Hoda RANJBAR, Maryam RADAHMADI, Hojjatallah ALAEI, Parham REISI, Sara KARIMI

The effect of basolateral amygdala nucleus lesion on memory under acute, mid and chronic stress in male rats

Background/aim: The basolateral amygdala (BLA) modulates memory for emotional events and is involved in both stress and memory. This study investigated different durations of stress and the role of BLA on serum corticosterone level and spatial and cognitive memory. Materials and methods: Different durations of stress (acute, mid, and chronic stress), with and without BLA lesion were induced in rats by 6 h/day restraint stress for 1, 7, and 21 days. Memory functions were evaluated by novel object recognition (NOR) and object location test (OLT). Results: The OLT findings showed locomotor activity and spatial memory slightly decreased with different durations of stress. The NOR findings significantly showed locomotor activity impairment in different durations of stress. Cognitive memory deficit was observed in mid stress. The corticosterone level significantly increased in the mid and chronic stress groups. Moreover, the mid stress was the strongest stress condition. There is a possibility that different stress durations act by different mechanisms. The recognition of a novel location decreased in all lesion groups. It was more severe in the NOR. The BLA lesion significantly decreased corticosterone level in the mid and chronic stress groups compared to similar groups without lesion. Conclusion: The BLA lesion caused more damage to cognitive than spatial memory in stressed groups.

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1. Li S, Wang C, Wang W, Dong H, Hou P, Tang Y. Chronic mild stress impairs cognition in mice: from brain homeostasis to behavior. Life Sci 2008; 82: 934-942.
2. Maeng LY, Shors TJ. The stressed female brain: neuronal activity in the prelimbic but not infralimbic region of the medial prefrontal cortex suppresses learning after acute stress. Front Neural Circuits 2013; 7: 1-10.
3. Sandi C, Pinelo-Nava MT. Stress and memory: behavioral effects and neurobiological mechanisms. Neural Plast 2007; 2007: 1-20.
4. Radahmadi M, Alaei H, Sharifi MR, Hosseini N. The effect of synchronized forced running with chronic stress on short, mid and long- term memory in rats. Asian J Sports Med 2013; 4: 54-62.
5. Radahmadi M, Hosseini N, Nasimi A. Effect of chronic stress on short and long-term plasticity in dentate gyrus; study of recovery and adaptation. Neuroscience 2014; 280C: 121-129.
6. Aragon CM, Trudeau LE, Amit Z. Stress-ethanol interaction: involvement of endogenous opioid mechanisms. Neurosci Biobehav Rev 1990; 14: 535-541.
7. Roozendaal B, Barsegyan A, Lee S. Adrenal stress hormones, amygdala activation, and memory for emotionally arousing experiences. Prog Brain Res 2008; 167: 79-97.
8. Campeau S, Hayward MD, Hope BT, Rosen JB, Nestler EJ, Davis M. Induction of the c-fos proto-oncogene in rat amygdala during unconditioned and conditioned fear. Brain Res 1991; 565: 349-352.
9. Pelletier JG, Likhtik E, Filali M, Pare D. Lasting increases in basolateral amygdala activity after emotional arousal: implications for facilitated consolidation of emotional memories. Learn Mem 2005; 12: 96-102.
10. Ritov G, Ardi Z, Richter-Levin G. Differential activation of amygdala, dorsal and ventral hippocampus following an exposure to a reminder of underwater trauma. Front Behav Neurosci 2014; 8: 1-7.
11. Kogan I, Richter-Levin G. Activation pattern of the limbic system following spatial learning under stress. Eur J Neurosci 2008; 27: 715-722.
12. Sarabdjitsingh RA, Joels M. Rapid corticosteroid actions on synaptic plasticity in the mouse basolateral amygdala: relevance of recent stress history and beta-adrenergic signaling. Neurobiol Learn Mem 2014; 112: 168-175.
13. McGaugh JL, McIntyre CK, Power AE. Amygdala modulation of memory consolidation: interaction with other brain systems. Neurobiol Learn Mem 2002; 78: 539-552.
14. Pitkanen A, Pikkarainen M, Nurminen N, Ylinen A. Reciprocal connections between the amygdala and the hippocampal formation, perirhinal cortex, and postrhinal cortex in rat. A review. Ann N Y Acad Sci 2000; 911: 369-391.
15. Jarrard LE. On the role of the hippocampus in learning and memory in the rat. Behav Neural Biol 1993; 60: 9-26.
16. Zhang W, Rosenkranz JA. Repeated restraint stress increases basolateral amygdala neuronal activity in an age-dependent manner. Neuroscience 2012; 226: 459-474.
17. McGaugh JL. Memory consolidation and the amygdala: a systems perspective. Trends Neurosci 2002; 25: 456-461.
18. Werka T, Zielinski K. CS modality transfer of two-way avoidance in rats with central and basolateral amygdala lesions. Behav Brain Res 1998; 93: 11-24.
19. Li Z, Richter-Levin G. Stimulus intensity-dependent modulations of hippocampal long-term potentiation by basolateral amygdala priming. Front Cell Neurosci 2012; 6: 1-9.
20. Vouimba RM, Richter-Levin G. Different patterns of amygdala priming differentially affect dentate gyrus plasticity and corticosterone, but not CA1 plasticity. Front Neural Circuits 2013; 7: 1-10.
21. McGaugh JL. Memorya century of consolidation. Science 2000; 287: 248-251.
22. Bass DI, Partain KN, Manns JR. Event-specific enhancement of memory via brief electrical stimulation to the basolateral complex of the amygdala in rats. Behav Neurosci 2012; 126: 204-208.
23. Jobim PF, Pedroso TR, Werenicz A, Christoff RR, Maurmann N, Reolon GK, Schröder N, Roesler R. Impairment of object recognition memory by rapamycin inhibition of mTOR in the amygdala or hippocampus around the time of learning or reactivation. Behav Brain Res 2012; 228: 151-158.
24. Werenicz A, Christoff RR, Blank M, Jobim PF, Pedroso TR, Reolon GK, Schröder N, Roesler R. Administration of the phosphodiesterase type 4 inhibitor rolipram into the amygdala at a specific time interval after learning increases recognition memory persistence. Learn Mem 2012; 19: 495-498.
25. Boyle LM. A neuroplasticity hypothesis of chronic stress in the basolateral amygdala. Yale J Biol Med 2013; 86: 117-125.
26. Korz V, Frey JU. Bidirectional modulation of hippocampal long-term potentiation under stress and no-stress conditions in basolateral amygdala-lesioned and intact rats. J Neurosci 2005; 25: 7393-7400.
27. Radahmadi M, Alaei H, Sharifi MR, Hosseini N. The effect of synchronized running activity with chronic stress on passive avoidance learning and body weight in rats. Int J Prev Med 2013; 4: 430-437.
28. Avishai-Eliner S, Eghbal-Ahmadi M, Tabachnik E, Brunson KL, Baram TZ. Down-regulation of hypothalamic corticotropin-releasing hormone messenger ribonucleic acid (mRNA) precedes early-life experience-induced changes in hippocampal glucocorticoid receptor mRNA. Endocrinology 2001; 142: 89-97.
29. Li S, Fan YX, Wang W, Tang YY. Effects of acute restraint stress on different components of memory as assessed by objectrecognition and object-location tasks in mice. Behav Brain Res 2012; 227: 199-207.
30. Panahpour H, Dehghani GA. Attenuation of focal cerebral ischemic injury following post-ischemic inhibition of angiotensin converting enzyme (ACE) activity in normotensive rat. Iran Biomed J 2012; 16: 202-208.
31. Hosseini N, Nasehi M, Radahmadi M, Zarrindast MR. Effects of CA1 glutamatergic systems upon memory impairments in cholestatic rats. Behav Brain Res 2013; 256: 636-645.
32. Roozendaal B, Griffith QK, Buranday J, De Quervain DJ, McGaugh JL. The hippocampus mediates glucocorticoidinduced impairment of spatial memory retrieval: dependence on the basolateral amygdala. Proc Natl Acad Sci USA 2003; 100: 1328-1333.
33. Silvers JM, Harrod SB, Mactutus CF, Booze RM. Automation of the novel object recognition task for use in adolescent rats. J Neurosci Methods 2007; 166: 99-103.
34. Ennaceur A, Delacour J. A new one-trial test for neurobiological studies of memory in rats. 1: Behavioral data. Behav Brain Res 1988; 31: 47-59.
35. Ainge JA, Heron-Maxwell C, Theofilas P, Wright P, de Hoz L, Wood ER. The role of the hippocampus in object recognition in rats: examination of the influence of task parameters and lesion size. Behav Brain Res 2006; 167: 183-195.
36. Hughes RN. Neotic preferences in laboratory rodents: issues, assessment and substrates. Neurosci Biobehav Rev 2007; 31: 441-464.
37. Clark RE, Zola SM, Squire LR. Impaired recognition memory in rats after damage to the hippocampus. J Neurosci 2000; 20: 8853-8860.
38. Gaskin S, Tremblay A, Mumby DG. Retrograde and anterograde object recognition in rats with hippocampal lesions. Hippocampus 2003; 13: 962-969.
39. Sutcliffe JS, Marshall KM, Neill JC. Influence of gender on working and spatial memory in the novel object recognition task in the rat. Behav Brain Res 2007; 177: 117-125.
40. Segev A, Ramot A, Akirav I. Stress hormones receptors in the amygdala mediate the effects of stress on the consolidation, but not the retrieval, of a non aversive spatial task. PLoS One 2012; 7: 1-9.
41. Gaskin S, Tardif M, Cole E, Piterkin P, Kayello L, Mumby DG. Object familiarization and novel-object preference in rats. Behav Processes 2010; 83: 61-71.
42. De Rosa R, Garcia AA, Braschi C, Capsoni S, Maffei L, Berardi N, Cattaneo A. Intranasal administration of nerve growth factor (NGF) rescues recognition memory deficits in AD11 anti-NGF transgenic mice. Proc Natl Acad Sci USA 2005; 102: 3811-3816.
43. Gumuslu E, Mutlu O, Sunnetci D, Ulak G, Celikyurt IK, Cine N, Akar F, Savlı H, Erden F. The antidepressant agomelatine improves memory deterioration and upregulates CREB and BDNF gene expression levels in unpredictable chronic mild stress (UCMS)-exposed mice. Drug Target Insights 2014; 8: 11-21.
44. Antunes M, Biala G. The novel object recognition memory: neurobiology, test procedure, and its modifications. Cogn Process 2012; 13: 93-110.
45. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. 5th ed. Amsterdam, Netherlands: Elsevier Academic; 2005.
46. Simoens VL, Istok E, Hyttinen S, Hirvonen A, Naatanen R, Tervaniemi M. Psychosocial stress attenuates general sound processing and duration change detection. Psychophysiology 2007; 44: 30-38.
47. Oei NY, Everaerd WT, Elzinga BM, van Well S, Bermond B. Psychosocial stress impairs working memory at high loads: an association with cortisol levels and memory retrieval. Stress (Amsterdam, Netherlands) 2006; 9: 133-141.
48. Radahmadi M, Alaei H, Sharifi MR, Hosseini N. Effects of different timing of stress on corticosterone, BDNF and memory in male rats. Physiol Behav 2015; 139: 459-467.
49. Aziriova S, Repova Bednarova K, Krajcirovicova K, Hrenak J, Rajkovicova R, Arendasova K, Kamodyova N, Celec P, Zorad S, Adamcova M et al. Doxorubicin-induced behavioral disturbances in rats: protective effect of melatonin and captopril. Pharmacol Biochem Behav 2014; 124: 284-289.
50. Radahmadi M, Shadan F, Karimian SM, Sadr SS, Nasimi A. Effects of stress on exacerbation of diabetes mellitus, serum glucose and cortisol levels and body weight in rats. Pathophysiology 2006; 13: 51-55.
51. Li MH, Tang JP, Zhang P, Li X, Wang CY, Wei HJ, Yang XF, Zou W, Tang XQ. Disturbance of endogenous hydrogen sulfide generation and endoplasmic reticulum stress in hippocampus are involved in homocysteine-induced defect in learning and memory of rats. Behav Brain Res 2014; 262: 35-41.
52. Ferry B, Roozendaal B, McGaugh JL. Role of norepinephrine in mediating stress hormone regulation of long-term memory storage: a critical involvement of the amygdala. Biol Psychiatry 1999; 46: 1140-1152.
53. Zoladz PR, Park CR, Halonen JD, Salim S, Alzoubi KH, Srivareerat M, Fleshner M, Alkadhi KA, Diamond DM. Differential expression of molecular markers of synaptic plasticity in the hippocampus, prefrontal cortex, and amygdala in response to spatial learning, predator exposure, and stressinduced amnesia. Hippocampus 2012; 22: 577-589.
54. Lee MS, Kim YH, Lee BR, Kwon SH, Moon WJ, Hong KS, Song YS, Morita K, Hahm DH, Shim I et al. Novel antidepressant-like activity of caffeic acid phenethyl ester is mediated by enhanced glucocorticoid receptor function in the hippocampus. Evid Based Complement Alternat Med 2014; 2014: 1-10.
55. Li M, Fu Q, Li Y, Li S, Xue J, Ma S. Emodin opposes chronic unpredictable mild stress induced depressive-like behavior in mice by upregulating the levels of hippocampal glucocorticoid receptor and brain-derived neurotrophic factor. Fitoterapia 2014; 98C: 1-10.
56. Yoon SH, Kim BH, Ye SK, Kim MH. Chronic non-social stress affects depressive behaviors but not anxiety in mice. Korean J Physiol Pharmacol 2014; 18: 263-268.
57. Roozendaal B, Hahn EL, Nathan SV, de Quervain DJ, McGaugh JL. Glucocorticoid effects on memory retrieval require concurrent noradrenergic activity in the hippocampus and basolateral amygdala. J Neurosci 2004; 24: 8161-8169.
58. McIntyre CK, Power AE, Roozendaal B, McGaugh JL. Role of the basolateral amygdala in memory consolidation. Ann N Y Acad Sci 2003; 985: 273-293.
59. Roozendaal B. Stress and memory: opposing effects of glucocorticoids on memory consolidation and memory retrieval. Neurobiol Learn Mem 2002; 78: 578-595.
60. Hermans EJ, Battaglia FP, Atsak P, de Voogd LD, Fernandez G, Roozendaal B. How the amygdala affects emotional memory by altering brain network properties. Neurobiol Learn Mem 2014; 112: 2-16.
61. McGaugh JL, Roozendaal B. Role of adrenal stress hormones in forming lasting memories in the brain. Curr Opin Neurobiol 2002; 12: 205-210.
62. de Quervain DJ, Aerni A, Schelling G, Roozendaal B. Glucocorticoids and the regulation of memory in health and disease. Front Neuroendocrinol 2009; 30: 358-370.
63. Chegini HR, Nasehi M, Zarrindast MR. Differential role of the basolateral amygdala 5-HT3 and 5-HT4 serotonin receptors upon ACPA-induced anxiolytic-like behaviors and emotional memory deficit in mice. Behav Brain Res 2014; 261: 114-126.
64. Pardon MC, Gould GG, Garcia A, Phillips L, Cook MC, Miller SA, Mason PA, Morilak DA. Stress reactivity of the brain noradrenergic system in three rat strains differing in their neuroendocrine and behavioral responses to stress: implications for susceptibility to stress-related neuropsychiatric disorders. Neuroscience 2002; 115: 229-242.
65. Ennaceur A. One-trial object recognition in rats and mice: methodological and theoretical issues. Behav Brain Res 2010; 215: 244-254.
66. Shoji H, Mizoguchi K. Brain region-specific reduction in c-Fos expression associated with an anxiolytic effect of yokukansan in rats. J Ethnopharmacol 2013; 149: 93-102.
67. Gaszner B, Kormos V, Kozicz T, Hashimoto H, Reglodi D, Helyes Z. The behavioral phenotype of pituitary adenylatecyclase activating polypeptide-deficient mice in anxiety and depression tests is accompanied by blunted c-Fos expression in the bed nucleus of the stria terminalis, central projecting Edinger-Westphal nucleus, ventral lateral septum, and dorsal raphe nucleus. Neuroscience. 2012; 202: 283-299.
68. Marti O, Armario A. Anterior pituitary response to stress: time-related changes and adaptation. Int J Dev Neurosci 1998; 16: 241-260.
69. Schenberg LC. Towards a translational model of panic attack. Psychol Neurosci 2010; 3: 9-37.