Risk assessment behaviors associated with corticosterone trigger the defense reaction to social isolation in rats: Role of the anterior cingulate cortex

References

• Adamec RE, Blundell J, Burton P. 2005. Neural circuit changes mediating lasting brain and behavioral response to predator stress. Neurosci Biobehav Rev. 29:1225–1241.
   PubMed Web of Science ®Google Scholar
• Albrechet-Souza L, Brandão ML. 2010. Hormonal and cognitive factors associated with the exploratory behavior of rats submitted to repeated sessions of the elevated plus-maze. Psychol Neurosci. 3:43–52.
   Google Scholar
• Albrechet-Souza L, Carvalho MC, Franci CR, Brandão ML. 2007. Increases in plasma corticosterone and stretched-attend postures in rats naive and previously exposed to the elevated plus-maze are sensitive to the anxiolytic-like effects of midazolam. Horm Behav. 52:267–273.
   PubMed Web of Science ®Google Scholar
• Albrechet-Souza L, Borelli KG, Brandão ML. 2008. Activity of the medial prefrontal cortex and amygdala underlies one-trial tolerance of rats in the elevated plus-maze. J Neurosci Methods. 169:109–118.
   PubMed Web of Science ®Google Scholar
• Albrechet-Souza L, Borelli KG, Carvalho MC, Brandão ML. 2009. The anterior cingulate cortex is a target structure for the anxiolytic-like effects of benzodiazepines assessed by repeated exposure to the elevated plus-maze and Fos immunoreactivity. Neuroscience. 164:387–397.
   PubMed Web of Science ®Google Scholar
• Amaral VC, Santos Gomes K, Nunes-De-Souza RL. 2010. Increased corticosterone levels in mice subjected to the rat exposure test. Horm Behav. 57:128–133.
   PubMed Web of Science ®Google Scholar
• Andersen ML, Bignotto M, Machado RB, Tufik S. 2004. Different stress modalities result in distinct steroid hormone responses by male rats. Braz J Med Biol Res. 37:791–797.
   PubMed Web of Science ®Google Scholar
• Anseloni VCZ, Brandão ML. 1997. Ethopharmacological analysis of behaviour of rats using variations of the elevated plus-maze. Behav Pharmacol. 8:533–540.
   PubMed Web of Science ®Google Scholar
• Barsegyan A, Mackenzieb STM, Kuroseb BD, McGaughb JL, Roozendaal B. 2010. Glucocorticoids in the prefrontal cortex enhance memory consolidation and impair working memory by a common neural mechanism. Proc Natl Acad Sci USA. 107:16655–16660.
   PubMed Web of Science ®Google Scholar
• Blanchard RJ, Blanchard DC. 1989. Antipredator defensive behaviors in a visible burrow system. J Comp Psychol. 103:70–82.
   PubMed Web of Science ®Google Scholar
• Blanchard RJ, Yudko EB, Rodgers RJ, Blanchard DC. 1993. Defense system psychopharmacology: An ethological approach to the pharmacology of fear and anxiety. Behav Brain Res. 58:155–165.
   PubMed Web of Science ®Google Scholar
• Brinley-Reed M, Mascagni F, McDonald AJ. 1995. Synaptology of prefrontal projections to the basolateral amygdala: An electron microscopic study in the rat. Neurosci Lett. 202:45–48.
   PubMed Web of Science ®Google Scholar
• Brown SM, Henning S, Wellma CL. 2005. Mild, short-term stress alters dendritic morphology in rat medial prefrontal cortex. Cereb Cortex. 15:1714–1722.
   PubMed Web of Science ®Google Scholar
• Calvo N, Volosin M. 2001. Glucocorticoid and mineralocorticoid receptors are involved in the facilitation of anxiety-like response induced by restraint. Neuroendocrinology. 73:261–271.
   PubMed Web of Science ®Google Scholar
• Calvo N, Martijena ID, Molina VA, Volosin M. 1998. Metyrapone pretreatment prevents the behavioral and neurochemical sequelae induced by stress. Brain Res. 800:227–235.
   PubMed Web of Science ®Google Scholar
• Cerqueira JJ, Taipa R, Uylings HBM, Almeida FXO, Sousa N. 2007. Specific configuration of dendritic degeneration in pyramidal neurons of the medial prefrontal cortex induced by differing corticosteroid regimens. Cereb Cortex. 17:1998–2006.
   PubMed Web of Science ®Google Scholar
• Chao HM, Choo PH, McEwen BS. 1989. Glucocorticoid and mineralocorticoid receptor mRNA expression in rat brain. Neuroendocrinology. 50:365–371.
   PubMed Web of Science ®Google Scholar
• Chauveau F, Piérard C, Tronche C, Coutan M, Drouet I, Liscia P, Béracoché D. 2009. The hippocampus and prefrontal cortex are differentially involved in serial memory retrieval in non-stress and stress conditions. Neurobiol Learn Mem. 91:447–455.
   PubMed Web of Science ®Google Scholar
• Cole JC, Rodgers RJ. 1993. An ethological analysis of of the effects of chlordiazepoxide and bretazenil (Ro 16-6028) in the murine elevated plus-maze. Behav Pharmacol. 4:573–580.
   PubMed Web of Science ®Google Scholar
• Cullinan WE, Herman JP, Battaglia DF, Akil H, Watson SJ. 1995. Pattern and time course of immediate early gene expression in rat brain following acute stress. Neuroscience. 64:477–505.
   PubMed Web of Science ®Google Scholar
• Deakin JFW, Graeff FG. 1991. 5-HT and mechanisms of defense. J Psychopharmacol. 5:305–315.
   PubMedGoogle Scholar
• De Kloet ER, Joëls M, Holsboer F. 2005. Stress and the brain: From adaptation to disease. Nat Rev Neurosci. 6:463–475.
   PubMed Web of Science ®Google Scholar
• Diorio D, Viau V, Meaney MJ. 1993. The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypothalamic–pituitary–adrenal responses to stress. J Neurosci. 13:3839–3847.
   PubMed Web of Science ®Google Scholar
• Duvarci S, Paré D. 2007. Glucocorticoids enhance the excitability of principal basolateral amygdala neurons. J Neurosci. 27:4482–4491.
   PubMed Web of Science ®Google Scholar
• Etkin A, Egner T, Kalisch R. 2010. Emotional processing in anterior cingulate and medial prefrontal córtex. Trends Cogn Sci. 15:85–93.
   PubMed Web of Science ®Google Scholar
• Figueiredo HF, Bruestle A, Bodie B, Dolgas CM, Herman JP. 2003. The medial prefrontal cortex differentially regulates stress-induced c-fos expression in the forebrain depending on type of stressor. Eur J Neurosci. 18:2357–2364.
   PubMed Web of Science ®Google Scholar
• File SE, Zangrossi HJr, Sanders FL, Mabbutt PS. 1994. Raised corticosterone in the rat after exposure to the elevated plus-maze. Psychopharmacology (Berl). 113:543–546.
   PubMed Web of Science ®Google Scholar
• File SE, Gonzalez LE, Gallant R. 1998. Role of the basolateral nucleus of the amygdala in the formation of a phobia. Neuropsychopharmacology. 19:397–405.
   PubMed Web of Science ®Google Scholar
• Garcia A, Marti O, Valles A, Dal-Zotto S, Armario A. 2000. Recovery of the hypothalamic–pituitary–adrenal response to stress: Effect of stress intensity, stress duration and previous stress exposure. Neuroendocrinology. 72:114–125.
   PubMed Web of Science ®Google Scholar
• Genaro G, Schmidek WR, Franci CR. 2004. Social condition affects hormone secretion and exploratory behavior in rats. Braz J Med Biol Res. 37:833–840.
   PubMed Web of Science ®Google Scholar
• Graeff FG. 1981. Minor tranquilizers and brain defense systems. Braz J Med Biol Res. 14:239–265.
   PubMed Web of Science ®Google Scholar
• Graeff FG. 1994. Neuroanatomy and neurotransmitter regulation of defensive behaviors and related emotions in mammals. Braz J Med Biol Res. 27:811–829.
   PubMed Web of Science ®Google Scholar
• Gray JA, McNaughton N. 2000. The neuropsychology of anxiety: An enquiry into the functions of the septo-hippocampal system. Oxford: Oxford University Press.
   Google Scholar
• Hall FS, Wilkinson LS, Humby T, Inglis W, Kendall DA, Marsden CA, Robins TW. 1998. Isolation rearing in rats: Pre- and postsynaptic changes in striatal dopaminergic systems. Pharmacol Biochem Behav. 59:859–872.
   PubMed Web of Science ®Google Scholar
• Hatch AM, Wiberg GS, Zawidzka Z, Cann M, Airth JM, Grice HC. 1965. Isolation syndrome in the rat. Toxicol Appl Pharmacol. 7:737–745.
   PubMed Web of Science ®Google Scholar
• Hennessy JW, Levine S. 1979. Stress, arousal and the pituitary–adrenal system: A psychoendocrine hypothesis. In: Sprague JM, Epstein AN. editors. Progress in psychobiology and physiological psychology. New York: Academic Press133–178.
   Google Scholar
• Herman JP, Ostrander MM, Mueller NK, Figueiredo H. 2005. Limbic system mechanisms of stress regulation: Hypothalamo–pituitary–adrenocortical axis. Prog Neuropsychopharmacol Biol Psychiatry. 29:1201–1213.
   PubMed Web of Science ®Google Scholar
• Hlavacova N, Jezova D. 2008. Chronic treatment with the mineralocorticoid hormone aldosterone results in increased anxiety-like behavior. Horm Behav. 54:90–97.
   PubMed Web of Science ®Google Scholar
• Joëls M, Baram TZ. 2009. The neuro-symphony of stress. Nat Rev Neurosci. 10:459–466.
   PubMed Web of Science ®Google Scholar
• Joëls M, Karst H, De Rijk R, De Kloet ER. 2007. The coming out of the brain mineralocorticoid receptor. Trends Neurosci. 31:1–7.
   PubMed Web of Science ®Google Scholar
• Karst H, Nair S, Velzing E, Rumpff-van Essen L, Slagter E, Shinnick-Gallagher P, Joëls M. 2002. Glucocorticoids alter calcium conductances and calcium channel subunit expression in basolateral amygdala neurons. Eur J Neurosci. 16:1083–1089.
   PubMed Web of Science ®Google Scholar
• Karst H, Berger S, Turiault M, Tronche F, Schutz G, Joëls M. 2005. Mineralocorticoid receptors are indispensable for non-genomic modulation of hippocampal glutamate transmission by corticosterone. Proc Natl Acad Sci USA. 102:19204–19207.
   PubMed Web of Science ®Google Scholar
• Kim JW, Kirkpatrick B. 1996. Social isolation in animal models of relevance to neuropsychiatric disorders. Biol Psychiatry. 40:918–922.
   PubMed Web of Science ®Google Scholar
• Kim SS, Wang H, Li XY, Chen T, Mercaldo V, Descalzi G, Wu LJ, Zhuo M. 2011. Neurabin in the anterior cingulate cortex regulates anxiety-like behavior in adult mice. Mol Brain. 4:6.
   PubMed Web of Science ®Google Scholar
• Krugers HJ, Hoogenraad CC, Groc L. 2010. Stress hormones and AMPA receptor trafficking in synaptic plasticity and memory. Nat Rev Neurosci. 11:675–681.
   PubMed Web of Science ®Google Scholar
• Lightman SL, Conway-Campbell BL. 2010. The crucial role of pulsatile activity of the HPA axis for continuous dynamic equilibration. Nat Rev Neurosci. 11:710–718.
   PubMed Web of Science ®Google Scholar
• Likhtik E, Pelletier JG, Paz R, Paré D. 2005. Prefrontal control of the amygdala. J Neurosci. 25:7429–7437.
   PubMed Web of Science ®Google Scholar
• Maisonnette S, Morato S, Brandão ML. 1993. Role of resocialization and 5-HT1A receptor activation on the anxiogenic effects induced by isolation in the elevated plus-maze test. Physiol Behav. 54:753–758.
   PubMed Web of Science ®Google Scholar
• Martijena ID, Calvo N, Volosin M, Molina VA. 1997. Prior exposure to a brief restraint session facilitates the occurrence of fear in response to a conflict situation: Behavioral and neurochemical correlates. Brain Res. 752:136–142.
   PubMed Web of Science ®Google Scholar
• McDonald AJ. 1998. Cortical pathways to the mammalian amygdala. Prog Neurobiol. 55:257–332.
   PubMed Web of Science ®Google Scholar
• McDonald AJ, Mascagni F, Guo L. 1996. Projections of the medial and lateral prefrontal cortices to the amygdala: A Phaseolus vulgaris leucoagglutinin study in the rat. Neuroscience. 71:55–75.
   PubMed Web of Science ®Google Scholar
• Meaney MJ, Aitken DH, Bodnoff SR, Iny LJ, Tatarewicz JE, Sapolsky RM. 1985. Early postnatal handling alters glucocorticoid receptor concentrations in selected brain regions. Behav Neurosci. 99:765–770.
   PubMed Web of Science ®Google Scholar
• Mikics E, Barsy B, Barsvari B, Haller J. 2005. Behavioral specificity of non-genomic glucocorticoid effects in rats: Effects on risk assessment in the elevated plus-maze and the open-field. Horm Behav. 48:152–162.
   PubMed Web of Science ®Google Scholar
• Mitra R, Ferguson D, Sapolsky RM. 2009. Mineralocorticoid receptor overexpression in basolateral amygdala reduces corticosterone secretion and anxiety. Biol Psychiatry. 66:686–690.
   PubMed Web of Science ®Google Scholar
• Myers RD. 1966. Injection of solutions into cerebral tissue: Relation between volume and diffusion. Physiol Behav. 1:171–174.
   Web of Science ®Google Scholar
• Mobbs D, Petrovic P, Marchant JL, Hassabis D, Weiskopf N, Seymour B, Dolan RJ, Frith CD. 2007. When fear is near: Threat imminence elicits prefrontal-periaqueductal gray shifts in humans. Science. 317:1079–1083.
   PubMed Web of Science ®Google Scholar
• Moghaddam B. 1993. Stress preferentially increases extraneuronal levels of excitatory amino acids in the prefrontal cortex: Comparison to hippocampus and basal ganglia. J Neurochem. 60:1650–1657.
   PubMed Web of Science ®Google Scholar
• Motta V, Maisonette S, Morato S, Castrechini P, Brandão ML. 1992. Effects of blockade of 5-HT2 receptors and activation of 5-HT1A receptors on the exploratory activity of rats in the elevated plus-maze. Psychopharmacology (Berl). 107:135–139.
   PubMed Web of Science ®Google Scholar
• Musazzi L, Milanese M, Farisello P, Zappettini S, Tardito D, Barbiero VS, Bonifacino T, Mallei A, Baldelli P, Racagni G, Raiteri M, Benfenati F, Bonanno G, Popoli M. 2010. Acute stress increases depolarization-evoked glutamate release in the rat prefrontal/frontal cortex: The dampening action of antidepressants. PLoS One. 5:e8566.
   PubMed Web of Science ®Google Scholar
• Pacak K, Palkovitz M. 2001. Stressor specificity of central neuroendocrine responses: Implications for stress-related disorders. Endocr Rev. 22:502–548.
   PubMed Web of Science ®Google Scholar
• Patel PD, Lopez JF, Lyons DM, Burke S, Wallace M, Schatzberg AF. 2000. Glucocorticoid and mineralocorticoid receptor mRNA expression in squirrel monkey brain. J Psychiatr Res. 34:383–392.
   PubMed Web of Science ®Google Scholar
• Paxinos G, Watson C. 2007. The rat brain in stereotaxic coordinates. New York: Academic Press.
   Google Scholar
• Pellow S, Chopin P, File SE, Briley M. 1985. Validation of open:closed arm entries in the elevated plus-maze as a measure of anxiety in the rat. J Neurosci Methods. 14:149–167.
   PubMed Web of Science ®Google Scholar
• Pryce CR. 2008. Postnatal ontogeny of expression of the corticosteroid receptor genes in mammalian brains: Inter-species and intra-species differences. Brain Res Rev. 57:596–605.
   PubMed Web of Science ®Google Scholar
• Quirarte GL, de la Teja IS, Casillas M, Serafin N, Prado-Alcala RA, Roozendaal B. 2009. Corticosterone infused into the dorsal striatum selectively enhances memory consolidation of cued water-maze training. Learn Mem. 16:586–589.
   PubMed Web of Science ®Google Scholar
• Quirk GJ, Likhtik E, Pelletier JG, Paré D. 2003. Stimulation of medial prefrontal cortex decreases the responsiveness of central amygdala output neurons. J Neurosci. 23:8800–8807.
   PubMed Web of Science ®Google Scholar
• Radley JJ, Gosselink KL, Sawchenko PE. 2009. A discrete GABAergic relay mediates medial prefrontal cortical inhibition of the neuroendocrine stress response. J Neurosci. 29:7330–7340.
   PubMed Web of Science ®Google Scholar
• Rodgers RJ, Haller J, Holmes A, Halasz J, Walton TJ, Brain PF. 1999. Corticosterone response to the plus-maze: High correlation with risk assessment in rats and mice. Physiol Behav. 68:47–53.
   PubMed Web of Science ®Google Scholar
• Rodrigues SM, LeDoux JE, Sapolsky RM. 2009. The influence of stress hormones on fear circuitry. Annu Rev Neurosci. 32:289–313.
   PubMed Web of Science ®Google Scholar
• Roozendaal B, McReynolds JR, Van der Zee EA, Lee S, McGaugh JL, McIntyre CK. 2009. Glucocorticoid effects on memory consolidation depend on functional interactions between the medial prefrontal cortex and basolateral amygdala. J Neurosci. 29:14299–14308.
   PubMed Web of Science ®Google Scholar
• Shackman AJ, Salomons TV, Slagter HA, Fox AS, Winter JJ, Davidson RJ. 2011. The integration of negative affect, pain and cognitive control in the cingulated cortex. Nat Rev Neurosci. 12:154–167.
   PubMed Web of Science ®Google Scholar
• Singewald N. 2007. Altered brain activity processing in high-anxiety rodents revealed by challenge paradigms and functional mapping. Neurosci Biobehav Rev. 31:18–40.
   PubMed Web of Science ®Google Scholar
• Sotres-Bayon F, Quirk GJ. 2010. Prefrontal control of fear: More than just extinction. Curr Opin Neurobiol. 20:231–235.
   PubMed Web of Science ®Google Scholar
• Stam R. 2007. PTSD and stress sensitisation: A tale of brain and body: Part 2. Animal models. Neurosci Biobehav Rev. 31:558–584.
   PubMed Web of Science ®Google Scholar
• Sullivan RM, Gratton A. 2002. Prefrontal cortical regulation of hypothalamic–pituitary–adrenal function in the rat and implications for psychopathology: Side matters. Psychoneuroendocrinology. 27:99–114.
   PubMed Web of Science ®Google Scholar
• Tomazini FM, Reimer A, Albrechet-Souza L, Brandão ML. 2006. Opposite effects of short- and long-duration isolation on ultrasonic vocalization, startle and prepulse inhibition in rats. J Neurosci Methods. 153:114–120.
   PubMed Web of Science ®Google Scholar
• Wiedenmayer CP. 2004. Adaptations or pathologies? Long-term changes in brain and behavior after a single exposure to severe threat. Neurosci Biobehav Rev. 28:1–12.
   PubMed Web of Science ®Google Scholar
• Willner P, Mitchell PJ. 2002. The validity of animal models of predisposition to depression. Behav Pharmacol. 13:169–188.
   PubMed Web of Science ®Google Scholar
• Wright IK, Ismail H, Upton N, Marsden CA. 1991. Effect of isolation rearing on 5-HT agonist-induced responses in the rat. Psychopharmacology (Berl). 105:259–263.
   PubMed Web of Science ®Google Scholar