Lack of feedback inhibition on rat basolateral amygdala following stress or withdrawal from sedative-hypnotic drugs

European Journal of Neuroscience

Volumn 26, Issue 4, 2007, Pages 1036-1044

  Isoardi, Nora A ^a,b   Bertotto, Maria E ^a   Martijena, Irene D ^a   Molina, Victor A ^a   Carrer, Hugo F ^b  

^a UNIVERSIDAD NACIONAL DE CÓRDOBA   (Argentina)

^b INSTITUTO DE INVESTIGACIÓN MÉDICA MERCEDES Y MARTÍN FERREYRA   (Argentina)

Author keywords

Disinhibition; Negative emotional state; Patch clamp; Recurrent inhibition

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; ALCOHOL; DIAZEPAM; HYPNOTIC SEDATIVE AGENT; PICROTOXIN;

ACTION POTENTIAL; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; DRUG WITHDRAWAL; INHIBITORY POSTSYNAPTIC POTENTIAL; MALE; NEGATIVE FEEDBACK; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; RECEPTOR BLOCKING; STRESS;

AMYGDALA; ANIMALS; CENTRAL NERVOUS SYSTEM DEPRESSANTS; DIAZEPAM; ELECTRIC STIMULATION; ELECTROPHYSIOLOGY; ETHANOL; EXCITATORY POSTSYNAPTIC POTENTIALS; FEEDBACK; GAMMA-AMINOBUTYRIC ACID; HYPNOTICS AND SEDATIVES; MALE; PATCH-CLAMP TECHNIQUES; RATS; RATS, WISTAR; RESTRAINT, PHYSICAL; STRESS, PSYCHOLOGICAL; SUBSTANCE WITHDRAWAL SYNDROME;

EID: 34547995159     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2007.05714.x     Document Type: Article

References (56)

1. Aggleton, J.P. (2000) The Amygdala: A Functional Analysis. Wiley-Liss, New York.
2. Baldwin, H.A., Rassnick, S., Rivier, J., Koob, G.F. Britton, K.T. (1991) CRF antagonist reverses the 'anxiogenic' response to ethanol withdrawal in the rat. Psychopharmacology (Berl.), 103, 227 232.
3. Benes, F.M. Berretta, S. (2001) GABAergic interneurons: implications for understanding schizophrenia and bipolar disorder. Neuropsychopharmacology, 25, 1 27.
4. Bertotto, M.E., Bustos, S.G., Molina, V.A. Martijena, I.D. (2006) Influence of ethanol withdrawal on fear memory: Effect of d-cycloserine. Neuroscience, 142, 979 990.
5. Bissiere, S., Humeau, Y. Luthi, A. (2003) Dopamine gates LTP induction in lateral amygdala by suppressing feedforward inhibition. Nat. Neurosci., 6, 587 592.
6. Blair, H.T., Schafe, G.E., Bauer, E.P., Rodrigues, S.M. LeDoux, J.E. (2001) Synaptic plasticity in the lateral amygdala: a cellular hypothesis of fear conditioning. Learn. Mem., 8, 229 242.
7. Bonson, K.R., Grant, S.J., Contoreggi, C.S., Links, J.M., Metcalfe, J., Weyl, H.L., Kurian, V., Ernst, M. London, E.D. (2002) Neural systems and cue-induced cocaine craving. Neuropsychopharmacology, 26, 376 386.
8. Braga, M.F.M., Aroniadou-Anderjaska, V., Xie, J.W. Li, H. (2003) Bidirectional modulation of GABA release by presynaptic glutamate receptor 5 kainate receptors in the basolateral amygdala. J. Neurosci., 23, 442 452.
9. Braga, M.F., Aroniadou-Anderjaska, V., Manion, S.T., Hough, C.J. Li, H. (2004) Stress impairs alpha(1A) adrenoceptor-mediated noradrenergic facilitation of GABAergic transmission in the basolateral amygdala. Neuropsychopharmacology, 29, 45 58.
10. Childress, A.R., Mozley, P.D., McElgin, W., Fitzgerald, J., Reivich, M. O'Brien, C.P. (1999) Limbic activation during cue-induced cocaine craving. Am. J. Psychiat., 156, 11 18.
11. Davis, M. (1992) The role of amygdala in fear-potentiated startle: implications for animal models of anxiety. Trends Pharmacol. Sci., 13, 35 41.
12. Davis, M. (1997) Neurobiology of fear responses: the role of the amygdala. J. Neuropsychiat. Clin. Neurosci., 9, 382 402.
13. Davis, M. Whalen, P.J. (2001) The amygdala: vigilance and emotion. Mol. Psychiat., 6, 13 34.
14. Debarbieux, F., Brunton, J. Charpak, S. (1998) Effect of bicuculline on thalamic activity: a direct blockade of IAHP in reticularis neurons. J. Neurophysiol., 79, 2911 2918.
15. Delaney, A.J. Sah, P. (1999) GABA receptors inhibited by benzodiazepines mediate fast inhibitory transmission in the central amygdala. J. Neurosci., 19, 9698 9704.
16. Dityatev, A.E. Bolshakov, V.Y. (2005) Amygdala, long-term potentiation, and fear conditioning. Neuroscientist, 11, 75 88.
17. Farrant, M. Nusser, Z. (2005) Variations on an inhibitory theme: phasic and tonic activation of GABA(A) receptors. Nat. Rev. Neurosci., 6, 215 229.
18. Fendt, M. Fanselow, M.S. (1999) The neuroanatomical and neurochemical basis of conditioned fear. Neurosci. Biobehav. Rev., 23, 743 760.
19. File, S.E. (1990) The history of benzodiazepine dependence: a review of animal studies. Neurosci. Biobehav. Rev., 14, 135 146.
20. File, S.E. Andrews, N. (1991) Low but not high doses of buspirone reduce the anxiogenic effects of diazepam withdrawal. Psychopharmacology, 105, 578 582.
21. Hamill, O.P., Marty, A., Neher, E., Sakmann, B. Sigworth, F.J. (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell free membrane patches. Pflugers Arch., 391, 85 100.
22. Isoardi, N.A., Martijena, I.D., Carrer, H.F. Molina, V.A. (2004) Increased fear learning coincides with neuronal dysinhibition and facilitated LTP in the basolateral amygdala following benzodiazepine withdrawal in rats. Neuropsychopharmacology, 29, 1852 1864.
23. Koob, G.F. (2004) A role for GABA mechanisms in the motivational effects of alcohol. Biochem. Pharmacol., 68, 1515 1525.
24. Koob, G.F. LeMoal, M. (2001) Drug addiction, dysregulation of reward, and allostasis. Neuropsychopharmacology, 24, 97 129.
25. Kreek, M.J. Koob, G.F. (1998) Drug dependence: stress and dysregulation of brain reward pathways. Drug Alcohol Depend., 51, 23 47.
26. Kroner, S., Rosenkranz, J.A., Grace, A.A. Barrionuevo, G. (2005) Dopamine modulates excitability of basolateral amygdala neurons in vitro. J. Neurophysiol., 93, 1598 1610.
27. LeDoux, J.E. (2000) Emotion circuits in the brain. Annu. Rev. Neurosci., 23, 155 184.
28. Liu, M. Glowa, J.R. (2000) Regulation of benzodiazepine receptor binding and GABA(A) subunit mRNA expression by punishment and acute alprazolam administration. Brain Res., 887, 23 33.
29. Markou, A., Kosten, T.R. Koob, G.F. (1998) Neurobiological similarities in depression and drug dependence: a self-medication hypothesis. Neuropsychopharmacology, 18, 135 174.
30. Martijena, I.D., Tapia, M. Molina, V.A. (1996) Altered behavioral and neurochemical response to stress in benzodiazepine-withdrawn rats. Brain Res., 712, 239 244.
31. Martijena, I.D., Calvo, N., Volosin, M. Molina, V.A. (1997a) 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.
32. Martijena, I.D., Lacerra, C. Molina, V.A. (1997b) Carbamazepine normalizes the altered behavioral and neurochemical response to stress in benzodiazepine-withdrawn rats. Eur. J. Pharmacol., 330, 101 108.
33. Martijena, I.D., Lacerra, C., Bustos, S.G. Molina, V.A. (2001) Chronic benzodiazepine administration facilitates the subsequent development of ethanol dependence. Brain Res., 891, 227 335.
34. Martijena, I.D., Rodriguez Manzanares, P.A., Lacerra, C. Molina, V.A. (2002) Gabaergic modulation of the stress response in frontal cortex and amygdala. Synapse, 45, 86 94.
35. Mcdonald, A.J. Betette, R.L. (2001) Parvalbumin-containing neurons in the rat basolateral amygdala: morphology and co-localization of Calbindin-D (28k). Neuroscience, 102, 413 425.
36. Mcdonald, A.J. Mascagni, F. (2002) Immunohistochemical characterization of somatostatin containing interneurons in the rat basolateral amygdala. Brain Res., 943, 237 244.
37. Mcdonald, A.J., Mascagni, F., Mania, I. Rainnie, D.G. (2005) Evidence for a perisomatic innervation of parvalbumin-containing interneurons by individual pyramidal cells in the basolateral amygdala. Brain Res., 1035, 32 40.
38. Moyer, J.R. Brown, T.H. (1998) Methods for whole-cell recording from visually preselected neurons of perirhinal cortex in brain slices from young and aging rats. J. Neurosci. Meth., 86, 35 54.
39. Pflieger, J.F., Clarac, F. Vinay, L. (2002) Picrotoxin and bicuculline have different effects on lumbar spinal networks and motoneurons in the neonatal rat. Brain Res., 935, 81 86.
40. Pitkanen, A., Savander, V. LeDoux, J.E. (1998) Organization of intra-amygdaloid circuitries in the rat: an emerging framework for understanding functions of the amygdala (Vol. 20, pg. 517, 1997). Trends Neurosci., 21, 52.
41. Rainnie, D.G. (1999) Serotonergic modulation of neurotransmission in the rat basolateral amygdala. J. Neurophysiol., 82, 69 85.
42. Rainnie, D.G., Asprodini, E.K. Shinnick-Gallagher, P. (1991a) Excitatory transmission in the basolateral amygdala. J. Neurophysiol., 66, 986 998.
43. Rainnie, D.G., Asprodini, E.K. Shinnick-Gallagher, P. (1991b) Inhibitory transmission in the basolateral amygdala. J. Neurophysiol., 66, 999 1009.
44. Rainnie, D.G., Asprodini, E.K. Shinnick-Gallagher, P. (1992) Kindling-induced long-lasting changes in synaptic transmission in the basolateral amygdala. J. Neurophysiol., 67, 443 454.
45. Rainnie, D.G., Bergeron, R., Sajdyk, T.J., Patil, M., Gehlert, D.R. Shekhar, A. (2004) Corticotrophin releasing factor-induced synaptic plasticity in the amygdala translates stress into emotional disorders. J. Neurosci., 24, 3471 3479.
46. Rodriguez Manzanares, P.A., Isoardi, N.A., Carrer, H.F. Molina, V.A. (2005) Previous stress facilitates fear memory, attenuates GABAergic inhibition, and increases synaptic plasticity in the rat basolateral amygdala. J. Neurosci., 25, 8725 8734.
47. Rosenkranz, J.A. Grace, A.A. (2002) Cellular mechanisms of infralimbic and prelimbic prefrontal cortical inhibition and dopaminergic modulation of basolateral amygdala neurons in vivo. J. Neurosci., 22, 324 337.
48. Sah, P., Faber, E.S., Lopez, D.A. Power, J. (2003) The amygdaloid complex: anatomy and physiology. Physiol. Rev., 83, 803 834.
49. Sanders, S.K. Shekhar, A. (1991) Blockade of GABAA receptors in the region of the anterior basolateral amygdala of rats elicits increases in heart rate and blood pressure. Brain Res., 567, 101 110.
50. Sanders, S.K., Morzorati, S.L. Shekhar, A. (1995) Priming of experimental anxiety by repeated subthreshold GABA blockade in the rat amygdala. Brain Res., 699, 250 259.
51. Shekhar, A., Truitt, W., Rainnie, D. Sajdyk, T. (2005) Role of stress, corticotrophin releasing factor (CRF) and amygdala plasticity in chronic anxiety. Stress, 8, 209 219.
52. Shors, T.J., Weiss, C. Thompson, R.F. (1992) Stress-induced facilitation of classical conditioning. Science, 257, 537 539.
53. Smith, Y., Pare, J.F. Pare, D. (2000) Differential innervation of parvalbumin-immunoreactive interneurons of the basolateral amygdaloid complex by cortical and intrinsic inputs. J. Comp. Neurol., 416, 496 508.
54. Washburn, M.S. Moises, H.C. (1992) Inhibitory responses of rat basolateral amygdaloid neurons recorded in vitro. Neuroscience, 50, 811 830.
55. Woodruff, A.R., Monyer, H. Sah, P. (2006) GABAergic excitation in the basolateral amygdala. J. Neurosci., 26, 11 881 11 887.
56. Zurita, A., Murua, S. Molina, V. (1996) An endogenous opiate mechanism seems to be involved in stress-induced anhedonia. Eur. J. Pharmacol., 299, 1 7.