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Original Articles

Alteration of the α5 GABA receptor and 5HTT lead to cognitive deficits associated with major depressive-like behaviors in a 14-day combined stress rat model

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Pages 959-976 | Received 13 Aug 2020, Accepted 08 Dec 2021, Published online: 02 Jan 2022

References

  • Otte C, Gold SM, Penninx BW, et al. Major depressive disorder. Nat Rev Dis Primers. 2016;2:16065.
  • Richardson L, Adams S. Cognitive deficits in patients with depression. J Nurse Pract. 2018;6:437–443.
  • De Hert M, Correll CU, Bobes J, et al. Physical illness in patients with severe mental disorders. I. Prevalence, impact of medications and disparities in health care. World Psychiatry. 2011;10(1):52–77.
  • Charara R, Forouzanfar M, Naghavi M, et al. The burden of mental disorders in the Eastern mediterranean region, 1990–2013. PloS One. 2017;12(1):e0169575.
  • Collins PY, Patel V, Joestl SS, et al. Grand challenges in global mental health. Nature. 2011;475(7354):27–30.
  • Kupfer DJ, Frank E, Phillips ML. Major depressive disorder: new clinical, neurobiological, and treatment perspectives. The Lancet. 2012;379(9820):1045–1055.
  • Greenberg PE, Fournier AA, Sisitsky T, et al. The economic burden of adults with major depressive disorder in the United States (2005 and 2010). J Clin Psychiatry. 2015;76(2):155–162.
  • Baune BT, Renger L. Pharmacological and non-pharmacological interventions to improve cognitive dysfunction and functional ability in clinical depression: a systematic review. Psychiatry Res. 2014;219(1):25–50.
  • Chaudhury D, Liu H, Han MH. Neuronal correlates of depression. Cell Mol Life Sci. 2015;72(24):4825–4848.
  • World Health Organization. 2018. Depression. Available from: https://www.who.int/news-room/fact-sheets/detail/depression.
  • Beblo T, Sinnamon G, Baune BT. Specifying the neuropsychology of affective disorders: clinical, demographic and neurobiological factors. Neuropsychol Rev. 2011;21(4):337–359.
  • Listunova L, Roth C, Bartolovic M, et al. Cognitive impairment along the course of depression: non-pharmacological treatment options. Psychopathology. 2018;51(5):295–305.
  • Baune BT, McAfoose J, Leach G, et al. Impact of psychiatric and medical comorbidity on cognitive function in depression. Psychiatry Clin Neurosci. 2009;63(3):392–400.
  • Baune BT, Malhi GS, Morris G, et al. Cognition in depression: can we THINC-it better? J Affect Disord. 2018;225:559–562.
  • Thomas CM, Morris S. Cost of depression among adults in England in 2000. Br J Psychiatry. 2003;183(6):514–519.
  • Krol M, Papenburg J, Koopmanschap M, et al. Do productivity costs matter?: the impact of including productivity costs on the incremental costs of interventions targeted at depressive disorders Pharmacoeconomics. 2011;29(7):601–619.
  • Olesen J, Gustavsson A, Svensson M, et al. CDBE2010 Study Group, European brain council. The economic cost of brain disorders in Europe. Eur J Neurol. 2012;19(1):155–162.
  • Schildkraut JJ. The catecholamine hypothesis of affective disorders: a review of supporting evidence. Am J Psychiatry. 1965;122(5):509–522.
  • Czéh B, Fuchs E, Wiborg O, et al. Animal models of major depression and their clinical implications. Prog Neuropsychopharmacol Biol Psychiatry. 2016;64:293–310.
  • Liu Z, Liu X, Luo S, et al. Extract of sesame cake and sesamol alleviate chronic unpredictable mild stress-induced depressive-like behaviors and memory deficits. J. Funct Foods. 2018;42:237–247.
  • Garcia-Garcia AL, Newman-Tancredi A, Leonardo ED. 5-HT 1A receptors in mood and anxiety: recent insights into autoreceptor versus heteroreceptor function. Psychopharmacology (Berl). 2014;231(4):623–636. http://dx.doi.org/10.1007/s00213-013-3425-x
  • Albert PR, Vahid-Ansari F, Luckhart C. Serotonin-prefrontal cortical circuitry in anxiety and depression phenotypes: pivotal role of pre-and post-synaptic 5-HT1A receptor expression. Front Behav Neurosci. 2014;6(8):199.
  • Bravo JA, Dinan TG, Cryan JF. Early-life stress induces persistent alterations in 5-HT1A receptor and serotonin transporter mRNA expression in the adult rat brain. Front Mol Neurosci. 2014;7(7):24.
  • Kaufman J, DeLorenzo C, Choudhury S, et al. The 5-HT1A receptor in major depressive disorder. Eur Neuropsychopharmacol. 2016;26(3):397–410.
  • Olivier JD, Jans LA, Blokland A, et al. Serotonin transporter deficiency in rats contributes to impaired object memory. Genes Brain Behav. 2009;8(8):829–834.
  • Ramirez-Mahaluf JP, Compte A. Serotonergic modulation of cognition in prefrontal cortical circuits in major depression. In Computational psychiatry. Cambridge, MA: Academic Press. p. 27–46. 2018.
  • Neumeister A, Konstantinidis A, Stastny J, et al. Association between serotonin transporter gene promoter polymorphism (5HTTLPR) and behavioral responses to tryptophan depletion in healthy women with and without family history of depression. Arch Gen Psychiatry. 2002;59(7):613–620.
  • Firk C, Markus CR. Differential effects of 5-HTTLPR genotypes on mood, memory, and attention bias following acute tryptophan depletion and stress exposure. Psychopharmacology (Berl). 2009;203(4):805–818.
  • Nautiyal KM, Hen R. Serotonin receptors in depression: from A to B. F1000 Research. 2017;6:123.
  • Hariri AR, Mattay VS, Tessitore A, et al. Serotonin transporter genetic variation and the response of the human amygdala. Science. 2002;297(5580):400–403.
  • Marsh AA, Finger EC, Buzas B, et al. Impaired recognition of fear facial expressions in 5-HTTLPR S-polymorphism carriers following tryptophan depletion. Psychopharmacology (Berl). 2006;189(3):387–394.
  • Shopsin B, Feiner NF. Serotonin and depression: a brief review. Adv Biol Psychiatry. 1984;14:1–11. http://dx.doi.org/10.1159/000409889
  • Bhagwagar Z, Whale R, Cowen PJ. State and trait abnormalities in serotonin function in major depression. Br J Psychiatry. 2002;180(1):24–28.
  • Fairchild G, Leitch MM, Ingram CD. Acute and chronic effects of corticosterone on 5-HT1A receptor-mediated autoinhibition in the rat dorsal raphe nucleus. Neuropharmacology. 2003;45(7):925–934.
  • Stiedl O, Pappa E, Konradsson-Geuken Å, et al. The role of the serotonin receptor subtypes 5-HT1A and 5-HT7 and its interaction in emotional learning and memory. Front Pharmacol. 2015;6:162.
  • Healy D. Serotonin and depression. BMJ (Online). 2015;350:h1771.
  • Ngoupaye GT, Yassi FB, Bahane DAN, et al. Antidepressant and anti-amnesic effects of the aqueous lyophilisate of the leaves of Leptadenia arborea on an animal model of cognitive deficit associated depression. Biomed Pharmacother. 2020;130:110603.
  • Anacker C, Zunszain PA, Carvalho LA, et al. The glucocorticoid receptor: pivot of depression and of antidepressant treatment? Psychoneuroendocrinology. 2011;36(3):415–425.
  • Snyder JS, Soumier A, Brewer M, et al. Adult hippocampal neurogenesis buffers stress responses and depressive behaviour. Nature. 2011;476(7361):458–461.
  • Robinson SA, Brookshire BR, Lucki I. Corticosterone exposure augments sensitivity to the behavioral and neuroplastic effects of fluoxetine in C57BL/6 mice. Neurobiol Stress. 2016;3(3):34–42.
  • Dranovsky A, Hen R. Hippocampal neurogenesis: regulation by stress and antidepressants. Biol Psychiatry. 2006;59(12):1136–1143.
  • Finsterwald C, Alberini CM. Stress and glucocorticoid receptor-dependent mechanisms in long-term memory: from adaptive responses to psychopathologies. Neurobiol Learn Mem. 2014;112:17–29.
  • Vinkers CH, Joëls M, Milaneschi Y, et al. Stress exposure across the life span cumulatively increases depression risk and is moderated by neuroticism. Depress Anxiety. 2014;31(9):737–745.
  • Lucassen PJ, Oomen CA, Naninck EF, et al. Regulation of adult neurogenesis and plasticity by (early) stress, glucocorticoids, and inflammation. Cold Spring Harb Perspect Biol. 2015;7(9):a021303.
  • Hadad-Ophir O, Albrecht A, Stork O, et al. Amygdala activation and GABAergic gene expression in hippocampal Sub-regions at the interplay of stress and spatial learning. Front Behav Neurosci. 2014;8:3.
  • Fischell J, Van Dyke AM, Kvarta MD, et al. Rapid antidepressant action and restoration of excitatory synaptic strength after chronic stress by negative modulators of Alpha5-containing GABAA receptors. Neuropsychopharmacology. 2015;40(11):2499–2509.
  • Mcginnity CJ, Riaño Barros DA, Rosso L, et al. Test-retest reproducibility of quantitative binding measures of [11C]Ro15-4513, a PET ligand for GABAA receptors containing alpha5 subunits. NeuroImage. 2017;152:270–282.
  • Koh MT, Rosenzweig-Lipson S, Gallagher M. Selective GABA(A) α5 positive allosteric modulators improve cognitive function in aged rats with memory impairment. Neuropharmacology. 2013;64:145–152.
  • Ngoupaye GT, Yassi FB, Bahane DA, et al. Combined corticosterone treatment and chronic restraint stress lead to depression associated with early cognitive deficits in mice. Metab Brain Dis. 2018;33(2):421–431.
  • Nestler EJ, Gould E, Manji H. Preclinical models: status of basic research in depression. Biological Psychia. 2002;52(6):503–528.(02)01405-1
  • Marks W, Fournier NM, Kalynchuk LE. Repeated exposure to corticosterone increases depression-like behavior in two different versions of the forced swim test without altering nonspecific locomotor activity or muscle strength. Physiol Behav. 2009;98(1–2):67–72.
  • Zhao Y, Ma R, Shen J, et al. A mouse model of depression induced by repeated corticosterone injections. Eur J Pharmacol. 2008;581(1–2):113–120.
  • Yau SY, Li A, Tong JB, et al. Chronic corticosterone administration reduces dendritic complexity in mature, but not young granule cells in the rat dentate gyrus. Restor Neurol Neurosci. 2016;34(5):849–857.
  • Kott JM, Mooney-Leber SM, Shoubah FA, et al. Effectiveness of different corticosterone administration methods to elevate corticosterone serum levels, induce depressive-like behavior, and affect neurogenesis levels in female rats. Neurosci. 2016;312:201–214.
  • Wong EY, Herbert J. Roles of mineralocorticoid and glucocorticoid receptors in the regulation of progenitor proliferation in the adult hippocampus. Eur J Neurosci. 2005;22(4):785–792.
  • Lussier AL, Lebedeva K, Fenton EY, et al. The progressive development of depression-like behavior in corticosterone-treated rats is paralleled by slowed granule cell maturation and decreased reelin expression in the adult dentate gyrus. Neuropharmacology. 2013;71:174–183.
  • Eng J. Sample size estimation: how many individuals should be studied? Radiology. 2003;227(2):309–313.
  • Paukert M, Agarwal A, Cha J, et al. Norepinephrine controls astroglial responsiveness to local circuit activity. Neuron. 2014;82(6):1263–1270. https://doi.org/10.1016/j.neuron.2014.04.038
  • Yankelevitch-Yahav R, Franko M, Huly A, et al. The forced swim test as a model of depressive-like behavior. J Visual Exp. 2015;2015(97):52587.
  • Willner P, Towell A, Sampson D, et al. Reduction of sucrose preference by chronic unpredictable mild stress, and its restoration by a tricyclic antidepressant. Psychopharmacol. 1987;93(3):358–364.
  • Riad M, Kobert A, Descarries L, et al. Chronic fluoxetine rescues changes in plasma membrane density of 5-HT1A autoreceptors and serotonin transporters in the olfactory bulbectomy rodent model of depression. Neurosci. 2017;356:78–88.
  • Ngoupaye GT, Pahaye DB, Ngondi J, et al. Gladiolus dalenii lyophilisate reverses scopolamine-induced amnesia and reduces oxidative stress in rat brain. Biomed Pharmacother. 2017;91:350–357.
  • Morris R. Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods. 1984;11(1):47–60.
  • Svensson M, Hallin T, Broms J, et al. Spatial memory impairment in Morris water maze after electroconvulsive seizures. Acta Neuropsychiatr. 2017;29(1):17–26.
  • Garthe A, Kempermann G. An old test for new neurons: refining the Morris water maze to study the functional relevance of adult hippocampal neurogenesis. Front Neurosci. 2013;7:63.
  • D’Hooge R, De Deyn PP. Applications of the Morris water maze in the study of learning and memory. Brain Res Rev. 2001;36(1):60–90.
  • Grayson B, Leger M, Piercy C, et al. Assessment of disease-related cognitive impairments using the novel object recognition (nor) task in rodents. Behav Brain Res. 2015;285:176–193.
  • Gehring TV, Luksys G, Sandi C, et al. Detailed classification of swimming paths in the Morris water maze: multiple strategies within one trial. Sci Rep. 2015;5:14562.
  • Makhathini KB, Abboussi O, Stein DJ, et al. Repetitive stress leads to impaired cognitive function that is associated with DNA hypomethylation, reduced BDNF and a dysregulated HPA axis. Int J Dev Neurosci. 2017;60:63–69.
  • Dalle E, Daniels WM, Mabandla MV. Fluvoxamine maleate effects on dopamine signaling in the prefrontal cortex of stressed parkinsonian rats: implications for learning and memory. Brain Res Bull. 2017;132:75–81.
  • Rizvi SJ, Pizzagalli DA, Sproule BA, et al. Assessing anhedonia in depression: potentials and pitfalls. Neurosci Biobehav Rev. 2016;65:21–35.
  • Buck KD, McLeod HJ, Gumley A, et al. Anhedonia in prolonged schizophrenia spectrum patients with relatively lower vs. higher levels of depression disorders: associations with deficits in social cognition and metacognition. Conscious Cogn. 2014;29:68–75.
  • Mello AF, Juruena MF, Pariante CM, et al. Depression and stress: is there an endophenotype? Brazil J Psychiatry. 2007;29:13–18.
  • Klimes-Dougan B, Eberly LE, Schreiner MW, et al. Multilevel assessment of the neurobiological threat system in depressed adolescents: interplay between the limbic system and hypothalamic-pituitary-adrenal axis. Dev Psychopathol. 2014;26(4 Pt 2):1321–1335.
  • De Kloet ER, Otte C, Kumsta R, et al. Stress and depression: a crucial role of the mineralocorticoid receptor. J Neuroendocrinol. 2016;28(8):12379. https://doi.org/10.1111/jne.12379.
  • Owens SA, Helms SW, Rudolph KD, et al. 2018. Interpersonal stress severity longitudinally predicts adolescent girls’ depressive symptoms: the moderating role of subjective and HPA axis stress responses. J Abnorm Child Psychol. 2019;47(5):895–905.
  • Tsilimigras MC, Gharaibeh RZ, Sioda M, et al. Interactions between stress and sex in microbial responses within the microbiota-gut-brain axis in a mouse model. Psychosom Med. 2018;80:361–369.
  • Ziabreva I, Poeggel G, Schnabel R, et al. Separation-induced receptor changes in the hippocampus and amygdala of Octodon degus: influence of maternal vocalizations. J Neurosci. 2003;23(12):5329–5336.
  • Vicentic A, Francis D, Moffett M, et al. Maternal separation alters serotonergic transporter densities and serotonergic 1A receptors in rat brain. Neuroscience. 2006;140(1):355–365.
  • Neumaier JF, Edwards E, Plotsky PM. 5-HT1B mRNA regulation in two animal models of altered stress reactivity. Biol Psychiatry. 2002;51(11):902–908.
  • Arborelius L, Hawks BW, Owens MJ, et al. Increased responsiveness of presumed 5-HT cells to citalopram in adult rats subjected to prolonged maternal separation relative to brief separation. Psychopharmacology (Berl). 2004;176(3–4):248–255.
  • Mahar I, Bambico FR, Mechawar N, et al. Stress, serotonin, and hippocampal neurogenesis in relation to depression and antidepressant effects. Neurosci Biobehav Rev. 2014;38:173–192.
  • Kasper S, Tauscher J, Willeit M, et al. Receptor and transporter imaging studies in schizophrenia, depression, bulimia and tourette’s disorder-implications for psychopharmacology. World J Biol Psychiatry. 2002;3(3):133–146.
  • Thompson MD, Kenna GA. Variation in the serotonin transporter gene and alcoholism: risk and response to pharmacotherapy. Alcohol Alcohol. 2016;51(2):164–171.
  • Kranz GS, Wadsak W, Kaufmann U, et al. High-dose testosterone treatment increases serotonin transporter binding in transgender people. Biol Psychiatry. 2015;78(8):525–533.
  • Wellman CL. Dendritic reorganization in pyramidal neurons in medial prefrontal cortex after chronic corticosterone administration. J Neurobiol. 2001;49(3):245–253.
  • Cook SC, Wellman CL. Chronic stress alters dendritic morphology in rat medial prefrontal cortex. J Neurobiol. 2004;60(2):236–248.
  • Grailhe R, Cardona A, Even N, et al. Regional changes in the cholinergic system in mice lacking monoamine oxidase A. Brain Res Bull. 2009;78(6):283–289.
  • Vorhees CV, Williams MT. Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat Protoc. 2006;1(2):848–858.
  • Sprowles JL, Hufgard JR, Gutierrez A, et al. Perinatal exposure to the selective serotonin reuptake inhibitor citalopram alters spatial learning and memory, anxiety, depression, and startle in Sprague-Dawley rats. Int J Dev Neurosci. 2016;54:39–52.
  • de Quervain DJF, Aerni A, Schelling G, et al. Glucocorticoids and the regulation of memory in health and disease. Front Neuroendocrinol. 2009;30(3):358–370.
  • Mendez MA, Horder J, Myers J, et al. The brain GABA-benzodiazepine receptor alpha-5 subtype in autism spectrum disorder: a pilot [(11)C]Ro15-4513 positron emission tomography study. Neuropharmacology. 2013;68:195–201.
  • de Fátima O-SI, Pereira SR, Fernandes PA, et al. Mild thiamine deficiency and chronic ethanol consumption modulate acetylcholinesterase activity change and ­spatial memory performance in a water maze task. J Mol Neurosci. 2015;55(1):217–226.
  • Furey ML, Pietrini P, Haxby J. Cholinergic enhancement and increased selectivity of perceptual processing during working memory. Science. 2000;290(5500):2315–2319.
  • Freo U, Ricciardi E, Pietrini P, et al. Pharmacological modulation of prefrontal cortical activity during a working memory task in young and older humans: a PET study with physostigmine. AJP. 2005;162(11):2061–2070.
  • Akirav I, Maroun M. Ventromedial prefrontal cortex is obligatory for consolidation and reconsolidation of object recognition memory. Cereb Cortex. 2006;16(12):1759–1765.
  • Cerqueira JJ, Pêgo JM, Taipa R, et al. Morphological correlates of corticosteroid-induced changes in prefrontal cortex-dependent behaviors. J Neurosci. 2005;25(34):7792–7800.
  • Cerqueira JJ, Taipa R, Uylings HB, et al. Specific configuration of dendritic degeneration in pyramidal neurons of the medial prefrontal cortex induced by differing corticosteroid regimens. Cereb Cortex. 2007;17(9):1998–2006.
  • Swanson LW, Cowan WM. An autoradiographic study of the organization of the efferent connections of the hippocampal formation in the rat. J Comp Neurol. 1977;172(1):49–84.
  • Anderson MC, Bunce JG, Barbas H. Prefrontal–hippocampal pathways underlying inhibitory control over memory. Neurobiol Learn Memory. 2016;134:145–161.
  • Depue BE, Curran T, Banich MT. Prefrontal regions orchestrate suppression of emotional memories via a two-phase process. Science. 2007;317(5835):215–219.
  • Levy BJ, Anderson MC. Purging of memories from conscious awareness tracked in the human brain. J Neurosci. 2012;32(47):16785–16794.
  • Ota Y, Ago Y, Tanaka T, et al. Anxiolytic-like effects of restraint during the dark cycle in adolescent mice. Behav Brain Res. 2015;284:103–111.
  • King MV, Marsden CA, Fone KC. A role for the 5-HT(1A), 5-HT4 and 5-HT6 receptors in learning and memory. Trends Pharmacol Sci. 2008;29(9):482–492.
  • Karabeg MM, Grauthoff S, Kollert SY, et al. 5-HTT deficiency affects neuroplasticity and increases stress sensitivity resulting in altered spatial learning performance in the Morris water maze but not in the barnes maze. PloS One. 2013;8(10):e78238.
  • Nyarko JN, Quartey MO, Heistad RM, et al. Glycosylation states of pre-and post-synaptic markers of 5-HT neurons differ with sex and 5-HTTLPR genotype in cortical autopsy samples. Front Neurosci. 2018;12:545.

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