Chronic Restraint Stress Did Not Alter Active Avoidance Coping or Neuronal Activation Levels of the Medial Prefrontal Cortex or the Nucleus Accumbens in Male Rats.
Journal
Journal of physiological investigation
ISSN: 2950-6344
Titre abrégé: J Physiol Investig
Pays: India
ID NLM: 9918803386606676
Informations de publication
Date de publication:
01 Sep 2024
01 Sep 2024
Historique:
received:
24
06
2024
accepted:
05
09
2024
medline:
28
10
2024
pubmed:
28
10
2024
entrez:
28
10
2024
Statut:
ppublish
Résumé
Stress is an adaptive response crucial for survival. However, chronic stress can lead to maladaptive behaviors and health issues. Prolonged stress reduces the flexibility of defensive coping behaviors. Previous studies have shown that the medial prefrontal cortex (mPFC) and the nucleus accumbens (NAc) play critical roles in maintaining active avoidance instead of freezing behaviors in face of threats. This study aimed to investigate whether chronic stress altered the prelimbic cortex, infralimbic cortex, NAc core and the NAc shell neuronal activation levels and the defensive coping in male rats in face of danger, and we hypothesized that the activation levels of these two brain regions would decrease and the animals would spend more time in freezing. The animals underwent a chronic restraint stress procedure (2 h/day) for consecutive 14 days. Using a cued lever-pressing shock avoidance task, we assessed the avoidance coping and the neuronal activities in the mPFC and the NAc. Our results showed that compared to nonstressed controls, animals that underwent chronic restraint stress were slower in gaining body weight and developed despair-like behaviors in the forced swim test. However, contrary to our hypothesis, chronic restraint stress did not alter active avoidance coping or neuronal activation levels of the mPFC and the NAc.
Identifiants
pubmed: 39465568
doi: 10.4103/ejpi.EJPI-D-24-00066
pii: 02275668-202467050-00005
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
270-280Informations de copyright
Copyright © 2024 Copyright: © 2024 Journal of Physiological Investigation.
Références
Lazarus RS, Folkman S Stress, Appraisal, and Coping New York: Springer Publishing Company; 1984.
Pacák K, Palkovits M Stressor specificity of central neuroendocrine responses: Implications for stress-related disorders. Endocr Rev 2001; 22: 502–48.
Salleh MR Life event, stress and illness. Malays J Med Sci 2008; 15: 9–18.
Patriquin MA, Mathew SJ The neurobiological mechanisms of generalized anxiety disorder and chronic stress. Chronic Stress (Thousand Oaks) 2017; 1: 2470547017703993 [doi: 10.1177/247 0547017703993].
doi: 10.1177/247
Culpepper L Generalized anxiety disorder and medical illness. J Clin Psychiatry 2009; 70 Suppl 2 20–4.
Maeng LY, Milad MR Post-traumatic stress disorder: The relationship between the fear response and chronic stress. Chronic Stress (Thousand Oaks) 2017; 1: 2470547017713297.
Sherin JE, Nemeroff CB Post-traumatic stress disorder: The neurobiological impact of psychological trauma. Dialogues Clin Neurosci 2011; 13: 263–78.
de Kloet ER, Joëls M, Holsboer F Stress and the brain: From adaptation to disease. Nat Rev Neurosci 2005; 6: 463–75.
Schneiderman N, Ironson G, Siegel SD Stress and health: Psychological, behavioral, and biological determinants. Annu Rev Clin Psychol 2005; 1: 607–28.
Roelofs K Freeze for action: Neurobiological mechanisms in animal and human freezing. Philos Trans R Soc Lond B Biol Sci 2017; 372: 20160206.
LeDoux JE, Gorman JM A call to action: Overcoming anxiety through active coping. Am J Psychiatry 2001; 158: 1953–5.
Sandi C, Merino JJ, Cordero MI, Touyarot K, Venero C Effects of chronic stress on contextual fear conditioning and the hippocampal expression of the neural cell adhesion molecule, its polysialylation, and L1. Neuroscience 2001; 102: 329–39.
Hatherall L, Sánchez C, Morilak DA Chronic vortioxetine treatment reduces exaggerated expression of conditioned fear memory and restores active coping behavior in chronically stressed rats. Int J Neuropsychopharmacol 2017; 20: 316–23.
Roth MK, Bingham B, Shah A, Joshi A, Frazer A, Strong R, et al. Effects of chronic plus acute prolonged stress on measures of coping style, anxiety, and evoked HPA-axis reactivity. Neuropharmacology 2012; 63: 1118–26.
Hoffman AN, Lorson NG, Sanabria F, Foster Olive M, Conrad CD Chronic stress disrupts fear extinction and enhances amygdala and hippocampal fos expression in an animal model of post-traumatic stress disorder. Neurobiol Learn Mem 2014; 112: 139–47.
Miracle AD, Brace MF, Huyck KD, Singler SA, Wellman CL Chronic stress impairs recall of extinction of conditioned fear. Neurobiol Learn Mem 2006; 85: 213–8.
Conrad CD, LeDoux JE, Magariños AM, McEwen BS Repeated restraint stress facilitates fear conditioning independently of causing hippocampal CA3 dendritic atrophy. Behav Neurosci 1999; 113: 902–13.
Baran SE, Armstrong CE, Niren DC, Hanna JJ, Conrad CD Chronic stress and sex differences on the recall of fear conditioning and extinction. Neurobiol Learn Mem 2009; 91: 323–32.
Garcia R, Spennato G, Nilsson-Todd L, Moreau JL, Deschaux O Hippocampal low-frequency stimulation and chronic mild stress similarly disrupt fear extinction memory in rats. Neurobiol Learn Mem 2008; 89: 560–6.
Gamaro GD, Michalowski MB, Catelli DH, Xavier MH, Dalmaz C Effect of repeated restraint stress on memory in different tasks. Braz J Med Biol Res 1999; 32: 341–7.
Lopes FL, Azevedo TM, Imbiriba LA, Freire RC, Valença AM, Caldirola D, et al. Freezing reaction in panic disorder patients associated with anticipatory anxiety. Depress Anxiety 2009; 26: 917–21.
Gillan CM, Morein-Zamir S, Urcelay GP, Sule A, Voon V, Apergis-Schoute AM, et al. Enhanced avoidance habits in obsessive-compulsive disorder. Biol Psychiatry 2014; 75: 631–8.
Ressler KJ Amygdala activity, fear, and anxiety: Modulation by stress. Biol Psychiatry 2010; 67: 1117–9.
LeDoux J The emotional brain, fear, and the amygdala. Cell Mol Neurobiol 2003; 23: 727–38.
LeDoux JE, Moscarello J, Sears R, Campese V The birth, death and resurrection of avoidance: A reconceptualization of a troubled paradigm. Mol Psychiatry 2017; 22: 24–36.
Amorapanth P, LeDoux JE, Nader K Different lateral amygdala outputs mediate reactions and actions elicited by a fear-arousing stimulus. Nat Neurosci 2000; 3: 74–9.
Choi JS, Cain CK, LeDoux JE The role of amygdala nuclei in the expression of auditory signaled two-way active avoidance in rats. Learn Mem 2010; 17: 139–47.
Herry C, Johansen JP Encoding of fear learning and memory in distributed neuronal circuits. Nat Neurosci 2014; 17: 1644–54.
Hoover WB, Vertes RP Anatomical analysis of afferent projections to the medial prefrontal cortex in the rat. Brain Struct Funct 2007; 212: 149–79.
McDonald AJ Organization of amygdaloid projections to the prefrontal cortex and associated striatum in the rat. Neuroscience 1991; 44: 1–14.
Mcdonald AJ, Mascagni F, Guo L Projections of the medial and lateral prefrontal cortices to the amygdala: A Phaseolus vulgaris leucoagglutinin study in the rat. Neuroscience 1996; 71: 55–75.
Radley JJ, Rocher AB, Rodriguez A, Ehlenberger DB, Dammann M, McEwen BS, et al. Repeated stress alters dendritic spine morphology in the rat medial prefrontal cortex. J Comp Neurol 2008; 507: 1141–50.
Radley JJ, Sisti HM, Hao J, Rocher AB, McCall T, Hof PR, et al. Chronic behavioral stress induces apical dendritic reorganization in pyramidal neurons of the medial prefrontal cortex. Neuroscience 2004; 125: 1–6.
Liston C, Miller MM, Goldwater DS, Radley JJ, Rocher AB, Hof PR, et al. Stress-induced alterations in prefrontal cortical dendritic morphology predict selective impairments in perceptual attentional set-shifting. J Neurosci 2006; 26: 7870–4.
Bravo-Rivera C, Roman-Ortiz C, Brignoni-Perez E, Sotres-Bayon F, Quirk GJ Neural structures mediating expression and extinction of platform-mediated avoidance. J Neurosci 2014; 34: 9736–42.
Capuzzo G, Floresco SB Prelimbic and infralimbic prefrontal regulation of active and inhibitory avoidance and reward-seeking. J Neurosci 2020; 40: 4773–87.
Moscarello JM, LeDoux JE Active avoidance learning requires prefrontal suppression of amygdala-mediated defensive reactions. J Neurosci 2013; 33: 3815–23.
Dadkhah M, Rashidy-Pour A, Vafaei AA Temporary inactivation of the infralimbic cortex impairs while the blockade of its DA D2 receptors enhances auditory fear extinction in rats. Pharmacol Biochem Behav 2021; 203: 173131.
Bloodgood DW, Sugam JA, Holmes A, Kash TL Fear extinction requires infralimbic cortex projections to the basolateral amygdala. Transl Psychiatry 2018; 8: 60.
Do-Monte FH, Manzano-Nieves G, Quiñones-Laracuente K, Ramos-Medina L, Quirk GJ Revisiting the role of infralimbic cortex in fear extinction with optogenetics. J Neurosci 2015; 35: 3607–15.
Oleson EB, Gentry RN, Chioma VC, Cheer JF Subsecond dopamine release in the nucleus accumbens predicts conditioned punishment and its successful avoidance. J Neurosci 2012; 32: 14804–8.
Piantadosi PT, Yeates DC, Floresco SB Cooperative and dissociable involvement of the nucleus accumbens core and shell in the promotion and inhibition of actions during active and inhibitory avoidance. Neuropharmacology 2018; 138: 57–71.
Ramirez F, Moscarello JM, LeDoux JE, Sears RM Active avoidance requires a serial basal amygdala to nucleus accumbens shell circuit. J Neurosci 2015; 35: 3470–7.
Wenzel JM, Oleson EB, Gove WN, Cole AB, Gyawali U, Dantrassy HM, et al. Phasic dopamine signals in the nucleus accumbens that cause active avoidance require endocannabinoid mobilization in the Midbrain. Curr Biol 2018; 28: 1392–404.e5.
Levita L, Hoskin R, Champi S Avoidance of harm and anxiety: A role for the nucleus accumbens. Neuroimage 2012; 62: 189–98.
Belujon P, Grace AA Restoring mood balance in depression: Ketamine reverses deficit in dopamine-dependent synaptic plasticity. Biol Psychiatry 2014; 76: 927–36.
Ampuero E, Luarte A, Santibañez M, Varas-Godoy M, Toledo J, Diaz-Veliz G, et al. Two chronic stress models based on movement restriction in rats respond selectively to antidepressant drugs: Aldolase C as a potential biomarker. Int J Neuropsychopharmacol 2015; 18: pyv038.
Markov DD Sucrose preference test as a measure of anhedonic behavior in a chronic unpredictable mild stress model of depression: Outstanding issues. Brain Sci 2022; 12: 1287.
Richardson JT Eta squared and partial eta squared as measures of effect size in educational research. Educ Res Rev 2011; 6: 135–47.
Chiba S, Numakawa T, Ninomiya M, Richards MC, Wakabayashi C, Kunugi H Chronic restraint stress causes anxiety- and depression-like behaviors, downregulates glucocorticoid receptor expression, and attenuates glutamate release induced by brain-derived neurotrophic factor in the prefrontal cortex. Prog Neuropsychopharmacol Biol Psychiatry 2012; 39: 112–9.
Beck KD, Luine VN Sex differences in behavioral and neurochemical profiles after chronic stress: Role of housing conditions. Physiol Behav 2002; 75: 661–73.
Adachi N, Sakhri FZ, Ikemoto H, Ohashi Y, Kato M, Inoue T, et al. Kamikihito rescued depressive-like behaviors and hippocampus neurogenesis in chronic restraint stress rats. J Tradit Complement Med 2022; 12: 172–9.
Liang S, Wang T, Hu X, Luo J, Li W, Wu X, et al. Administration of Lactobacillus helveticus NS8 improves behavioral, cognitive, and biochemical aberrations caused by chronic restraint stress. Neuroscience 2015; 310: 561–77.
Moreno C, Hermosilla T, Hardy P, Aballai V, Rojas P, Varela D Ca (v) 1.2 activity and downstream signaling pathways in the hippocampus of an animal model of depression. Cells 2020; 9: 2609.
Shilpa BM, Bhagya V, Harish G, Srinivas Bharath MM, Shankaranarayana Rao BS Environmental enrichment ameliorates chronic immobilisation stress-induced spatial learning deficits and restores the expression of BDNF, VEGF, GFAP and glucocorticoid receptors. Prog Neuropsychopharmacol Biol Psychiatry 2017; 76: 88–100.
Pan Q, Wu J, Liu Y, Li X, Chen J Involvement of hepatic SHIP2 and PI3K/Akt signalling in the regulation of plasma insulin by Xiaoyaosan in chronic immobilization-stressed rats. Molecules 2019; 24: 480.
Liu L, Zhou X, Zhang Y, Liu Y, Yang L, Pu J, et al. The identification of metabolic disturbances in the prefrontal cortex of the chronic restraint stress rat model of depression. Behav Brain Res 2016; 305: 148–56.
Bąk J, Bobula B, Hess G Restraint stress and repeated corticosterone administration differentially affect neuronal excitability, synaptic transmission and 5-HT (7) receptor reactivity in the dorsal raphe nucleus of young adult male rats. Int J Mol Sci 2022; 23: 14303.
Gregus A, Wintink AJ, Davis AC, Kalynchuk LE Effect of repeated corticosterone injections and restraint stress on anxiety and depression-like behavior in male rats. Behav Brain Res 2005; 156: 105–14.
Platt JE, Stone EA Chronic restraint stress elicits a positive antidepressant response on the forced swim test. Eur J Pharmacol 1982; 82: 179–81.
Rosenkranz JA, Venheim ER, Padival M Chronic stress causes amygdala hyperexcitability in rodents. Biol Psychiatry 2010; 67: 1128–36.
Olave FA, Aguayo FI, Román-Albasini L, Corrales WA, Silva JP, González PI, et al. Chronic restraint stress produces sex-specific behavioral and molecular outcomes in the dorsal and ventral rat hippocampus. Neurobiol Stress 2022; 17: 100440.
Mao Y, Xu Y, Yuan X Validity of chronic restraint stress for modeling anhedonic-like behavior in rodents: A systematic review and meta-analysis. J Int Med Res 2022; 50: 3000605221075816.
Bielajew C, Konkle AT, Merali Z The effects of chronic mild stress on male Sprague-Dawley and long Evans rats: I. Biochemical and physiological analyses. Behav Brain Res 2002; 136: 583–92.
Turner KM, Burne TH Comprehensive behavioural analysis of long Evans and Sprague-Dawley rats reveals differential effects of housing conditions on tests relevant to neuropsychiatric disorders. PLoS One 2014; 9: e93411.
Vanderschuren LJ, Achterberg EJ, Trezza V The neurobiology of social play and its rewarding value in rats. Neurosci Biobehav Rev 2016; 70: 86–105.
Buynitsky T, Mostofsky DI Restraint stress in biobehavioral research: Recent developments. Neurosci Biobehav Rev 2009; 33: 1089–98.
McLaughlin KJ, Gomez JL, Baran SE, Conrad CD The effects of chronic stress on hippocampal morphology and function: An evaluation of chronic restraint paradigms. Brain Res 2007; 1161: 56–64.
Bowman RE, Beck KD, Luine VN Chronic stress effects on memory: Sex differences in performance and monoaminergic activity. Horm Behav 2003; 43: 48–59.
Perez-Rando M, Carceller H, Castillo-Gomez E, Bueno-Fernandez C, García-Mompó C, Gilabert-Juan J, et al. Impact of stress on inhibitory neuronal circuits, our tribute to Bruce McEwen. Neurobiol Stress 2022; 19: 100460.
Tang J, Yang C, Shi M, Chen W Activation of dopamine D (2) receptors in the shell of nucleus accumbens triggers conditioned avoidance responses in rats. Behav Brain Res 2022; 422: 113759.
Dong X, Li S, Kirouac GJ A projection from the paraventricular nucleus of the thalamus to the shell of the nucleus accumbens contributes to footshock stress-induced social avoidance. Neurobiol Stress 2020; 13: 100266.