Chronic stress alters inhibitory networks in the medial prefrontal cortex of adult mice

Brain Structure and Function

Volumn 218, Issue 6, 2013, Pages 1591-1605

  Gilabert Juan, Javier ^a,b,c   Castillo Gomez, Esther ^a   Guirado, Ramón ^a   Moltó, Maria Dolores ^a,b,c   Nacher, Juan ^a,b,c  

^a UNIVERSITY OF VALENCIA   (Spain)

^b HOSPITAL CLÍNICO UNIVERSITARIO   (Spain)

^c CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED DE SALUD MENTAL CIBERSAM   (Spain)

Author keywords

Calretinin; Dendritic spines; Glutamic acid decarboxylase; Interneuron; Somatostatin; Structural plasticity; Synaptophysin

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR ALPHA1; ENHANCED GREEN FLUORESCENT PROTEIN; GLUTAMATE DECARBOXYLASE 67; NERVE CELL ADHESION MOLECULE; SYNAPTOPHYSIN;

AMYGDALOID NUCLEUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ATROPHY; AVERSION; BEHAVIOR CHANGE; BRAIN CORTEX; BRAIN NERVE CELL; BRAIN REGION; CELL COUNT; CELL DENSITY; CELL STRUCTURE; CELL SUBPOPULATION; CELL TYPE; CELLULAR PARAMETERS; CHRONIC STRESS; CLINICAL FEATURE; CONTROLLED STUDY; DENDRITIC CELL; ENZYME SYNTHESIS; GABA A ALPHA1 GENE; GABAERGIC SYSTEM; GENE CONTROL; GENE EXPRESSION; GENETIC ANALYSIS; HYPERTROPHY; IMMOBILIZATION STRESS; INTERNEURON; MAJOR DEPRESSION; MALE; MARTINOTTI CELL; MEDIAL PREFRONTAL CORTEX; MENTAL DISEASE; MOUSE; NCAM GENE; NERVE CELL DEGENERATION; NERVE CELL INHIBITION; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NEUROPROTECTION; NEUROTRANSMISSION; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPINE; STRESS; STRUCTURE ANALYSIS;

ANIMALIA; MUS;

ANIMALS; DENDRITES; DNA PRIMERS; GENE EXPRESSION REGULATION; GLUTAMATE DECARBOXYLASE; IMMUNOHISTOCHEMISTRY; INTERNEURONS; MALE; MICE; MICROSCOPY, CONFOCAL; MODELS, NEUROLOGICAL; NEURAL CELL ADHESION MOLECULES; NEURONAL PLASTICITY; PREFRONTAL CORTEX; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STRESS, PHYSIOLOGICAL; SYNAPTIC TRANSMISSION; SYNAPTOPHYSIN;

EID: 84887215433     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-012-0479-1     Document Type: Article

References (61)

1. Bisaz R, Sandi C (2012) Vulnerability of conditional NCAM-deficient mice to develop stress-induced behavioral alterations. Stress 15:195-206
2. Bowers G, Cullinan WE, Herman JP (1998) Region-specific regulation of glutamic acid decarboxylase (GAD) mRNA expression in central stress circuits. J Neurosci 18:5938-5947
3. Brambilla P, Perez J, Barale F, Schettini G, Soares JC (2003) GABAergic dysfunction in mood disorders. Mol Psychiatry 8:721-737
4. Bremner JD (2005) Effects of traumatic stress on brain structure and function: relevance to early responses to trauma. J Trauma Dissociation 6:51-68
5. Brody A, Barsom MW, Bota RG, Saxena S (2001) Prefrontal-subcortical and limbic circuit mediation of major depressive disorder. Semin Clin Neuropsychiatry 6:102-112
6. Carvalho-Netto EF, Myers B, Jones K, Solomon MB, Herman JP (2011) Sex differences in synaptic plasticity in stress-responsive brain regions following chronic variable stress. Physiol Behav 104:242-247
7. Castillo-Gomez E, Varea E, Blasco-Ibanez JM, Crespo C, Nacher J (2011) Polysialic acid is required for dopamine d2 receptor-mediated plasticity involving inhibitory circuits of the rat medial prefrontal cortex. PLoS ONE 6:e29516
8. Chen JL, Flanders GH, Lee WC, Lin WC, Nedivi E (2011) Inhibitory dendrite dynamics as a general feature of the adult cortical microcircuit. J Neurosci 31:12437-12443
9. Cook SC, Wellman CL (2004) Chronic stress alters dendritic morphology in rat medial prefrontal cortex. J Neurobiol 60:236-248
10. Cordero MI, Rodriguez JJ, Davies HA, Peddie CJ, Sandi C, Stewart MG (2005) Chronic restraint stress down-regulates amygdaloid expression of polysialylated neural cell adhesion molecule. Neuroscience 133:903-910
11. Czeh B, Simon M, van der Hart MG, Schmelting B, Hesselink MB, Fuchs E (2005) Chronic stress decreases the number of parvalbumin-immunoreactive interneurons in the hippocampus: prevention by treatment with a substance P receptor (NK1) antagonist. Neuropsychopharmacology 30:67-79
12. Gilabert-Juan J, Castillo-Gomez E, Perez-Rando M, Molto MD, Nacher J (2011) Chronic stress induces changes in the structure of interneurons and in the expression of molecules related to neuronal structural plasticity and inhibitory neurotransmission in the amygdala of adult mice. Exp Neurol 232:33-40
13. Gomez-Climent MA, Guirado R, Castillo-Gomez E, Varea E, Gutierrez-Mecinas M, Gilabert-Juan J, Garcia-Mompo C, Vidueira S, Sanchez-Mataredona D, Hernandez S, Blasco-Ibanez JM, Crespo C, Rutishauser U, Schachner M, Nacher J (2011) The polysialylated form of the neural cell adhesion molecule (PSA-NCAM) is expressed in a subpopulation of mature cortical interneurons characterized by reduced structural features and connectivity. Cereb Cortex 21:1028-1041
14. Gould E, Woolley CS, McEwen BS (1991) Adrenal steroids regulate postnatal development of the rat dentate gyrus: I. Effects of glucocorticoids on cell death. J Comp Neurol 313:479-485
15. Greengard P, Valtorta F, Czernik AJ, Benfenati F (1993) Synaptic vesicle phosphoproteins and regulation of synaptic function. Science 259:780-785
16. Gruen RJ, Wenberg K, Elahi R, Friedhoff AJ (1995) Alterations in GABAA receptor binding in the prefrontal cortex following exposure to chronic stress. Brain Res 684:112-114
17. Gutierrez H, Davies AM (2007) A fast and accurate procedure for deriving the Sholl profile in quantitative studies of neuronal morphology. J Neurosci Methods 163:24-30
18. Hasler G, van der Veen JW, Tumonis T, Meyers N, Shen J, Drevets WC (2007) Reduced prefrontal glutamate/glutamine and gamma-aminobutyric acid levels in major depression determined using proton magnetic resonance spectroscopy. Arch Gen Psychiatry 64:193-200
19. Hu W, Zhang M, Czeh B, Flugge G, Zhang W (2010) Stress impairs GABAergic network function in the hippocampus by activating nongenomic glucocorticoid receptors and affecting the integrity of the parvalbumin-expressing neuronal network. Neuropsychopharmacology 35:1693-1707
20. Jurgenson M, Aonurm-Helm A, Zharkovsky A (2012) Partial reduction in neural cell adhesion molecule (NCAM) in heterozygous mice induces depression-related behaviour without cognitive impairment. Brain Res 1447:106-118
21. Karolewicz B, Maciag D, O'Dwyer G, Stockmeier CA, Feyissa AM, Rajkowska G (2010) Reduced level of glutamic acid decarboxylase-67 kDa in the prefrontal cortex in major depression. Int J Neuropsychopharmacol 13:411-420
22. Keck T, Scheuss V, Jacobsen RI, Wierenga CJ, Eysel UT, Bonhoeffer T, Hubener M (2011) Loss of sensory input causes rapid structural changes of inhibitory neurons in adult mouse visual cortex. Neuron 71:869-882
23. Krystal JH, Sanacora G, Blumberg H, Anand A, Charney DS, Marek G, Epperson CN, Goddard A, Mason GF (2002) Glutamate and GABA systems as targets for novel antidepressant and mood-stabilizing treatments. Mol Psychiatry 7(Suppl 1):S71-S80
24. Lee WC, Huang H, Feng G, Sanes JR, Brown EN, So PT, Nedivi E (2006) Dynamic remodeling of dendritic arbors in GABAergic interneurons of adult visual cortex. PLoS Biol 4:e29
25. Lee WC, Chen JL, Huang H, Leslie JH, Amitai Y, So PT, Nedivi E (2008) A dynamic zone defines interneuron remodeling in the adult neocortex. Proc Natl Acad Sci USA 105:19968-19973
26. Liston C, Miller MM, Goldwater DS, Radley JJ, Rocher AB, Hof PR, Morrison JH, McEwen BS (2006) Stress-induced alterations in prefrontal cortical dendritic morphology predict selective impairments in perceptual attentional set-shifting. J Neurosci 26:7870-7874
27. Lowy MT, Wittenberg L, Yamamoto BK (1995) Effect of acute stress on hippocampal glutamate levels and spectrin proteolysis in young and aged rats. J Neurochem 65:268-274
28. Lucassen PJ, Vollmann-Honsdorf GK, Gleisberg M, Czeh B, De Kloet ER, Fuchs E (2001) Chronic psychosocial stress differentially affects apoptosis in hippocampal subregions and cortex of the adult tree shrew. Eur J Neurosci 14:161-166
29. Ma Y, Hu H, Berrebi AS, Mathers PH, Agmon A (2006) Distinct subtypes of somatostatin-containing neocortical interneurons revealed in transgenic mice. J Neurosci 26:5069-5082
30. Magarinos AM, Deslandes A, McEwen BS (1999) Effects of antidepressants and benzodiazepine treatments on the dendritic structure of CA3 pyramidal neurons after chronic stress. Eur J Pharmacol 371:113-122
31. Maness PF, Schachner M (2007) Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration. Nat Neurosci 10:19-26
32. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C (2004) Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5:793-807
33. Masliah E, Terry RD, Alford M, DeTeresa R (1990) Quantitative immunohistochemistry of synaptophysin in human neocortex: an alternative method to estimate density of presynaptic terminals in paraffin sections. J Histochem Cytochem 38:837-844
34. McEwen BS (2000) The neurobiology of stress: from serendipity to clinical relevance. Brain Res 886:172-189
35. McEwen BS (2008) Central effects of stress hormones in health and disease: understanding the protective and damaging effects of stress and stress mediators. Eur J Pharmacol 583:174-185
36. Nacher J, Pham K, Gil-Fernandez V, McEwen BS (2004) Chronic restraint stress and chronic corticosterone treatment modulate differentially the expression of molecules related to structural plasticity in the adult rat piriform cortex. Neuroscience 126:503-509
37. Oh DH, Son H, Hwang S, Kim SH (2012) Neuropathological abnormalities of astrocytes, GABAergic neurons, and pyramidal neurons in the dorsolateral prefrontal cortices of patients with major depressive disorder. Eur Neuropsychopharmacol 22:330-338
38. Oliva AA Jr, Jiang M, Lam T, Smith KL, Swann JW (2000) Novel hippocampal interneuronal subtypes identified using transgenic mice that express green fluorescent protein in GABAergic interneurons. J Neurosci 20:3354-3368
39. Patel S, Roelke CT, Rademacher DJ, Cullinan WE, Hillard CJ (2004) Endocannabinoid signaling negatively modulates stress-induced activation of the hypothalamic-pituitary-adrenal axis. Endocrinology 145:5431-5438
40. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45
41. Pham K, Nacher J, Hof PR, McEwen BS (2003) Repeated restraint stress suppresses neurogenesis and induces biphasic PSA-NCAM expression in the adult rat dentate gyrus. Eur J Neurosci 17:879-886
42. Radley JJ, Morrison JH (2005) Repeated stress and structural plasticity in the brain. Ageing Res Rev 4:271-287
43. Radley JJ, Sisti HM, Hao J, Rocher AB, McCall T, Hof PR, McEwen BS, Morrison JH (2004) Chronic behavioral stress induces apical dendritic reorganization in pyramidal neurons of the medial prefrontal cortex. Neuroscience 125:1-6
44. Rajkowska G, O'Dwyer G, Teleki Z, Stockmeier CA, Miguel-Hidalgo JJ (2007) GABAergic neurons immunoreactive for calcium binding proteins are reduced in the prefrontal cortex in major depression. Neuropsychopharmacology 32:471-482
45. Roozendaal B, McEwen BS, Chattarji S (2009) Stress, memory and the amygdala. Nat Rev Neurosci 10:423-433
46. Sanacora G, Mason GF, Rothman DL, Behar KL, Hyder F, Petroff OA, Berman RM, Charney DS, Krystal JH (1999) Reduced cortical gamma-aminobutyric acid levels in depressed patients determined by proton magnetic resonance spectroscopy. Arch Gen Psychiatry 56:1043-1047
47. Sandi C (2004) Stress, cognitive impairment and cell adhesion molecules. Nat Rev Neurosci 5:917-930
48. Sandi C, Merino JJ, Cordero MI, Touyarot K, Venero C (2001) Effects of chronic stress on contextual fear conditioning and the hippocampal expression of the neural cell adhesion molecule, its polysialylation, and L1. Neuroscience 102:329-339
49. Seib LM, Wellman CL (2003) Daily injections alter spine density in rat medial prefrontal cortex. Neurosci Lett 337:29-32
50. Shalaby A, Kamal S (2009) Effect of Escitalopram on GABA level and anti-oxidant markers in prefrontal cortex and nucleus accumbens of chronic mild stress-exposed albino rats. Int J Physiol Pathophysiol Pharmacol 1:154-161
51. Shansky RM, Morrison JH (2009) Stress-induced dendritic remodeling in the medial prefrontal cortex: effects of circuit, hormones and rest. Brain Res 1293:108-113
52. Sholl DA (1953) Dendritic organization in the neurons of the visual and motor cortices of the cat. J Anat 87:387-406
53. Sousa N, Lukoyanov NV, Madeira MD, Almeida OF, Paula-Barbosa MM (2000) Reorganization of the morphology of hippocampal neurites and synapses after stress-induced damage correlates with behavioral improvement. Neuroscience 97:253-266
54. Varea E, Nacher J, Blasco-Ibanez JM, Gomez-Climent MA, Castillo-Gomez E, Crespo C, Martinez-Guijarro FJ (2005) PSA-NCAM expression in the rat medial prefrontal cortex. Neuroscience 136:435-443
55. Varea E, Blasco-Ibanez JM, Gomez-Climent MA, Castillo-Gomez E, Crespo C, Martinez-Guijarro FJ, Nacher J (2007a) Chronic fluoxetine treatment increases the expression of PSA-NCAM in the medial prefrontal cortex. Neuropsychopharmacology 32:803-812
56. Varea E, Castillo-Gomez E, Gomez-Climent MA, Blasco-Ibanez JM, Crespo C, Martinez-Guijarro FJ, Nacher J (2007b) PSA-NCAM expression in the human prefrontal cortex. J Chem Neuroanat 33:202-209
57. Venero C, Tilling T, Hermans-Borgmeyer I, Schmidt R, Schachner M, Sandi C (2002) Chronic stress induces opposite changes in the mRNA expression of the cell adhesion molecules NCAM and L1. Neuroscience 115:1211-1219
58. Vyas A, Mitra R, Shankaranarayana R, McEwen BS, Chattarji S (2002) Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. J Neurosci 22:6810-6818
59. Watanabe Y, Gould E, McEwen BS (1992) Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Res 588:341-345
60. West MJ, Slomianka L, Gundersen HJ (1991) Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482-497
61. Xu X, Roby KD, Callaway EM (2010) Immunochemical characterization of inhibitory mouse cortical neurons: three chemically distinct classes of inhibitory cells. J Comp Neurol 518:389-404