Skip to main content
SpringerLink
Log in

Inactivation of Basolateral Amygdala Prevents Stress-Induced Astroglial Loss in the Prefrontal Cortex

  • Published:
Molecular Neurobiology Aims and scope Submit manuscript

Abstract

Repeated stress causes cognitive decline and decreases the expression of glial fibrillary acidic protein (GFAP)+ astroglial cells in the prefrontal cortex (PFC). The stress-induced alterations in astroglial density and morphology might significantly contribute to cognitive impairments. Apart from PFC, a key region involved in modulation of repercussions of stress is basolateral amygdala (BLA), which undergoes hypertrophy following chronic immobilization stress (CIS) and has intense reciprocal connections to the PFC. Interestingly, inactivation of BLA precludes stress-induced learning deficits. However, the modulatory role of BLA on CIS-induced alterations in GFAP+ astroglial density and associated learning deficits are presently unknown. Accordingly, we present two sets of experiments evaluating the effects of BLA inactivation either permanently or temporarily on CIS-induced changes in learning and astroglial expression in the PFC. CIS causes impairment in novel object recognition memory and astroglial loss in the PFC. In experiment I, we permanently inactivated the BLA by ibotenate lesion prior to CIS and observed a significant improvement in learning. Surprisingly, BLA lesion also prevented the stress-induced astroglial loss in the PFC. Furthermore, in the experiment II, we analyzed whether the effects of permanent inactivation could be mirrored by the temporary blockage of BLA specifically during stress. Interestingly, temporary inactivation of BLA mimics the effects of lesion. There was a notable prevention of learning impairment and astroglial loss in the PFC following BLA inactivation during stress. The present study emphasizes that stress-induced astroglial loss might contribute to cognitive deficits and modulation of BLA activity might be a viable strategy for management of stress-related PFC dysfunctions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Abbreviations

BLA:

Basolateral amygdala

PFC:

Prefrontal cortex

PrL:

Prelimbic cortex

ACC:

Anterior cingulate cortex

GFAP:

Glial fibrillary acidic protein

CIS:

Chronic immobilization stress

NOR:

Novel object recognition

HPA axis:

Hypothalamic pituitary adrenal axis

NMDA:

N-methyl-d-aspartate

References

  1. Yuen EY, Wei J, Liu W, Zhong P, Li X, Yan Z (2012) Repeated stress causes cognitive impairment by suppressing glutamate receptor expression and function in prefrontal cortex. Neuron 73(5):962–977

    CAS  PubMed  PubMed Central  Google Scholar 

  2. Ramkumar K, Srikumar BN, Venkatasubramanian D, Siva R, Shankaranarayana Rao BS, Raju TR (2012) Reversal of stress-induced dendritic atrophy in the prefrontal cortex by intracranial self-stimulation. J Neural Transm (Vienna) 119(5):533–543

    CAS  Google Scholar 

  3. Pawlak R, Shankaranarayana Rao BS, Melchor JP, Chattarji S, McEwen B, Strickland S (2005) Tissue plasminogen activator and plasminogen mediate stress-induced decline of neuronal and cognitive functions in the mouse hippocampus. Proc Natl Acad Sci U S A 102(50):18201–18206

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Shilpa BM, Bhagya V, Harish G, Srinivas Bharath MM, Shankaranarayana Rao BS (2017) Environmental enrichment ameliorates chronic immobilisation stress-induced spatial learning deficits and restores the expression of BDNF, VEGF, GFAP and glucocorticoid receptors. Prog Neuro-Psychopharmacol Biol Psychiatry 76:88–100

    CAS  Google Scholar 

  5. Veena J, Srikumar BN, Raju TR, Shankaranarayana Rao BS (2009) Exposure to enriched environment restores the survival and differentiation of new born cells in the hippocampus and ameliorates depressive symptoms in chronically stressed rats. Neurosci Lett 455(3):178–182

    CAS  PubMed  Google Scholar 

  6. Willner P, Towell A, Sampson D, Sophokleous S, Muscat R (1987) Reduction of sucrose preference by chronic unpredictable mild stress, and its restoration by a tricyclic antidepressant. Psychopharmacology 93(3):358–364

    CAS  PubMed  Google Scholar 

  7. Pawlak R, Magarinos AM, Melchor J, McEwen B, Strickland S (2003) Tissue plasminogen activator in the amygdala is critical for stress-induced anxiety-like behavior. Nat Neurosci 6(2):168–174

    CAS  PubMed  Google Scholar 

  8. Wei J, Zhong P, Qin L, Tan T, Yan Z (2017) Chemicogenetic restoration of the prefrontal cortex to amygdala pathway ameliorates stress-induced deficits. Cereb Cortex. https://doi.org/10.1093/cercor/bhx104

  9. Czeh B, Simon M, Schmelting B, Hiemke C, Fuchs E (2006) Astroglial plasticity in the hippocampus is affected by chronic psychosocial stress and concomitant fluoxetine treatment. Neuropsychopharmacology 31(8):1616–1626

    CAS  PubMed  Google Scholar 

  10. Banasr M, Duman RS (2008) Glial loss in the prefrontal cortex is sufficient to induce depressive-like behaviors. Biol Psychiatry 64(10):863–870

    PubMed  PubMed Central  Google Scholar 

  11. Tynan RJ, Beynon SB, Hinwood M, Johnson SJ, Nilsson M, Woods JJ, Walker FR (2013) Chronic stress-induced disruption of the astrocyte network is driven by structural atrophy and not loss of astrocytes. Acta Neuropathol 126(1):75–91

    CAS  PubMed  Google Scholar 

  12. Newman EA (2003) New roles for astrocytes: Regulation of synaptic transmission. Trends Neurosci 26(10):536–542

    CAS  PubMed  Google Scholar 

  13. Perea G, Navarrete M, Araque A (2009) Tripartite synapses: astrocytes process and control synaptic information. Trends Neurosci 32(8):421–431

    CAS  PubMed  Google Scholar 

  14. Kant D, Tripathi SS, Qureshi MF, Tripathi S 2nd, Pandey S, Singh G, Kumar T, Mir FA et al (2014) The effect of glial glutamine synthetase inhibition on recognition and temporal memories in the rat. Neurosci Lett 560:98–102

    CAS  PubMed  Google Scholar 

  15. Suzuki A, Stern SA, Bozdagi O, Huntley GW, Walker RH, Magistretti PJ, Alberini CM (2011) Astrocyte-neuron lactate transport is required for long-term memory formation. Cell 144(5):810–823

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Gibbs ME, Hertz L, Ng KT (2004) Inhibition of short-term memory formation in the chick by blockade of extracellular glutamate uptake. Neurobiol Learn Mem 81(2):115–119

    CAS  PubMed  Google Scholar 

  17. Lee HS, Ghetti A, Pinto-Duarte A, Wang X, Dziewczapolski G, Galimi F, Huitron-Resendiz S, Pina-Crespo JC et al (2014) Astrocytes contribute to gamma oscillations and recognition memory. Proc Natl Acad Sci U S A 111(32):E3343–E3352

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Orr AG, Hsiao EC, Wang MM, Ho K, Kim DH, Wang X, Guo W, Kang J et al (2015) Astrocytic adenosine receptor A2A and Gs-coupled signaling regulate memory. Nat Neurosci 18(3):423–434

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Roozendaal B, Portillo-Marquez G, McGaugh JL (1996) Basolateral amygdala lesions block glucocorticoid-induced modulation of memory for spatial learning. Behav Neurosci 110(5):1074–1083

    CAS  PubMed  Google Scholar 

  20. Roozendaal B, McReynolds JR, McGaugh JL (2004) The basolateral amygdala interacts with the medial prefrontal cortex in regulating glucocorticoid effects on working memory impairment. J Neurosci 24(6):1385–1392

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Vyas A, Mitra R, Shankaranarayana Rao BS, Chattarji S (2002) Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. J Neurosci 22(15):6810–6818

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Radley JJ, Rocher AB, Rodriguez A, Ehlenberger DB, Dammann M, McEwen BS, Morrison JH, Wearne SL et al (2008) Repeated stress alters dendritic spine morphology in the rat medial prefrontal cortex. J Comp Neurol 507(1):1141–1150

    PubMed  PubMed Central  Google Scholar 

  23. Wellman CL (2001) Dendritic reorganization in pyramidal neurons in medial prefrontal cortex after chronic corticosterone administration. J Neurobiol 49(3):245–253

    CAS  PubMed  Google Scholar 

  24. Amaral DG, Price JL (1984) Amygdalo-cortical projections in the monkey (Macaca fascicularis). J Comp Neurol 230(4):465–496

    CAS  PubMed  Google Scholar 

  25. Hoover WB, Vertes RP (2007) Anatomical analysis of afferent projections to the medial prefrontal cortex in the rat. Brain Struct Funct 212(2):149–179

    PubMed  Google Scholar 

  26. Krettek JE, Price JL (1977) The cortical projections of the mediodorsal nucleus and adjacent thalamic nuclei in the rat. J Comp Neurol 171(2):157–191

    CAS  PubMed  Google Scholar 

  27. Little JP, Carter AG (2013) Synaptic mechanisms underlying strong reciprocal connectivity between the medial prefrontal cortex and basolateral amygdala. J Neurosci 33(39):15333–15342

    CAS  PubMed  PubMed Central  Google Scholar 

  28. 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(45):14299–14308

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Maroun M (2006) Stress reverses plasticity in the pathway projecting from the ventromedial prefrontal cortex to the basolateral amygdala. Eur J Neurosci 24(10):2917–2922

    PubMed  Google Scholar 

  30. Maroun M, Richter-Levin G (2003) Exposure to acute stress blocks the induction of long-term potentiation of the amygdala-prefrontal cortex pathway in vivo. J Neurosci 23(11):4406–4409

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Roozendaal B, Sapolsky RM, McGaugh JL (1998) Basolateral amygdala lesions block the disruptive effects of long-term adrenalectomy on spatial memory. Neuroscience 84(2):453–465

    CAS  PubMed  Google Scholar 

  32. Roozendaal B, Nguyen BT, Power AE, McGaugh JL (1999) Basolateral amygdala noradrenergic influence enables enhancement of memory consolidation induced by hippocampal glucocorticoid receptor activation. Proc Natl Acad Sci U S A 96(20):11642–11647

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Rei D, Mason X, Seo J, Graff J, Rudenko A, Wang J, Rueda R, Siegert S et al (2015) Basolateral amygdala bidirectionally modulates stress-induced hippocampal learning and memory deficits through a p25/Cdk5-dependent pathway. Proc Natl Acad Sci U S A 112(23):7291–7296

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Jeon B, Hwang YK, Lee SY, Kim D, Chung C, Han JS (2012) The role of basolateral amygdala in the regulation of stress-induced phosphorylated extracellular signal-regulated kinase expression in the hippocampus. Neuroscience 224:191–201

    CAS  PubMed  Google Scholar 

  35. Kim JJ, Lee HJ, Han JS, Packard MG (2001) Amygdala is critical for stress-induced modulation of hippocampal long-term potentiation and learning. J Neurosci 21(14):5222–5228

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Kim JJ, Koo JW, Lee HJ, Han JS (2005) Amygdalar inactivation blocks stress-induced impairments in hippocampal long-term potentiation and spatial memory. J Neurosci 25(6):1532–1539

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Tripathi SJ, Chakraborty S, Srikumar BN, Raju TR, Shankaranarayana Rao BS (2017) Inactivation of basolateral amygdala prevents chronic immobilization stress-induced memory impairment and associated changes in corticosterone levels. Neurobiol Learn Mem 142(Pt B):218–229

    CAS  PubMed  Google Scholar 

  38. Paxinos G, Watson C (2006) The rat brain in stereotaxic coordinates. Academic Press, Amsterdam

    Google Scholar 

  39. Tripathi SJ, Chakraborty S, Srikumar BN, Raju TR, Shankaranarayana Rao BS (2017) Prevention of chronic immobilization stress-induced enhanced expression of glucocorticoid receptors in the prefrontal cortex by inactivation of basolateral amygdala. J Chem Neuroanat. https://doi.org/10.1016/j.jchemneu.2017.12.006

  40. Nibuya M, Takahashi M, Russell DS, Duman RS (1999) Repeated stress increases catalytic TrkB mRNA in rat hippocampus. Neurosci Lett 267(2):81–84

    CAS  PubMed  Google Scholar 

  41. Roozendaal B, Okuda S, Van der Zee EA, McGaugh JL (2006) Glucocorticoid enhancement of memory requires arousal-induced noradrenergic activation in the basolateral amygdala. Proc Natl Acad Sci U S A 103(17):6741–6746

    CAS  PubMed  PubMed Central  Google Scholar 

  42. de Lima MN, Laranja DC, Bromberg E, Roesler R, Schroder N (2005) Pre- or post-training administration of the NMDA receptor blocker MK-801 impairs object recognition memory in rats. Behav Brain Res 156(1):139–143

    PubMed  Google Scholar 

  43. Karasawa J, Hashimoto K, Chaki S (2008) D-serine and a glycine transporter inhibitor improve MK-801-induced cognitive deficits in a novel object recognition test in rats. Behav Brain Res 186(1):78–83

    CAS  PubMed  Google Scholar 

  44. Veena J, Srikumar BN, Mahati K, Bhagya V, Raju TR, Shankaranarayana Rao BS (2009) Enriched environment restores hippocampal cell proliferation and ameliorates cognitive deficits in chronically stressed rats. J Neurosci Res 87(4):831–843

    CAS  PubMed  Google Scholar 

  45. Veena J, Srikumar BN, Mahati K, Raju TR, Shankaranarayana Rao BS (2011) Oxotremorine treatment restores hippocampal neurogenesis and ameliorates depression-like behaviour in chronically stressed rats. Psychopharmacology 217(2):239–253

    CAS  PubMed  Google Scholar 

  46. Abhijit S, Tripathi SJ, Bhagya V, Shankaranarayana Rao BS, Subramanyam MV, Asha Devi S (2018) Antioxidant action of grape seed polyphenols and aerobic exercise in improving neuronal number in the hippocampus is associated with decrease in lipid peroxidation and hydrogen peroxide in adult and middle-aged rats. Exp Gerontol 101:101–112

    CAS  PubMed  Google Scholar 

  47. Vrinda M, Sasidharan A, Aparna S, Srikumar BN, Kutty BM, Shankaranarayana Rao BS (2017) Enriched environment attenuates behavioral seizures and depression in chronic temporal lobe epilepsy. Epilepsia 58(7):1148–1158

    CAS  PubMed  Google Scholar 

  48. Shankaranarayana Rao BS, Govindaiah, Laxmi TR, Meti BL, Raju TR (2001) Subicular lesions cause dendritic atrophy in CA1 and CA3 pyramidal neurons of the rat hippocampus. Neuroscience 102(2):319–327

    CAS  PubMed  Google Scholar 

  49. Shankaranarayana Rao BS, Desiraju T, Raju TR (1993) Neuronal plasticity induced by self-stimulation rewarding experience in rats—a study on alteration in dendritic branching in pyramidal neurons of hippocampus and motor cortex. Brain Res 627(2):216–224

    Google Scholar 

  50. West MJ (1999) Stereological methods for estimating the total number of neurons and synapses: issues of precision and bias. Trends Neurosci 22(2):51–61

    CAS  PubMed  Google Scholar 

  51. Ennaceur A, Neave N, Aggleton JP (1997) Spontaneous object recognition and object location memory in rats: the effects of lesions in the cingulate cortices, the medial prefrontal cortex, the cingulum bundle and the fornix. Exp Brain Res 113(3):509–519

    CAS  PubMed  Google Scholar 

  52. Gaskin S, Tardif M, Cole E, Piterkin P, Kayello L, Mumby DG (2010) Object familiarization and novel-object preference in rats. Behav Process 83(1):61–71

    Google Scholar 

  53. Baxter MG (2010) "I've seen it all before": explaining age-related impairments in object recognition. Theoretical comment on Burke et al. (2010). Behav Neurosci 124(5):706–709

    PubMed  Google Scholar 

  54. Nishimura KJ, Ortiz JB, Conrad CD (2017) Antagonizing the GABAA receptor during behavioral training improves spatial memory at different doses in control and chronically stressed rats. Neurobiol Learn Mem 145:114–118

    CAS  PubMed  Google Scholar 

  55. Cerqueira JJ, Mailliet F, Almeida OF, Jay TM, Sousa N (2007) The prefrontal cortex as a key target of the maladaptive response to stress. J Neurosci 27(11):2781–2787

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Srikumar BN, Raju TR, Shankaranarayana Rao BS (2006) The involvement of cholinergic and noradrenergic systems in behavioral recovery following oxotremorine treatment to chronically stressed rats. Neuroscience 143(3):679–688

    CAS  PubMed  Google Scholar 

  57. McLaughlin KJ, Gomez JL, Baran SE, Conrad CD (2007) The effects of chronic stress on hippocampal morphology and function: an evaluation of chronic restraint paradigms. Brain Res 1161:56–64

    CAS  PubMed  PubMed Central  Google Scholar 

  58. Bodnoff SR, Humphreys AG, Lehman JC, Diamond DM, Rose GM, Meaney MJ (1995) Enduring effects of chronic corticosterone treatment on spatial learning, synaptic plasticity, and hippocampal neuropathology in young and mid-aged rats. J Neurosci 15(1 Pt 1):61–69

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Rahman MM, Callaghan CK, Kerskens CM, Chattarji S, O'Mara SM (2016) Early hippocampal volume loss as a marker of eventual memory deficits caused by repeated stress. Sci Rep 6:29127

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Sunanda, Shankaranarayana Rao BS, Raju TR (2000) Chronic restraint stress impairs acquisition and retention of spatial memory task in rats. Curr Sci 79(11):1581

    Google Scholar 

  61. Shankaranarayana Rao BS, Madhavi R, Sunanda RTR (2001) Complete reversal of dendritic atrophy in CA3 neurons of the hippocampus by rehabilitation in restraint stressed rats. Curr Sci 80:653–659

    Google Scholar 

  62. Hinwood M, Tynan RJ, Charnley JL, Beynon SB, Day TA, Walker FR (2013) Chronic stress induced remodeling of the prefrontal cortex: structural re-organization of microglia and the inhibitory effect of minocycline. Cereb Cortex 23(8):1784–1797

    PubMed  Google Scholar 

  63. Cerqueira JJ, Pego JM, Taipa R, Bessa JM, Almeida OF, Sousa N (2005) Morphological correlates of corticosteroid-induced changes in prefrontal cortex-dependent behaviors. J Neurosci 25(34):7792–7800

    CAS  PubMed  PubMed Central  Google Scholar 

  64. Mitra R, Jadhav S, McEwen BS, Vyas A, Chattarji S (2005) Stress duration modulates the spatiotemporal patterns of spine formation in the basolateral amygdala. Proc Natl Acad Sci U S A 102(26):9371–9376

    CAS  PubMed  PubMed Central  Google Scholar 

  65. Govindarajan A, Shankaranarayana Rao BS, Nair D, Trinh M, Mawjee N, Tonegawa S, Chattarji S (2006) Transgenic brain-derived neurotrophic factor expression causes both anxiogenic and antidepressant effects. Proc Natl Acad Sci U S A 103(35):13208–13213

    CAS  PubMed  PubMed Central  Google Scholar 

  66. Felix-Ortiz AC, Beyeler A, Seo C, Leppla CA, Wildes CP, Tye KM (2013) BLA to vHPC inputs modulate anxiety-related behaviors. Neuron 79(4):658–664

    CAS  PubMed  PubMed Central  Google Scholar 

  67. Felix-Ortiz AC, Burgos-Robles A, Bhagat ND, Leppla CA, Tye KM (2016) Bidirectional modulation of anxiety-related and social behaviors by amygdala projections to the medial prefrontal cortex. Neuroscience 321:197–209

    CAS  PubMed  Google Scholar 

  68. Parent MB, Avila E, McGaugh JL (1995) Footshock facilitates the expression of aversively motivated memory in rats given post-training amygdala basolateral complex lesions. Brain Res 676(2):235–244

    CAS  PubMed  Google Scholar 

  69. Maren S, Aharonov G, Fanselow MS (1996) Retrograde abolition of conditional fear after excitotoxic lesions in the basolateral amygdala of rats: absence of a temporal gradient. Behav Neurosci 110(4):718–726

    CAS  PubMed  Google Scholar 

  70. Steiner J, Bernstein HG, Bielau H, Berndt A, Brisch R, Mawrin C, Keilhoff G, Bogerts B (2007) Evidence for a wide extra-astrocytic distribution of S100B in human brain. BMC Neurosci 8:2

    PubMed  PubMed Central  Google Scholar 

  71. Steiner J, Bernstein HG, Bogerts B, Gos T, Richter-Landsberg C, Wunderlich MT, Keilhoff G (2008) S100B is expressed in, and released from, OLN-93 oligodendrocytes: influence of serum and glucose deprivation. Neuroscience 154(2):496–503

    CAS  PubMed  Google Scholar 

  72. Si X, Miguel-Hidalgo JJ, O'Dwyer G, Stockmeier CA, Rajkowska G (2004) Age-dependent reductions in the level of glial fibrillary acidic protein in the prefrontal cortex in major depression. Neuropsychopharmacology 29(11):2088–2096

    CAS  PubMed  Google Scholar 

  73. Miguel-Hidalgo JJ, Baucom C, Dilley G, Overholser JC, Meltzer HY, Stockmeier CA, Rajkowska G (2000) Glial fibrillary acidic protein immunoreactivity in the prefrontal cortex distinguishes younger from older adults in major depressive disorder. Biol Psychiatry 48(8):861–873

    CAS  PubMed  Google Scholar 

  74. Rajkowska G, Miguel-Hidalgo JJ (2007) Gliogenesis and glial pathology in depression. CNS Neurol Disord Drug Targets 6(3):219–233

    CAS  PubMed  PubMed Central  Google Scholar 

  75. Bremner JD, Vythilingam M, Vermetten E, Vaccarino V, Charney DS (2004) Deficits in hippocampal and anterior cingulate functioning during verbal declarative memory encoding in midlife major depression. Am J Psychiatry 161(4):637–645

    PubMed  Google Scholar 

  76. Castaneda AE, Tuulio-Henriksson A, Marttunen M, Suvisaari J, Lonnqvist J (2008) A review on cognitive impairments in depressive and anxiety disorders with a focus on young adults. J Affect Disord 106(1–2):1–27

    PubMed  Google Scholar 

  77. Lima A, Sardinha VM, Oliveira AF, Reis M, Mota C, Silva MA, Marques F, Cerqueira JJ et al (2014) Astrocyte pathology in the prefrontal cortex impairs the cognitive function of rats. Mol Psychiatry 19(7):834–841

    CAS  PubMed  Google Scholar 

  78. Banasr M, Chowdhury GM, Terwilliger R, Newton SS, Duman RS, Behar KL, Sanacora G (2010) Glial pathology in an animal model of depression: reversal of stress-induced cellular, metabolic and behavioral deficits by the glutamate-modulating drug riluzole. Mol Psychiatry 15(5):501–511

    CAS  PubMed  Google Scholar 

  79. Chowdhury GM, Zhang J, Thomas M, Banasr M, Ma X, Pittman B, Bristow L, Schaeffer E et al (2017) Transiently increased glutamate cycling in rat PFC is associated with rapid onset of antidepressant-like effects. Mol Psychiatry 22(1):120–126

    CAS  PubMed  Google Scholar 

  80. Rothstein JD, Dykes-Hoberg M, Pardo CA, Bristol LA, Jin L, Kuncl RW, Kanai Y, Hediger MA et al (1996) Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 16(3):675–686

    CAS  PubMed  Google Scholar 

  81. Rappeneau V, Blaker A, Petro JR, Yamamoto BK, Shimamoto A (2016) Disruption of the glutamate-glutamine cycle involving astrocytes in an animal model of depression for males and females. Front Behav Neurosci 10:231

    PubMed  PubMed Central  Google Scholar 

  82. Mookherjee P, Green PS, Watson GS, Marques MA, Tanaka K, Meeker KD, Meabon JS, Li N et al (2011) GLT-1 loss accelerates cognitive deficit onset in an Alzheimer's disease animal model. J Alzheimers Dis 26(3):447–455

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Li SX, Han Y, Xu LZ, Yuan K, Zhang RX, Sun CY, Xu DF, Yuan M et al (2018) Uncoupling DAPK1 from NMDA receptor GluN2B subunit exerts rapid antidepressant-like effects. Mol Psychiatry 23(3):597–608

    PubMed  Google Scholar 

  84. Wang J, Tu J, Cao B, Mu L, Yang X, Cong M, Ramkrishnan AS, Chan RHM et al (2017) Astrocytic l-lactate signaling facilitates amygdala-anterior cingulate cortex synchrony and decision making in rats. Cell Rep 21(9):2407–2418

    CAS  PubMed  Google Scholar 

  85. Popoli M, Yan Z, McEwen BS, Sanacora G (2011) The stressed synapse: the impact of stress and glucocorticoids on glutamate transmission. Nat Rev Neurosci 13(1):22–37

    PubMed  PubMed Central  Google Scholar 

  86. Sheline YI (2000) 3D MRI studies of neuroanatomic changes in unipolar major depression: the role of stress and medical comorbidity. Biol Psychiatry 48(8):791–800

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Sunil Jamuna Tripathi was supported by a Senior Research Fellowship (File No. 09/490(0095)/2014-EMR-I) from the Council of Scientific and Industrial Research (CSIR), New Delhi, India. Suwarna Chakraborty was supported by a research fellowship (NIMH: A&E/C:PhD(NP):2013-14: SC) from the National Institute of Mental Health and Neuro Sciences (NIMHANS), Bengaluru, India. We acknowledge financial support from the Department of Biotechnology (DBT), Science and Engineering Research Board, Department of Science & Technology, Government of India (SERB-DST), New Delhi and National Institute of Mental Health and Neuro Sciences (NIMHANS), Bengaluru, India.

Contributions

S.J.T., T.R.R., and B.S.S.R. conceptualized and designed the experiments; S.J.T. and S.C. performed the experiments and analyzed the data; B.N.S, T.R.R., and B.S.S.R. contributed to reagents/materials/analysis tools; and S.J.T., S.C., B.N.S, T.R.R., and B.S.S.R. wrote the manuscript.

Author information

Authors and Affiliations

  1. Department of Neurophysiology, National Institute of Mental Health and Neuro Sciences (NIMHANS), Hosur Road, Bengaluru, 560 029, India

    Sunil Jamuna Tripathi, Suwarna Chakraborty, B. N. Srikumar, T. R. Raju & B. S. Shankaranarayana Rao

Authors
  1. Sunil Jamuna Tripathi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Suwarna Chakraborty
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. B. N. Srikumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. T. R. Raju
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. B. S. Shankaranarayana Rao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to B. S. Shankaranarayana Rao.

Ethics declarations

Conflict of Interest

The authors declare no conflict of interest.

Electronic Supplementary Material

ESM 1

(PDF 499 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tripathi, S.J., Chakraborty, S., Srikumar, B.N. et al. Inactivation of Basolateral Amygdala Prevents Stress-Induced Astroglial Loss in the Prefrontal Cortex. Mol Neurobiol 56, 350–366 (2019). https://doi.org/10.1007/s12035-018-1057-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12035-018-1057-1

Keywords

Search

Navigation