Effects of stress on behavioral flexibility in rodents

Neuroscience

Volumn 345, Issue , 2017, Pages 176-192

  Hurtubise, Jessica L ^a   Howland, John G ^a  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

attentional set shifting task; norepinephrine; reversal learning; serotonin; set shifting; strategy

Indexed keywords

3 [2 [2 (4 METHYL 1 PIPERIDINYL)ETHYL] 1 PYRROLIDINESULFONYL]PHENOL; 6 CHLORO 2,3,4,5 TETRAHYDRO 7,8 DIHYDROXY 1 PHENYL 1H 3 BENZAZEPINE; AMANTADINE; ATIPAMEZOLE; BENOXATHIAN; BRAIN DERIVED NEUROTROPHIC FACTOR; CATECHOLAMINE; CITALOPRAM; CORTICOSTERONE; CORTICOSTERONE RECEPTOR; DESIPRAMINE; DEXANABINOL; DOPAMINE RECEPTOR; ESCITALOPRAM; FLUOXETINE; GLUTAMIC ACID; HORMONE RECEPTOR; KETAMINE; METYRAPONE; MIFEPRISTONE; MILNACIPRAN; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NOMIFENSINE; NORADRENALIN; NORADRENALIN UPTAKE INHIBITOR; SEROTONIN; SPIRONOLACTONE; UNCLASSIFIED DRUG; UNINDEXED DRUG; VORTIOXETINE;

ACUTE STRESS; ANIMAL BEHAVIOR; ANTIDEPRESSANT ACTIVITY; ARTICLE; BEHAVIOR; BEHAVIORAL FLEXIBILITY; CHRONIC STRESS; COGNITION; COLD STRESS; CONNECTOME; DRUG MECHANISM; HORMONE INHIBITION; HORMONE SYNTHESIS; HUMAN; LEARNING; LEARNING DISORDER; NONHUMAN; RECEPTOR BLOCKING; REPETITION PRIMING; RODENT; SET SHIFTING TASK; TASK PERFORMANCE; TREATMENT DURATION; ANIMAL; ATTENTION; EXECUTIVE FUNCTION; MENTAL STRESS; METABOLISM; PHYSIOLOGY;

ANIMALS; ATTENTION; EXECUTIVE FUNCTION; HUMANS; REVERSAL LEARNING; RODENTIA; STRESS, PSYCHOLOGICAL;

EID: 84964587126     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2016.04.007     Document Type: Article

References (147)

1. Aloi, M., Rania, M., Caroleo, M., Bruni, A., Palmieri, A., Cauteruccio, M., De Fazio, P., Segura-García, C., Decision making, central coherence and set-shifting: a comparison between binge eating disorder, anorexia nervosa and healthy controls. BMC Psychiatry, 15, 2015, 6.
2. An, K., Salyer, J., Brown, R.E., Kao, H.-F.S., Starkweather, A., Shim, I., Salivary biomarkers of chronic psychosocial stress and CVD risks: a systematic review. Biol Res Nurs, 2015 in press.
3. Anisman, H., Matheson, K., Stress, depression, and anhedonia: caveats concerning animal models. Neurosci Biobehav Rev 29 (2005), 525–546.
4. Arnsten, A.F.T., Stress signalling pathways that impair prefrontal cortex structure and function. Nat Rev Neurosci 10 (2009), 410–422.
5. Arnsten, A.F.T., Stress weakens prefrontal networks: molecular insults to higher cognition. Nat Neurosci 18 (2015), 1376–1385.
6. Atmaca, M., Yildirim, H., Ozdemir, H., Tezcan, E., Kursad Poyraz, A., Volumetric MRI study of key brain regions implicated in obsessive–compulsive disorder. Prog Neuropsychopharmacol Biol Psychiatry 31 (2007), 46–52.
7. Balleine, B.W., O'Doherty, J.P., Human and rodent homologies in action control: corticostriatal determinants of goal-directed and habitual action. Neuropsychopharmacology 35 (2010), 48–69.
8. Ballendine, S.A., Greba, Q., Dawicki, W., Zhang, X., Gordon, J.R., Howland, J.G., Behavioral alterations in rat offspring following maternal immune activation and ELR-CXC chemokine receptor antagonism during pregnancy: implications for neurodevelopmental psychiatric disorders. Prog Neuropsychopharmacol Biol Psychiatry 57 (2015), 155–165.
9. Birrell, J.M., Brown, V.J., Medial frontal cortex mediates perceptual attentional set shifting in the rat. J Neurosci 20 (2000), 4320–4324.
10. Bissonette, G.B., Roesch, M.R., Neural correlates of rules and conflict in medial prefrontal cortex during decision and feedback epochs. Front Behav Neurosci, 9, 2015 Available at: http://journal.frontiersin.org/article/10.3389/fnbeh.2015.00266 [Accessed November 1, 2015].
11. Bissonette, G.B., Martins, G.J., Franz, T.M., Harper, E.S., Schoenbaum, G., Powell, E.M., Double dissociation of the effects of medial and orbital prefrontal cortical lesions on attentional and affective shifts in mice. J Neurosci 28 (2008), 11124–11130.
12. Bissonette, G.B., Powell, E.M., Roesch, M.R., Neural structures underlying set-shifting: roles of medial prefrontal cortex and anterior cingulate cortex. Behav Brain Res 250 (2013), 91–101.
13. Block, A.E., Dhanji, H., Thompson-Tardif, S.F., Floresco, S.B., Thalamic-prefrontal cortical-ventral striatal circuitry mediates dissociable components of strategy set shifting. Cereb Cortex 17 (2007), 1625–1636.
14. Bondi, C.O., Rodriguez, G., Gould, G.G., Frazer, A., Morilak, D.A., Chronic unpredictable stress induces a cognitive deficit and anxiety-like behavior in rats that is prevented by chronic antidepressant drug treatment. Neuropsychopharmacology 33 (2008), 320–331.
15. Bondi, C.O., Jett, J.D., Morilak, D.A., Beneficial effects of desipramine on cognitive function of chronically stressed rats are mediated by α1-adrenergic receptors in medial prefrontal cortex. Prog Neuropsychopharmacol Biol Psychiatry 34 (2010), 913–923.
16. Boulougouris, V., Dalley, J.W., Robbins, T.W., Effects of orbitofrontal, infralimbic and prelimbic cortical lesions on serial spatial reversal learning in the rat. Behav Brain Res 179 (2007), 219–228.
17. Brady, A.M., Floresco, S.B., Operant procedures for assessing behavioral flexibility in rats. J Vis Exp, 96, 2015, e52387.
18. Brown, S.M., Mild, short-term stress alters dendritic morphology in rat medial prefrontal cortex. Cereb Cortex 15 (2005), 1714–1722.
19. Brown, V.J., Tait, D.S., Behavioral flexibility: attentional shifting, rule switching, and response reversal. Encycl Psychopharmacol, 2014, 1–7.
20. Bryce, C.A., Howland, J.G., Stress facilitates late reversal learning using a touchscreen-based visual discrimination procedure in male Long Evans rats. Behav Brain Res 278 (2015), 21–28.
21. Bryden, D.W., Roesch, M.R., Executive control signals in orbitofrontal cortex during response inhibition. J Neurosci 35 (2015), 3903–3914.
22. Burgdorf, J., Kroes, R.A., Zhang, X., Gross, A.L., Schmidt, M., Weiss, C., Disterhoft, J.F., Burch, R.M., Stanton, P.K., Moskal, J.R., Rapastinel (GLYX-13) has therapeutic potential for the treatment of post-traumatic stress disorder: characterization of a NMDA receptor-mediated metaplasticity process in the medial prefrontal cortex of rats. Behav Brain Res 294 (2015), 177–185.
23. Butler, M., Retzlaff, P.D., Vanderploeg, R., Neuropsychological test usage. Prof Psychol Res Pract 22 (1991), 510–512.
24. Butts, K.A., Weinberg, J., Young, A.H., Phillips, A.G., Glucocorticoid receptors in the prefrontal cortex regulate stress-evoked dopamine efflux and aspects of executive function. Proc Natl Acad Sci USA 108 (2011), 18459–18464.
25. Butts, K.A., Floresco, S.B., Phillips, A.G., Acute stress impairs set-shifting but not reversal learning. Behav Brain Res 252 (2013), 222–229.
26. Buynitsky, T., Mostofsky, D.I., Restraint stress in biobehavioral research: recent developments. Neurosci Biobehav Rev 33 (2009), 1089–1098.
27. Cazakoff, B.N., Johnson, K.J., Howland, J.G., Converging effects of acute stress on spatial and recognition memory in rodents: a review of recent behavioural and pharmacological findings. Prog Neuropsychopharmacol Biol Psychiatry 34 (2010), 733–741.
28. Chaijale, N.N., Snyder, K., Arner, J., Curtis, A.L., Valentino, R.J., Repeated social stress increases reward salience and impairs encoding of prediction by rat locus coeruleus neurons. Neuropsychopharmacology 40 (2015), 513–523.
29. Cho, K.K.A., Hoch, R., Lee, A.T., Patel, T., Rubenstein, J.L.R., Sohal, V.S., Gamma rhythms link prefrontal interneuron dysfunction with cognitive inflexibility in Dlx5/6+/− Mice. Neuron 85 (2015), 1332–1343.
30. Chudasama, Y., Kralik, J., Murray, E., Rhesus monkeys with orbital prefrontal cortex lesions can learn to inhibit prepotent responses in the reversed reward contingency task. Cereb Cortex 17 (2006), 1154–1159.
31. Cook, S.C., Wellman, C.L., Chronic stress alters dendritic morphology in rat medial prefrontal cortex. J Neurobiol 60 (2004), 236–248.
32. Cools, R., Clark, L., Owen, A.M., Robbins, T.W., Defining the neural mechanisms of probabilistic reversal learning using event-related functional magnetic resonance imaging. J Neurosci 22 (2002), 4563–4567.
33. Cozzoli, D.K., Tanchuck-Nipper, M.A., Kaufman, M.N., Horowitz, C.B., Finn, D.A., Environmental stressors influence limited-access ethanol consumption by C57BL/6J mice in a sex-dependent manner. Alcohol 48 (2014), 741–754.
34. Curtis, A.L., Lechner, S.M., Pavcovich, L.A., Valentino, R.J., Activation of the locus coeruleus noradrenergic system by intracoerulear microinfusion of corticotropin-releasing factor: effects on discharge rate, cortical norepinephrine levels and cortical electroencephalographic activity. J Pharmacol Exp Ther 281 (1997), 163–172.
35. Dajani, D.R., Uddin, L.Q., Demystifying cognitive flexibility: implications for clinical and developmental neuroscience. Trends Neurosci 38 (2015), 571–578.
36. Danet, M., Lapiz-Bluhm, S., Morilak, D.A., A cognitive deficit induced in rats by chronic intermittent cold stress is reversed by chronic antidepressant treatment. Int J Neuropsychopharmacol 13 (2010), 997–1009.
37. Darcet, F., Mendez-David, I., Tritschler, L., Gardier, A.M., Guilloux, J.-P., David, D.J., Learning and memory impairments in a neuroendocrine mouse model of anxiety/depression. Front Behav Neurosci, 8, 2014, 136.
38. de Kloet, E.R., Joëls, M., Holsboer, F., Stress and the brain: from adaptation to disease. Nat Rev Neurosci 6 (2005), 463–475.
39. Déziel, R.A., Ryan, C.L., Tasker, R.A., Ischemic lesions localized to the medial prefrontal cortex produce selective deficits in measures of executive function in rats. Behav Brain Res 293 (2015), 54–61.
40. Diamond, D.M., Campbell, A.M., Park, C.R., Halonen, J., Zoladz, P.R., The temporal dynamics model of emotional memory processing: a synthesis on the neurobiological basis of stress-induced amnesia, flashbulb and traumatic memories, and the Yerkes-Dodson law. Neural Plast 2007 (2007), 1–33.
41. Dias-Ferreira, E., Sousa, J.C., Melo, I., Morgado, P., Mesquita, A.R., Cerqueira, J.J., Costa, R.M., Sousa, N., Chronic stress causes frontostriatal reorganization and affects decision-making. Science 325 (2009), 621–625.
42. Dickens, M.J., Romero, L.M., A consensus endocrine profile for chronically stressed wild animals does not exist. Gen Comp Endocrinol 191 (2013), 177–189.
43. Dong, Z., Bai, Y., Wu, X., Li, H., Gong, B., Howland, J.G., Huang, Y., He, W., Li, T., Wang, Y.T., Hippocampal long-term depression mediates spatial reversal learning in the Morris water maze. Neuropharmacology 64 (2013), 65–73.
44. Durstewitz, D., Vittoz, N.M., Floresco, S.B., Seamans, J.K., Abrupt transitions between prefrontal neural ensemble states accompany behavioral transitions during rule learning. Neuron 66 (2010), 438–448.
45. Eiland, L., Ramroop, J., Hill, M.N., Manley, J., McEwen, B.S., Chronic juvenile stress produces corticolimbic dendritic architectural remodeling and modulates emotional behavior in male and female rats. Psychoneuroendocrinology 37 (2012), 39–47.
46. D'Este, L., Casini, A., Puglisi-Allegra, S., Cabib, S., Renda, T.G., Comparative immunohistochemical study of the dopaminergic systems in two inbred mouse strains (C57BL/6J and DBA/2J). J Chem Neuroanat 33 (2007), 67–74.
47. Euston, D.R., Gruber, A.J., McNaughton, B.L., The role of medial prefrontal cortex in memory and decision making. Neuron 76 (2012), 1057–1070.
48. Fineberg, N.A., Day, G.A., de Koenigswarter, N., Reghunandanan, S., Kolli, S., Jefferies-Sewell, K., Hranov, G., Laws, K.R., The neuropsychology of obsessive-compulsive personality disorder: a new analysis. CNS Spectr 20 (2015), 490–499.
49. Finlay, J.M., Zigmond, M.J., Abercrombie, E.D., Increased dopamine and norepinephrine release in medial prefrontal cortex induced by acute and chronic stress: effects of diazepam. Neuroscience 64 (1995), 619–628.
50. Flak, J.N., Myers, B., Solomon, M.B., McKlveen, J.M., Krause, E.G., Herman, J.P., Role of paraventricular nucleus-projecting norepinephrine/epinephrine neurons in acute and chronic stress. Eur J Neurosci 39 (2014), 1903–1911.
51. Floresco, S.B., Magyar, O., Ghods-Sharifi, S., Vexelman, C., Tse, M.T.L., Multiple dopamine receptor subtypes in the medial prefrontal cortex of the rat regulate set-shifting. Neuropsychopharmacology 31 (2006), 297–309.
52. Floresco, S.B., Block, A.E., Tse, M.T.L., Inactivation of the medial prefrontal cortex of the rat impairs strategy set-shifting, but not reversal learning, using a novel, automated procedure. Behav Brain Res 190 (2008), 85–96.
53. Floresco, S.B., Zhang, Y., Enomoto, T., Neural circuits subserving behavioral flexibility and their relevance to schizophrenia. Behav Brain Res 204 (2009), 396–409.
54. Fox, J.H., Lowry, C.A., Corticotropin-releasing factor-related peptides, serotonergic systems, and emotional behavior. Front Neurosci, 7, 2013, 169.
55. George, S.A., Rodriguez-Santiago, M., Riley, J., Abelson, J.L., Floresco, S.B., Liberzon, I., Alterations in cognitive flexibility in a rat model of post-traumatic stress disorder. Behav Brain Res 286 (2015), 256–264.
56. Ghods-Sharifi, S., Haluk, D.M., Floresco, S.B., Differential effects of inactivation of the orbitofrontal cortex on strategy set-shifting and reversal learning. Neurobiol Learn Mem 89 (2008), 567–573.
57. Goldstein, D.S., McEwen, B., Allostasis, homeostats, and the nature of stress. Stress 5 (2002), 55–58.
58. Goldwater, D.S., Pavlides, C., Hunter, R.G., Bloss, E.B., Hof, P.R., McEwen, B.S., Morrison, J.H., Structural and functional alterations to rat medial prefrontal cortex following chronic restraint stress and recovery. Neuroscience 164 (2009), 798–808.
59. Graybeal, C., Feyder, M., Schulman, E., Saksida, L.M., Bussey, T.J., Brigman, J.L., Holmes, A., Paradoxical reversal learning enhancement by stress or prefrontal cortical damage: rescue with BDNF. Nat Neurosci 14 (2011), 1507–1509.
60. Graybeal, C., Bachu, M., Mozhui, K., Saksida, L.M., Bussey, T.J., Sagalyn, E., Williams, R.W., Holmes, A., Strains and stressors: an analysis of touchscreen learning in genetically diverse mouse strains. PLoS ONE, 9, 2014, e87745.
61. Haluk, D.M., Floresco, S.B., Ventral striatal dopamine modulation of different forms of behavioral flexibility. Neuropsychopharmacology 34 (2009), 2041–2052.
62. Hamilton, D.A., Brigman, J.L., Behavioral flexibility in rats and mice: contributions of distinct frontocortical regions. Genes Brain Behav 14 (2015), 4–21.
63. Heisler, J.M., Morales, J., Donegan, J.J., Jett, J.D., Redus, L., O'Connor, J.C., The attentional set shifting task: a measure of cognitive flexibility in mice. J Vis Exp, 96, 2015, 52387.
64. Herman, J.P., Spencer, R., Regulation of hippocampal glucocorticoid receptor gene transcription and protein expression in vivo. J Neurosci 18 (1998), 7462–7473.
65. Hill, M.N., Patel, S., Carrier, E.J., Rademacher, D.J., Ormerod, B.K., Hillard, C.J., Gorzalka, B.B., Downregulation of endocannabinoid signaling in the hippocampus following chronic unpredictable stress. Neuropsychopharmacology 30 (2005), 508–515.
66. Holmes, A., Wellman, C.L., Stress-induced prefrontal reorganization and executive dysfunction in rodents. Neurosci Biobehav Rev 33 (2009), 773–783.
67. Horn, N.R., Dolan, M., Elliott, R., Deakin, J.F.W., Woodruff, P.W.R., Response inhibition and impulsivity: an fMRI study. Neuropsychologia 41 (2003), 1959–1966.
68. Hornak, J., O'Doherty, J., Bramham, J., Rolls, E.T., Morris, R.G., Bullock, P.R., Polkey, C.E., Reward-related reversal learning after surgical excisions in orbito-frontal or dorsolateral prefrontal cortex in humans. J Cogn Neurosci 16 (2004), 463–478.
69. Hou, J., Wu, W., Lin, Y., Wang, J., Zhou, D., Guo, J., Gu, S., He, M., Ahmed, S., Hu, J., Qu, W., Li, H., Localization of cerebral functional deficits in patients with obsessive–compulsive disorder: a resting-state fMRI study. J Affect Disord 138 (2012), 313–321.
70. Howland, J.G., Wang, Y.T., Chapter 8 Synaptic plasticity in learning and memory: stress effects in the hippocampus. Prog Brain Res, 2008, Elsevier, 145–158 Available at: http://linkinghub.elsevier.com/retrieve/pii/S0079612307000088 [Accessed October 28, 2015].
71. Ishikawa, M., Ohdo, S., Watanabe, H., Hara, C., Ogawa, N., Alteration in circadian rhythm of plasma corticosterone in rats following sociopsychological stress induced by communication box. Physiol Behav 57 (1995), 41–47.
72. Itoi, K., Suda, T., Tozawa, F., Dobashi, I., Ohmori, N., Sakai, Y., Abe, K., Demura, H., Microinjection of norepinephrine into the paraventricular nucleus of the hypothalamus stimulates corticotropin-releasing factor gene expression in conscious rats. Endocrinology 135 (1994), 2177–2182.
73. Izquierdo, A., Suda, R.K., Murray, E.A., Bilateral orbital prefrontal cortex lesions in rhesus monkeys disrupt choices guided by both reward value and reward contingency. J Neurosci 24 (2004), 7540–7548.
74. Izquierdo, A., Brigman, J.L., Radke, A.K., Rudebeck, P.H., Holmes, A., The neural basis of reversal learning: an updated perspective. Neuroscience 345 (2017), 12–26.
75. Jett, J.D., Morilak, D.A., Too much of a good thing: blocking noradrenergic facilitation in medial prefrontal cortex prevents the detrimental effects of chronic stress on cognition. Neuropsychopharmacology 38 (2013), 585–595.
76. Jett, J.D., Boley, A.M., Girotti, M., Shah, A., Lodge, D.J., Morilak, D.A., Antidepressant-like cognitive and behavioral effects of acute ketamine administration associated with plasticity in the ventral hippocampus to medial prefrontal cortex pathway. Psychopharmacology 232 (2015), 3123–3133.
77. Kalsbeek, A., van der Spek, R., Lei, J., Endert, E., Buijs, R.M., Fliers, E., Circadian rhythms in the hypothalamo–pituitary–adrenal (HPA) axis. Mol Cell Endocrinol 349 (2012), 20–29.
78. Kehagia, A.A., Murray, G.K., Robbins, T.W., Learning and cognitive flexibility: frontostriatal function and monoaminergic modulation. Curr Opin Neurobiol 20 (2010), 199–204.
79. Kendler, K.S., Karkowski, L.M., Prescott, C.A., Causal relationship between stressful life events and the onset of major depression. Am J Psychiatry 156 (1999), 837–841.
80. Kesner, R.P., Churchwell, J.C., An analysis of rat prefrontal cortex in mediating executive function. Neurobiol Learn Mem 96 (2011), 417–431.
81. Kim, J.J., Diamond, D.M., The stressed hippocampus, synaptic plasticity and lost memories. Nat Rev Neurosci 3 (2002), 453–462.
82. Kitraki, E., Kremmyda, O., Youlatos, D., Alexis, M.N., Kittas, C., Gender-dependent alterations in corticosteroid receptor status and spatial performance following 21 days of restraint stress. Neuroscience 125 (2004), 47–55.
83. Knox, D., Nault, T., Henderson, C., Liberzon, I., Glucocorticoid receptors and extinction retention deficits in the single prolonged stress model. Neuroscience 223 (2012), 163–173.
84. Koolhaas, J.M., Bartolomucci, A., Buwalda, B., de Boer, S.F., Flügge, G., Korte, S.M., Meerlo, P., Murison, R., Olivier, B., Palanza, P., Richter-Levin, G., Sgoifo, A., Steimer, T., Stiedl, O., van Dijk, G., Wöhr, M., Fuchs, E., Stress revisited: a critical evaluation of the stress concept. Neurosci Biobehav Rev 35 (2011), 1291–1301.
85. Kvarta, M.D., Bradbrook, K.E., Dantrassy, H.M., Bailey, A.M., Thompson, S.M., Corticosterone mediates the synaptic and behavioral effects of chronic stress at rat hippocampal temporoammonic synapses. J Neurophysiol 114 (2015), 1713–1724.
86. Lapiz, M.D.S., Morilak, D.A., Noradrenergic modulation of cognitive function in rat medial prefrontal cortex as measured by attentional set shifting capability. Neuroscience 137 (2006), 1039–1049.
87. Lapiz-Bluhm, M.D.S., Soto-Piña, A.E., Hensler, J.G., Morilak, D.A., Chronic intermittent cold stress and serotonin depletion induce deficits of reversal learning in an attentional set-shifting test in rats. Psychopharmacology 202 (2009), 329–341.
88. Lee, H.S., Kim, D.-K., Kim, Y.B., Lee, K.J., Effect of acute stress on immune cell counts and the expression of tight junction proteins in the duodenal mucosa of rats. Gut Liver 7 (2013), 190–196.
89. Liston, C., Miller, M.M., Goldwater, D.S., Radley, J.J., Rocher, A.B., Hof, P.R., Morrison, J.H., McEwen, B.S., Stress-induced alterations in prefrontal cortical dendritic morphology predict selective impairments in perceptual attentional set-shifting. J Neurosci 26 (2006), 7870–7874.
90. Lupien, S.J., Maheu, F., Tu, M., Fiocco, A., Schramek, T.E., The effects of stress and stress hormones on human cognition: implications for the field of brain and cognition. Brain Cogn 65 (2007), 209–237.
91. McAlonan, K., Brown, V.J., Orbital prefrontal cortex mediates reversal learning and not attentional set shifting in the rat. Behav Brain Res 146 (2003), 97–103.
92. McEwen, B.S., Bowles, N.P., Gray, J.D., Hill, M.N., Hunter, R.G., Karatsoreos, I.N., Nasca, C., Mechanisms of stress in the brain. Nat Neurosci 18 (2015), 1353–1363.
93. McEwen, B.S., Wingfield, J.C., The concept of allostasis in biology and biomedicine. Horm Behav 43 (2003), 2–15.
94. Millstein, R.A., Holmes, A., Effects of repeated maternal separation on anxiety- and depression-related phenotypes in different mouse strains. Neurosci Biobehav Rev 31 (2007), 3–17.
95. Mizoguchi, K., Ishige, A., Aburada, M., Tabira, T., Chronic stress attenuates glucocorticoid negative feedback: involvement of the prefrontal cortex and hippocampus. Neuroscience 119 (2003), 887–897.
96. Moorman, D.E., Aston-Jones, G., Orbitofrontal cortical neurons encode expectation-driven initiation of reward-seeking. J Neurosci 34 (2014), 10234–10246.
97. Naegeli, K.J., O'Connor, J.A., Banerjee, P., Morilak, D.A., Effects of milnacipran on cognitive flexibility following chronic stress in rats. Eur J Pharmacol 703 (2013), 62–66.
98. Nava, N., Treccani, G., Liebenberg, N., Chen, F., Popoli, M., Wegener, G., Nyengaard, J.R., Chronic desipramine prevents acute stress-induced reorganization of medial prefrontal cortex architecture by blocking glutamate vesicle accumulation and excitatory synapse increase. Int J Neuropsychopharmacol, 18, 2015, pyu085.
99. Nikiforuk, A., Selective blockade of 5-HT7 receptors facilitates attentional set-shifting in stressed and control rats. Behav Brain Res 226 (2012), 118–123.
100. Nikiforuk, A., Dopamine D1 receptor modulation of set shifting: the role of stress exposure. Behav Pharmacol 23 (2012), 434–438.
101. Nikiforuk, A., Popik, P., Long-lasting cognitive deficit induced by stress is alleviated by acute administration of antidepressants. Psychoneuroendocrinology 36 (2011), 28–39.
102. Nikiforuk, A., Popik, P., Neurochemical modulation of stress-induced cognitive inflexibility in a rat model of an attentional set-shifting task. Pharmacol Rep 65 (2013), 1479–1488.
103. Nikiforuk, A., Popik, P., Ketamine prevents stress-induced cognitive inflexibility in rats. Psychoneuroendocrinology 40 (2014), 119–122.
104. Nilsson, S.R.O., Alsiö, J., Somerville, E.M., Clifton, P.G., The rat's not for turning: dissociating the psychological components of cognitive inflexibility. Neurosci Biobehav Rev 56 (2015), 1–14.
105. Nonkes, L.J.P., van de Vondervoort, I.I.G.M., de Leeuw, M.J.C., Wijlaars, L.P., Maes, J.H.R., Homberg, J.R., Serotonin transporter knockout rats show improved strategy set-shifting and reduced latent inhibition. Learn Mem 19 (2012), 190–193.
106. Odlaug, B.L., Chamberlain, S.R., Grant, J.E., Motor inhibition and cognitive flexibility in pathologic skin picking. Prog Neuropsychopharmacol Biol Psychiatry 34 (2010), 208–211.
107. Papadopoulou, A., Siamatras, T., Delgado-Morales, R., Amin, N.D., Shukla, V., Zheng, Y.-L., Pant, H.C., Almeida, O.F.X., Kino, T., Acute and chronic stress differentially regulate cyclin-dependent kinase 5 in mouse brain: implications to glucocorticoid actions and major depression. Transl Psychiatry, 5, 2015, e578.
108. Placek, K., Dippel, W.C., Jones, S., Brady, A.M., Impairments in set-shifting but not reversal learning in the neonatal ventral hippocampal lesion model of schizophrenia: further evidence for medial prefrontal deficits. Behav Brain Res 256 (2013), 405–413.
109. Plumb, T.N., Cullen, P.K., Minor, T.R., Parameters of hormetic stress and resilience to trauma in rats. Stress 18 (2015), 88–95.
110. Quan, M., Zheng, C., Zhang, N., Han, D., Tian, Y., Zhang, T., Yang, Z., Impairments of behavior, information flow between thalamus and cortex, and prefrontal cortical synaptic plasticity in an animal model of depression. Brain Res Bull 85 (2011), 109–116.
111. Rabinovici, G.D., Stephens, M.L., Possin, K.L., Executive dysfunction.Continuum (Minneap Minn)., 21, 2015, 646–659.
112. Ragozzino, M.E., The effects of dopamine D1 receptor blockade in the prelimbic-infralimbic areas on behavioral flexibility. Learn Mem 9 (2002), 18–28.
113. Ragozzino, M.E., Detrick, S., Kesner, R.P., Involvement of the prelimbic-infralimbic areas of the rodent prefrontal cortex in behavioral flexibility for place and response learning. J Neurosci 19 (1999), 4585–4594.
114. Razzoli, M., McCallum, J., Gurney, A., Engeland, W.C., Bartolomucci, A., Chronic stress aggravates glucose intolerance in leptin receptor-deficient (db/db) mice. Genes Nutr, 10, 2015, 8.
115. Remijnse, P.L., van den Heuvel, O.A., Nielen, M.M.A., Vriend, C., Hendriks, G.-J., Hoogendijk, W.J.G., Uylings, H.B.M., Veltman, D.J., Cognitive inflexibility in obsessive-compulsive disorder and major depression is associated with distinct neural correlates. PLoS One, 8, 2013, e59600.
116. Romeo, R.D., Ali, F.S., Karatsoreos, I.N., Bellani, R., Chhua, N., Vernov, M., McEwen, B.S., Glucocorticoid receptor mRNA expression in the hippocampal formation of male rats before and after pubertal development in response to acute or repeated stress. Neuroendocrinology 87 (2008), 160–167.
117. Romero, L.M., Platts, S.H., Schoech, S.J., Wada, H., Crespi, E., Martin, L.B., Buck, C.L., Understanding stress in the healthy animal – potential paths for progress. Stress 18 (2015), 491–497.
118. Roozendaal, B., Glucocorticoids and the regulation of memory consolidation. Psychoneuroendocrinology 25 (2000), 213–238.
119. Roy, J.E., Riesenhuber, M., Poggio, T., Miller, E.K., Prefrontal cortex activity during flexible categorization. J Neurosci 30 (2010), 8519–8528.
120. Rudebeck, P.H., Murray, E.A., The orbitofrontal oracle: cortical mechanisms for the prediction and evaluation of Specific Behavioral Outcomes. Neuron 84 (2014), 1143–1156.
121. Rudebeck, P.H., Saunders, R.C., Prescott, A.T., Chau, L.S., Murray, E.A., Prefrontal mechanisms of behavioral flexibility, emotion regulation and value updating. Nat Neurosci 16 (2013), 1140–1145.
122. Ruys, J., Mendoza, S., Capitanio, J., Mason, W., Behavioral and physiological adaptation to repeated chair restraint in rhesus macaques. Physiol Behav 82 (2004), 205–213.
123. Sapolsky, R.M., Glucocorticoids and hippocampal atrophy in neuropsychiatric disorders. Arch Gen Psychiatry 57 (2000), 925–935.
124. Sapolsky, R.M., Romero, L.M., Munck, A.U., How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21 (2000), 55–89.
125. Scheggia, D., Papaleo, F., An operant intra-/extra-dimensional set-shift task for mice. J Vis Exp, 2016 Available at: http://www.jove.com/video/53503/an-operant-intra-extra-dimensional-set-shift-task-for-mice (Accessed February 26, 2016).
126. Schoenbaum, G., Lesions of orbitofrontal cortex and basolateral amygdala complex disrupt acquisition of odor-guided discriminations and reversals. Learn Mem 10 (2003), 129–140.
127. Schwabe, L., Joëls, M., Roozendaal, B., Wolf, O.T., Oitzl, M.S., Stress effects on memory: an update and integration. Neurosci Biobehav Rev 36 (2012), 1740–1749.
128. Smitha, K.K., Mukkadan, J.K., Effect of different forms of acute stress in the generation of reactive oxygen species in albino Wistar rats. Indian J Physiol Pharmacol 58 (2014), 229–232.
129. Snyder, K., Wang, W.-W., Han, R., McFadden, K., Valentino, R.J., Corticotropin-releasing factor in the norepinephrine nucleus, locus coeruleus, facilitates behavioral flexibility. Neuropsychopharmacology 37 (2012), 520–530.
130. Snyder, K., Barry, M., Plona, Z., Ho, A., Zhang, X.-Y., Valentino, R.J., The impact of social stress during adolescence or adulthood and coping strategy on cognitive function of female rats. Behav Brain Res 286 (2015), 175–183.
131. Snyder, K.P., Hill-Smith, T.E., Lucki, I., Valentino, R.J., Corticotropin-releasing factor in the rat dorsal raphe nucleus promotes different forms of behavioral flexibility depending on social stress history. Neuropsychopharmacology 40 (2015), 2517–2525.
132. Stalnaker, T.A., Cooch, N.K., Schoenbaum, G., What the orbitofrontal cortex does not do. Nat Neurosci 18 (2015), 620–627.
133. Tait, D.S., Brown, V.J., Farovik, A., Theobald, D.E., Dalley, J.W., Robbins, T.W., Lesions of the dorsal noradrenergic bundle impair attentional set-shifting in the rat. Eur J Neurosci 25 (2007), 3719–3724.
134. Thai, C.A., Zhang, Y., Howland, J.G., Effects of acute restraint stress on set-shifting and reversal learning in male rats. Cogn Affect Behav Neurosci 13 (2013), 164–173.
135. Valentino, R.J., Van Bockstaele, E., Convergent regulation of locus coeruleus activity as an adaptive response to stress. Eur J Pharmacol 583 (2008), 194–203.
136. Van Eylen, L., Boets, B., Steyaert, J., Wagemans, J., Noens, I., Executive functioning in autism spectrum disorders: influence of task and sample characteristics and relation to symptom severity. Eur Child Adolesc Psychiatry 24 (2015), 1399–1417.
137. Vogel, S., Fernández, G., Joëls, M., Schwabe, L., Cognitive adaptation under stress: a case for the mineralocorticoid receptor. Trends Cogn Sci (Regul Ed) 20 (2016), 192–203.
138. Wallace, A., Pehrson, A.L., Sánchez, C., Morilak, D.A., Vortioxetine restores reversal learning impaired by 5-HT depletion or chronic intermittent cold stress in rats. Int J Neuropsychopharmacol 17 (2014), 1695–1706.
139. Weaver, I.C.G., Cervoni, N., Champagne, F.A., Alessio, A.C.D’, Sharma, S., Seckl, J.R., Dymov, S., Szyf, M., Meaney, M.J., Epigenetic programming by maternal behavior. Nat Neurosci 7 (2004), 847–854.
140. Woodson, J.C., Emotion-induced amnesia in rats: working memory-specific impairment, corticosterone-memory correlation, and fear versus arousal effects on memory. Learn Mem 10 (2003), 326–336.
141. Wright, R.L., Lightner, E.N., Harman, J.S., Meijer, O.C., Conrad, C.D., Attenuating corticosterone levels on the day of memory assessment prevents chronic stress-induced impairments in spatial memory. Eur J Neurosci 24 (2006), 595–605.
142. Xiang, Y., Yan, H., Zhou, J., Zhang, Q., Hanley, G., Caudle, Y., LeSage, G., Zhang, X., Yin, D., The role of toll-like receptor 9 in chronic stress-induced apoptosis in macrophage. PLoS One, 10, 2015, e0123447.
143. Yu, M., Zhang, Y., Chen, X., Zhang, T., Antidepressant-like effects and possible mechanisms of amantadine on cognitive and synaptic deficits in a rat model of chronic stress. Stress 15 (2015), 1–32.
144. Yuen, E.Y., Liu, W., Karatsoreos, I.N., Ren, Y., Feng, J., McEwen, B.S., Yan, Z., Mechanisms for acute stress-induced enhancement of glutamatergic transmission and working memory. Mol Psychiatry 16 (2011), 156–170.
145. Zhang, Y., Cazakoff, B.N., Thai, C.A., Howland, J.G., Prenatal exposure to a viral mimetic alters behavioural flexibility in male, but not female, rats. Neuropharmacology 62 (2012), 1299–1307.
146. Zhang, J., Yang, X., Yang, Q., Neuropsychological dysfunction in adults with early-onset obsessive-compulsive disorder: the search for a cognitive endophenotype. Rev Bras Psiquiatr 37 (2015), 126–132.
147. Zitnik, G.A., Curtis, A.L., Wood, S.K., Arner, J., Valentino, R.J., Adolescent social stress produces an enduring activation of the rat locus coeruleus and alters its coherence with the prefrontal cortex. Neuropsychopharmacology 41 (2016), 1376–1385.