septum in elemental and contextual fear conditioning. Learn. Mem., 2007, 14(6), 422-429.
[http://dx.doi.org/10.1101/lm.531407] [PMID: 17554087]
[146]
Yoshida, K.; Oka, H. Topographical projections from the medial septum-diagonal band complex to the hippocampus: a retrograde tracing study with multiple fluorescent dyes in rats. Neurosci. Res., 1995, 21(3), 199-209.
[http://dx.doi.org/10.1016/0168-0102(94)00852-7] [PMID: 7753501]
[147]
Nyakas, C.; Luiten, P.G.M.; Spencer, D.G.; Traber, J. Detailed projection patterns of septal and diagonal band efferents to the hippocampus in the rat with emphasis on innervation of CA1 and dentate gyrus. Brain Res. Bull., 1987, 18(4), 533-545.
[http://dx.doi.org/10.1016/0361-9230(87)90117-1] [PMID: 3607523]
[148]
Gilmartin, M.R.; Kwapis, J.L.; Helmstetter, F.J. Trace and contextual fear conditioning are impaired following unilateral microinjection of muscimol in the ventral hippocampus or amygdala, but not the medial prefrontal cortex. Neurobiol. Learn. Mem., 2012, 97(4), 452-464.
[http://dx.doi.org/10.1016/j.nlm.2012.03.009] [PMID: 22469748]
[149]
Twining, R.C.; Lepak, K.; Kirry, A.J.; Gilmartin, M.R. Ventral hippocampal input to the prelimbic cortex dissociates the context from the cue association in trace fear memory. J. Neurosci., 2020, 40(16), 3217-3230.
[http://dx.doi.org/10.1523/JNEUROSCI.1453-19.2020] [PMID: 32188770]
[150]
Jones, K.R.; Myers, B.; Herman, J.P. Stimulation of the prelimbic cortex differentially modulates neuroendocrine responses to psychogenic and systemic stressors. Physiol. Behav., 2011, 104(2), 266-271.
[http://dx.doi.org/10.1016/j.physbeh.2011.03.021] [PMID: 21443894]
[151]
Lemos, J.I.; Resstel, L.B.; Guimarães, F.S. Involvement of the prelimbic prefrontal cortex on cannabidiol-induced attenuation of contextual conditioned fear in rats. Behav. Brain Res., 2010, 207(1), 105-111.
[http://dx.doi.org/10.1016/j.bbr.2009.09.045] [PMID: 19800921]
[152]
Holmes, N.M.; Parkes, S.L.; Killcross, A.S.; Westbrook, R.F. The basolateral amygdala is critical for learning about neutral stimuli in the presence of danger, and the perirhinal cortex is critical in the absence of danger. J. Neurosci., 2013, 33(32), 13112-13125.
[http://dx.doi.org/10.1523/JNEUROSCI.1998-13.2013] [PMID: 23926265]
[153]
Deacon, T.W.; Eichenbaum, H.; Rosenberg, P.; Eckmann, K.W. Afferent connections of the perirhinal cortex in the rat. J. Comp. Neurol., 1983, 220(2), 168-190.
[http://dx.doi.org/10.1002/cne.902200205] [PMID: 6643724]
[154]
Jones, B.F.; Witter, M.P. Cingulate cortex projections to the parahippocampal region and hippocampal formation in the rat. Hippocampus, 2007, 17(10), 957-976.
[http://dx.doi.org/10.1002/hipo.20330] [PMID: 17598159]
[155]
Wiersma, A.; Konsman, J.P.; Knollema, S.; Bohus, B.; Koolhaas, J.M. Differential effects of CRH infusion into the central nucleus of the amygdala in the Roman high-avoidance and low-avoidance rats. Psychoneuroendocrinology, 1998, 23(3), 261-274.
[http://dx.doi.org/10.1016/S0306-4530(97)00098-X] [PMID: 9695130]
[156]
Meyza, K.Z.; Boguszewski, P.M.; Nikolaev, E.; Zagrodzka, J. Diverse sensitivity of RHA/Verh and RLA/Verh rats to emotional and spatial aspects of a novel environment as a result of a distinct pattern of neuronal activation in the fear/anxiety circuit. Behav. Genet., 2009, 39(1), 48-61.
[http://dx.doi.org/10.1007/s10519-008-9234-z] [PMID: 18972198]
[157]
Muigg, P.; Scheiber, S.; Salchner, P.; Bunck, M.; Landgraf, R.; Singewald, N. Differential stress-induced neuronal activation patterns in mouse lines selectively bred for high, normal or low anxiety. PLoS One, 2009, 4(4), e5346.
[http://dx.doi.org/10.1371/journal.pone.0005346] [PMID: 19399175]
[158]
Salomé, N.; Salchner, P.; Viltart, O.; Sequeira, H.; Wigger, A.; Landgraf, R.; Singewald, N. Neurobiological correlates of high (HAB) versus low anxiety-related behavior (LAB): differential Fos expression in HAB and LAB rats. Biol. Psychiatry, 2004, 55(7), 715-723.
[http://dx.doi.org/10.1016/j.biopsych.2003.10.021] [PMID: 15039000]
[159]
Kalisch, R.; Salomé, N.; Platzer, S.; Wigger, A.; Czisch, M.; Sommer, W.; Singewald, N.; Heilig, M.; Berthele, A.; Holsboer, F.; Landgraf, R.; Auer, D.P. High trait anxiety and hyporeactivity to stress of the dorsomedial prefrontal cortex: a combined phMRI and Fos study in rats. Neuroimage, 2004, 23(1), 382-391.
[http://dx.doi.org/10.1016/j.neuroimage.2004.06.012] [PMID: 15325386]
[160]
Muigg, P.; Hoelzl, U.; Palfrader, K.; Neumann, I.; Wigger, A.; Landgraf, R.; Singewald, N. Altered brain activation pattern associated with drug-induced attenuation of enhanced depression-like behavior in rats bred for high anxiety. Biol. Psychiatry, 2007, 61(6), 782-796.
[http://dx.doi.org/10.1016/j.biopsych.2006.08.035] [PMID: 17224133]
[161]
Muigg, P.; Hetzenauer, A.; Hauer, G.; Hauschild, M.; Gaburro, S.; Frank, E.; Landgraf, R.; Singewald, N. Impaired extinction of learned fear in rats selectively bred for high anxiety - evidence of altered neuronal processing in prefrontal-amygdala pathways. Eur. J. Neurosci., 2008, 28(11), 2299-2309.
[http://dx.doi.org/10.1111/j.1460-9568.2008.06511.x] [PMID: 19019199]
[162]
Mousovich-Neto, F.; Lourenço, A.L.; Landeira-Fernandez, J.; Corrêa da Costa, V.M. Endocrine and metabolic function in male Carioca High-conditioned Freezing rats. Physiol. Behav., 2015, 142, 90-96.
[http://dx.doi.org/10.1016/j.physbeh.2015.01.028] [PMID: 25623541]
[163]
León, L.; Gomes, V.; Brandão, M.; Franci, C.; Cardenas, F.; Landeira-Fernandez, J. Corticosterone plasma concentrations in Carioca High-and Low-conditioned freezing rats after a fear conditioned task. Av. Psicol. Latinoam., 2013, 31, 279-287.
[164]
Feldman, S.; Weidenfeld, J. Glucocorticoid receptor antagonists in the hippocampus modify the negative feedback following neural stimuli. Brain Res., 1999, 821(1), 33-37.
[http://dx.doi.org/10.1016/S0006-8993(99)01054-9] [PMID: 10064785]
[165]
Wilson, M.M.; Greer, S.E.; Greer, M.A.; Roberts, L. Hippocampal inhibition of pituitary-adrenocortical function in female rats. Brain Res., 1980, 197(2), 433-441.
[http://dx.doi.org/10.1016/0006-8993(80)91128-2] [PMID: 6250667]
[166]
Brinks, V.; de Kloet, E.R.; Oitzl, M.S. Corticosterone facilitates extinction of fear memory in BALB/c mice but strengthens cue related fear in C57BL/6 mice. Exp. Neurol., 2009, 216(2), 375-382.
[http://dx.doi.org/10.1016/j.expneurol.2008.12.011] [PMID: 19162011]
[167]
Carrasco, J.; Márquez, C.; Nadal, R.; Tobeña, A.; Fernández-Teruel, A.; Armario, A. Characterization of central and peripheral components of the hypothalamus–pituitary–adrenal axis in the inbred Roman rat strains. Psychoneuroendocrinology, 2008, 33(4), 437-445.
[http://dx.doi.org/10.1016/j.psyneuen.2008.01.001] [PMID: 18276081]
[168]
Steimer, T.; Driscoll, P. Divergent stress responses and coping styles in psychogenetically selected Roman high-(RHA) and low-(RLA) avoidance rats: behavioural, neuroendocrine and developmental aspects. Stress, 2003, 6(2), 87-100.
[http://dx.doi.org/10.1080/1025389031000111320] [PMID: 12775328]
[169]
Salome, N.; Tasiemski, A.; Dutriez, I.; Wigger, A.; Landgraf, R.; Viltart, O. Immune challenge induces differential corticosterone and interleukin-6 responsiveness in rats bred for extremes in anxiety-related behavior. Neuroscience, 2008, 151(4), 1112-1118.
[http://dx.doi.org/10.1016/j.neuroscience.2007.12.010] [PMID: 18207648]
[170]
Landgraf, R.; Wigger, A. Born to be anxious: neuroendocrine and genetic correlates of trait anxiety in HAB rats. Stress, 2003, 6(2), 111-119.
[http://dx.doi.org/10.1080/1025389031000104193] [PMID: 12775330]
[171]
Landgraf, R.; Wigger, A.; Holsboer, F.; Neumann, I.D. Hyper-reactive hypothalamo-pituitary-adrenocortical axis in rats bred for high anxiety-related behaviour. J. Neuroendocrinol., 1999, 11(6), 405-407.
[http://dx.doi.org/10.1046/j.1365-2826.1999.00342.x] [PMID: 10336720]
[172]
Physiology, Adrenocorticotropic Hormone (ACTH).StatPearls; StatPearls Publishing: Florida, 2022.
[173]
Frank, E.; Salchner, P.; Aldag, J.M.; Salomé, N.; Singewald, N.; Landgraf, R.; Wigger, A. Genetic predisposition to anxiety-related behavior determines coping style, neuroendocrine responses, and neuronal activation during social defeat. Behav. Neurosci., 2006, 120(1), 60-71.
[http://dx.doi.org/10.1037/0735-7044.120.1.60] [PMID: 16492117]
[174]
Appel, B.; Fried, S.K. Effects of insulin and dexamethasone on lipoprotein lipase in human adipose tissue. Am. J. Physiol., 1992, 262(5 Pt 1), E695-E699.
[PMID: 1590379]
[175]
Bujalska, I.J.; Kumar, S.; Hewison, M.; Stewart, P.M. Differentiation of adipose stromal cells: the roles of glucocorticoids and 11beta-hydroxysteroid dehydrogenase. Endocrinology, 1999, 140(7), 3188-3196.
[http://dx.doi.org/10.1210/endo.140.7.6868] [PMID: 10385414]
[176]
van Rossum, E.F.C.; Binder, E.B.; Majer, M.; Koper, J.W.; Ising, M.; Modell, S.; Salyakina, D.; Lamberts, S.W.J.; Holsboer, F. Polymorphisms of the glucocorticoid receptor gene and major depression. Biol. Psychiatry, 2006, 59(8), 681-688.
[http://dx.doi.org/10.1016/j.biopsych.2006.02.007] [PMID: 16580345]
[177]
Rebuffé-Scrive, M.; Mårin, P.; Björntorp, P. Effect of testosterone on abdominal adipose tissue in men. Int. J. Obes., 1991, 15(11), 791-795.
[PMID: 1778664]
[178]
Gentile, M.A.; Nantermet, P.V.; Vogel, R.L.; Phillips, R.; Holder, D.; Hodor, P.; Cheng, C.; Dai, H.; Freedman, L.P.; Ray, W.J. Androgen-mediated improvement of body composition and muscle function involves a novel early transcriptional program including IGF1, mechano growth factor, and induction of β-catenin. J. Mol. Endocrinol., 2010, 44(1), 55-73.
[http://dx.doi.org/10.1677/JME-09-0048] [PMID: 19726620]
[179]
Per, M.; Björntorp, L. Effects of testosterone on triglyceride uptake and mobilization in different adipose tissues in male rats in vivo. Obes. Res., 1995, 3(2), 113-119.
[http://dx.doi.org/10.1002/j.1550-8528.1995.tb00128.x] [PMID: 7719957]
[180]
Xu, X.; Pergola, G.D.; Björntorp, P. Testosterone increases lipolysis and the number of beta-adrenoceptors in male rat adipocytes. Endocrinology, 1991, 128(1), 379-382.
[http://dx.doi.org/10.1210/endo-128-1-379] [PMID: 1846106]
[181]
Lundgren, M.; Burén, J.; Ruge, T.; Myrnäs, T.; Eriksson, J.W. Glucocorticoids down-regulate glucose uptake capacity and insulin-signaling proteins in omental but not subcutaneous human adipocytes. J. Clin. Endocrinol. Metab., 2004, 89(6), 2989-2997.
[http://dx.doi.org/10.1210/jc.2003-031157] [PMID: 15181089]
[182]
Steimer, T.; la Fleur, S.; Schulz, P.E. Neuroendocrine correlates of emotional reactivity and coping in male rats from the Roman high (RHA/Verh)- and low (RLA/Verh)-avoidance lines. Behav. Genet., 1997, 27(6), 503-512.
[http://dx.doi.org/10.1023/A:1021448713665] [PMID: 9476359]
[183]
Boersma, G.J.; Scheurink, A.J.W.; Wielinga, P.Y.; Steimer, T.J.; Benthem, L. The passive coping Roman Low Avoidance rat, a non-obese rat model for insulin resistance. Physiol. Behav., 2009, 97(3-4), 353-358.
[http://dx.doi.org/10.1016/j.physbeh.2009.03.005] [PMID: 19296906]
[184]
Neumann, I.D.; Wigger, A.; Liebsch, G.; Holsboer, F.; Landgraf, R. Increased basal activity of the hypothalamo-pituitary-adrenal axis during pregnancy in rats bred for high anxiety-related behaviour. Psychoneuroendocrinology, 1998, 23(5), 449-463.
[http://dx.doi.org/10.1016/S0306-4530(98)00023-7] [PMID: 9802120]
[185]
Windle, R.J.; Shanks, N.; Lightman, S.L.; Ingram, C.D. Central oxytocin administration reduces stress-induced corticosterone release and anxiety behavior in rats. Endocrinology, 1997, 138(7), 2829-2834.
[http://dx.doi.org/10.1210/endo.138.7.5255] [PMID: 9202224]
[186]
Neumann, I.D.; Wigger, A.; Torner, L.; Holsboer, F.; Landgraf, R. Brain oxytocin inhibits basal and stress-induced activity of the hypothalamo-pituitary-adrenal axis in male and female rats: partial action within the paraventricular nucleus. J. Neuroendocrinol., 2000, 12(3), 235-243.
[http://dx.doi.org/10.1046/j.1365-2826.2000.00442.x] [PMID: 10718919]
[187]
Bale, T.L.; Davis, A.M.; Auger, A.P.; Dorsa, D.M.; McCarthy, M.M.; Region-Specific Oxytocin Receptor Expression, C.N.S. CNS region-specific oxytocin receptor expression: importance in regulation of anxiety and sex behavior. J. Neurosci., 2001, 21(7), 2546-2552.
[http://dx.doi.org/10.1523/JNEUROSCI.21-07-02546.2001] [PMID: 11264328]
[188]
Wigger, A.; Sánchez, M.M.; Mathys, K.C.; Ebner, K.; Frank, E.; Liu, D.; Kresse, A.; Neumann, I.D.; Holsboer, F.; Plotsky, P.M.; Landgraf, R. Alterations in central neuropeptide expression, release, and receptor binding in rats bred for high anxiety: Critical role of vasopressin. Neuropsychopharmacology, 2004, 29(1), 1-14.
[http://dx.doi.org/10.1038/sj.npp.1300290] [PMID: 12942143]
[189]
Hassan, W.; Silva, C.E.B.; Rocha, J.B.T.; Landeira-Fernandez, J. Modulatory effect of diphenyl diselenide in Carioca High- and Low-conditioned Freezing rats. Eur. J. Pharmacol., 2015, 761, 341-344.
[http://dx.doi.org/10.1016/j.ejphar.2015.05.069] [PMID: 26086858]
[190]
Souza, C.G.; Moreira, J.D.; Siqueira, I.R.; Pereira, A.G.; Rieger, D.K.; Souza, D.O.; Souza, T.M.; Portela, L.V.; Perry, M.L.S. Highly palatable diet consumption increases protein oxidation in rat frontal cortex and anxiety-like behavior. Life Sci., 2007, 81(3), 198-203.
[http://dx.doi.org/10.1016/j.lfs.2007.05.001] [PMID: 17574275]
[191]
Salim, S.; Asghar, M.; Chugh, G.; Taneja, M.; Xia, Z.; Saha, K. Oxidative stress: A potential recipe for anxiety, hypertension and insulin resistance. Brain Res., 2010, 1359, 178-185.
[http://dx.doi.org/10.1016/j.brainres.2010.08.093] [PMID: 20816762]
[192]
Salim, S.; Sarraj, N.; Taneja, M.; Saha, K.; Tejada-Simon, M.V.; Chugh, G. Moderate treadmill exercise prevents oxidative stress-induced anxiety-like behavior in rats. Behav. Brain Res., 2010, 208(2), 545-552.
[http://dx.doi.org/10.1016/j.bbr.2009.12.039] [PMID: 20064565]
[193]
Deoliveira, M.; Silvestrin, R.; Melloesouza, T.; Moreira, J. Oxidative stress in the hippocampus, anxiety-like behavior and decreased locomotory and exploratory activity of adult rats: Effects of sub acute vitamin A supplementation at therapeutic doses. Neurotoxicology, 2007, 28(6), 1191-1199.
[http://dx.doi.org/10.1016/j.neuro.2007.07.008] [PMID: 17727954]
[194]
Leal, P.E.d.P.T.; da Silva, A.A.; Rocha-Gomes, A.; Riul, T.R.; Cunha, R.A.; Reichetzeder, C.; Villela, D.C. High-salt diet in the pre- and postweaning periods leads to amygdala oxidative stress and changes in locomotion and anxiety-like behaviors of male wistar rats. Front. Behav. Neurosci., 2022, 15, 779080.
[http://dx.doi.org/10.3389/fnbeh.2021.779080] [PMID: 35058757]
[195]
Namgyal, D.; Ali, S.; Hussain, M.D.; Kazi, M.; Ahmad, A.; Sarwat, M. Curcumin ameliorates the Cd-induced anxiety-like behavior in mice by regulating oxidative stress and neuro-inflammatory proteins in the prefrontal cortex region of the brain. Antioxidants, 2021, 10(11), 1710.
[http://dx.doi.org/10.3390/antiox10111710] [PMID: 34829581]
[196]
Bouayed, J.; Rammal, H.; Younos, C.; Soulimani, R. Positive correlation between peripheral blood granulocyte oxidative status and level of anxiety in mice. Eur. J. Pharmacol., 2007, 564(1-3), 146-149.
[http://dx.doi.org/10.1016/j.ejphar.2007.02.055] [PMID: 17395178]
[197]
Gomes, V.C.; León, L.A.; Mograbi, D.; Cardenas, F.; Landeira-Fernandez, J. Contextual fear extinction and re-extinction in Carioca High- and Low-conditioned Freezing rats. World J. Neurosci., 2014, 4(3), 247-252.
[http://dx.doi.org/10.4236/wjns.2014.43028]
[198]
Bezerra-Karounis, M.A.; Krahe, T.E.; Maisonnette, S.; Landeira-Fernandez, J. Alcohol intake in Carioca High- and Low-conditioned Freezing rats. Pharmacol. Biochem. Behav., 2020, 197, 173019.
[http://dx.doi.org/10.1016/j.pbb.2020.173019] [PMID: 32827503]

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