Amygdalar GABAergic-rich neural grafts attenuate anxiety-like behavior in rats

Behavioural Brain Research

Volumn 205, Issue 1, 2009, Pages 146-153

  Cunningham, Miles Gregory ^a   Connor, Caroline Martine ^a   Carlezon Jr , William A ^a   Meloni, Edward ^a  

^a MCLEAN HOSPITAL   (United States)

Author keywords

Basolateral amygdaloid nucleus; Elevated plus maze; Fear potentiated startle; GABAergic; Lateral amygdaloid nucleus; Lateral ganglionic eminance; Unconditioned light response

Indexed keywords

AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; BRAIN FUNCTION; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENGRAFTMENT; FEAR; FETUS; GABAERGIC SYSTEM; MALE; MAZE TEST; NERVE CELL; NERVE GRAFT; NONHUMAN; PRIORITY JOURNAL; RAT; STARTLE REFLEX;

AMYGDALA; ANIMALS; ANXIETY DISORDERS; AUDITORY PERCEPTION; BEHAVIOR, ANIMAL; BRAIN TISSUE TRANSPLANTATION; EXPLORATORY BEHAVIOR; FEAR; FETAL TISSUE TRANSPLANTATION; GAMMA-AMINOBUTYRIC ACID; MALE; MAZE LEARNING; MOTOR ACTIVITY; NEURONS; NEUROPSYCHOLOGICAL TESTS; RATS; RATS, SPRAGUE-DAWLEY; STARTLE REACTION; VISUAL PERCEPTION;

EID: 70349417739     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2009.06.015     Document Type: Article

References (52)

1. Borlongan C.V., Koutouzis T.K., Poulos S.G., Saporta S., and Sanberg P.R. Bilateral fetal striatal grafts in the 3-nitropropionic acid-induced hypoactive model of Huntington's disease. Cell Transplant 7 (1998) 131-135
2. Cunningham M.G., Donalds R.A., Carlezon Jr. W.A., Hong S., Kim D.S., Kim D.W., et al. Antidepressant effect of stem cell-derived monoaminergic grafts. Neuroreport 18 (2007) 1663-1667
3. Davis M. The role of the amygdala in fear and anxiety. Annu Rev Neurosci 15 (1992) 353-375
4. Davis M., Walker D.L., and Lee Y. Roles of the amygdala and bed nucleus of the stria terminalis in fear and anxiety measured with the acoustic startle reflex. Possible relevance to PTSD. Ann N Y Acad Sci 821 (1997) 305-331
5. Davis M. Neural systems involved in fear and anxiety measured with fear-potentiated startle. Am Psychol 61 (2006) 741-756
6. De Sarro G., Meldrum B.S., and Reavill C. Anticonvulsant action of 2-amino-7-phosphonoheptanoic acid in the substantia nigra. Eur J Pharmacol 106 (1984) 175-179
7. Dong H.W., Petrovich G.D., and Swanson L.W. Topography of projections from amygdala to bed nuclei of the stria terminalis. Brain Res Brain Res Rev 38 (2001) 192-246
8. Fanselow M.S., and Gale G.D. The amygdala, fear, and memory. Ann N Y Acad Sci 985 (2003) 125-134
9. Freund T.F., and Gulyas A.I. Inhibitory control of GABAergic interneurons in the hippocampus. Can J Physiol Pharmacol 75 (1997) 479-487
10. Gernert M., Thompson K.W., Loscher W., and Tobin A.J. Genetically engineered GABA-producing cells demonstrate anticonvulsant effects and long-term transgene expression when transplanted into the central piriform cortex of rats. Exp Neurol 176 (2002) 183-192
11. Goosens K.A., and Maren S. Contextual and auditory fear conditioning are mediated by the lateral, basal, and central amygdaloid nuclei in rats. Learn Mem (Cold Spring Harbor, NY) 8 (2001) 148-155
12. Goosens K.A., and Maren S. Contextual and auditory fear conditioning are mediated by the lateral, basal, and central amygdaloid nuclei in rats. Learn Mem 8 (2008) 148-155
13. Hajizadeh Moghaddam A., Roohbakhsh A., Rostami P., Heidary-Davishani A., and Zarrindast M.R. GABA and histamine interaction in the basolateral amygdala of rats in the plus-maze test of anxiety-like behaviors. Pharmacology 82 (2008) 59-66
14. Jacoby D.B., Lindberg C., Cunningham M.G., Ratliff J., and Dinsmore J. Long-term survival of fetal porcine lateral ganglionic eminance cells in the hippocampus of rats. J Neurosci Res 56 (1999) 581-594
15. 2O PET study. Am J Psychiatry 161 (2004) 748-751
16. Kemppainen S., and Pitkanen A. Distribution of parvalbumin, calretinin, and calbindin-D(28k) immunoreactivity in the rat amygdaloid complex and colocalization with gamma-aminobutyric acid. J Comp Neurol 426 (2000) 441-467
17. Knoll A.T., Meloni E.G., Thomas J.B., Carroll F.I., and Carlezon Jr. W.A. Anxiolytic-like effects of kappa-opioid receptor antagonists in models of unlearned and learned fear in rats. J Pharmacol Exp Ther 323 (2007) 838-845
18. Lang P.J., Davis M., and Ohman A. Fear and anxiety: animal models and human cognitive psychophysiology. J Affect Disord 61 (2000) 137-159
19. LeDoux J. The emotional brain, fear, and the amygdala. Cell Mol Neurobiol 23 (2003) 727-738
20. LeDoux J.E., Cicchetti P., Xagoraris A., and Romanski L.M. The lateral amygdaloid nucleus: sensory interface of the amygdala in fear conditioning. J Neurosci 10 (1990) 1062-1069
21. LeDoux J.E. The Amygdala. In: Aggleton J.P. (Ed). The amygdala and emotion: a view through fear (2000), Oxford University Press, Oxford 289-310
22. Loscher W., and Ebert U. Basic mechanisms of seizure propagation: targets for rational drug design and rational polypharmacy. Epilepsy Res Suppl 11 (1996) 17-43
23. Loscher W., Ebert U., Lehmann H., Rosenthal C., and Nikkhah G. Seizure suppression in kindling epilepsy by grafts of fetal GABAergic neurons in rat substantia nigra. J Neurosci Res 51 (1998) 196-209
24. Maren S., and Fanselow M.S. Synaptic plasticity in the basolateral amygdala induced by hippocampal formation stimulation in vivo. J Neurosci 15 (1995) 7548-7564
25. Maren S. Pavlovian fear conditioning as a behavioral assay for hippocampus and amygdala function: cautions and caveats. Eur J Neurosci 28 (2008) 1661-1666
26. McDonald A.J. Coexistence of somatostatin with neuropeptide Y, but not with cholecystokinin or vasoactive intestinal peptide, in neurons of the rat amygdala. Brain Res 500 (1989) 37-45
27. McDonald A.J., and Mascagni F. Parvalbumin-containing interneurons in the basolateral amygdala express high levels of the alpha1 subunit of the GABAA receptor. J Comp Neurol 473 (2004) 137-146
28. Muller J., Corodimas K.P., Fridel Z., and LeDoux J.E. Functional inactivation of the lateral and basal nuclei of the amygdala by muscimol infusion prevents fear conditioning to an explicit conditioned stimulus and to contextual stimuli. Behav Neurosci 111 (1997) 683-691
29. Muller J.F., Mascagni F., and McDonald A.J. Synaptic connections of distinct interneuronal subpopulations in the rat basolateral amygdalar nucleus. J Comp Neurol 456 (2003) 217-236
30. Nikkhah G., Olsson M., Eberhard J., Bentlage C., Cunningham M.G., and Bjorklund A. A microtransplantation approach for cell suspension grafting in the rat Parkinson model: a detailed account of the methodology. Neuroscience 63 (1994) 57-72
31. Pakzaban P., Burns D.T., and Isacson O L.H. Increased proportion of acetylcholinesterase-rich zones and improved morphological integration in host striatum of fetal grafts derived from the lateral but not the medial ganglionic eminance. Exp Brain Res 97 (1993) 13-22
32. Pape H.C., and Stork O. Genes and mechanisms in the amygdala involved in the formation of fear memory. Ann N Y Acad Sci 985 (2003) 92-105
33. Pare D., and Gaudreau H. Projection cells and interneurons of the lateral and basolateral amygdala: distinct firing patterns and differential relation to theta and delta rhythms in conscious cats. J Neurosci 16 (1996) 3334-3350
34. Pare D., Royer S., Smith Y., and Lang E.J. Contextual inhibitory gating of impulse traffic in the intra-amygdaloid network. Ann N Y Acad Sci 985 (2003) 78-91
35. Pellow S., Chopin P., File S.E., and Briley M. Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J Neurosci Methods 14 (1985) 149-167
36. Pitkanen A., Savander V., and LeDoux J.E. Organization of intra-amygdaloid circuitries in the rat: an emerging framework for understanding functions of the amygdala. Trends Neurosci 20 (1997) 517-523
37. Quirk G.J., and Gehlert D.R. Inhibition of the amygdala: key to pathological states?. Ann N Y Acad Sci 985 (2003) 263-272
38. Sajdyk T.J., and Shekhar A. Sodium lactate elicits anxiety in rats after repeated GABA receptor blockade in the basolateral amygdala. Eur J Pharmacol 394 (2000) 265-273
39. Sanders S.K., Morzorati S.L., and Shekhar A. Priming of experimental anxiety by repeated subthreshold GABA blockade in the rat amygdala. Brain Res 699 (1995) 250-259
40. Sanders S.K., and Shekhar A. Regulation of anxiety by GABAA receptors in the rat amygdala. Pharmacol Biochem Behav 52 (1995) 701-706
41. Sirinathsinghji D.J., Dunnett S.B., Isacson O., Clarke D.J., Kendrick K., and Bjorklund A. Striatal grafts in rats with unilateral neostriatal lesions-II. In vivo monitoring of GABA release in globus pallidus and substantia nigra. Neuroscience 24 (1988) 803-811
42. Sloviter R.S., Ali-Akbarian L., Horvath K.D., and Menkens K.A. Substance P receptor expression by inhibitory interneurons of the rat hippocampus: enhanced detection using improved immunocytochemical methods for the preservation and colocalization of GABA and other neuronal markers. J Comp Neurol 430 (2001) 283-305
43. Takagi M., and Yamamoto C. The long-lasting inhibition recorded in vitro from the lateral nucleus of the amygdala. Brain Res 206 (1981) 474-478
44. Walker D.L., Cassella J.V., Lee Y., De Lima T.C.L., and Davis M. Opposing roles of the amygdala and dorsolateral periaqueductal gray in fear-potentiated startle. Neurosci Biobehav Rev 21 (1997) 743-753
45. Walker D.L., and Davis M. Double dissociation between the involvement of the bed nucleus of the stria terminalis and the central nucleus of the amygdala in startle increases produced by conditioned versus unconditioned fear. J Neurosci 17 (1997) 9375-9383
46. Walker D.L., Toufexis D.J., and Davis M. Role of the bed nucleus of the stria terminalis versus the amygdala in fear, stress, and anxiety. Eur J Pharmacol 463 (2003) 199-216
47. Walker D.L., and Davis M. Role of the extended amygdala in short-duration versus sustained fear: a tribute to Dr. Lennart Heimer. Brain Struct Funct 213 (2008) 29-42
48. Watts C., Brasted P.J., and Dunnett S.B. The morphology, integration, and functional efficacy of striatal grafts differ between cell suspensions and tissue pieces. Cell Transplant 9 (2000) 395-407
49. Weiss I.C., Pryce C.R., Jongen-Relo A.L., Nanz-Bahr N.I., and Feldon J. Effect of social isolation on stress-related behavioural and neuroendocrine state in the rat. Behav Brain Res 152 (2004) 279-295
50. Wictorin K., Isacson O., Fischer W., Nothias F., Peschanski M., and Bjorklund A. Connectivity of striatal grafts implanted into the ibotenic acid-lesioned striatum-I. Subcortical afferents. Neuroscience 27 (1988) 547-562
51. Wictorin K., Simerly R.B., Isacson O., Swanson L.W., and Bjorklund A. Connectivity of striatal grafts implanted into the ibotenic acid-lesioned striatum-III. Efferent projecting graft neurons and their relation to host afferents within the grafts. Neuroscience 30 (1989) 313-330
52. Wilensky A.E., Schafe G.E., and LeDoux J.E. Functional inactivation of the amygdala before but not after auditory fear conditioning prevents memory formation. J Neurosci 19 (1999) RC48