Cholecystokinin excites interneurons in rat basolateral amygdala

Journal of Neurophysiology

Volumn 102, Issue 1, 2009, Pages 272-284

  Chung, Leeyup ^a   Moore, Scott D ^a,b  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b DURHAM VA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLECYSTOKININ;

AMYGDALOID NUCLEUS; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; INTERNEURON; MALE; NONHUMAN; POTASSIUM CURRENT; PRIORITY JOURNAL; RAT; SYNAPTIC INHIBITION; SYNAPTIC TRANSMISSION;

AMYGDALA; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; BENZODIAZEPINES; BIOPHYSICS; BORON COMPOUNDS; CADMIUM; CALCIUM; CALCIUM CHANNEL BLOCKERS; CHOLAGOGUES AND CHOLERETICS; CHOLECYSTOKININ; ELECTRIC STIMULATION; IMIDAZOLES; INTERNEURONS; MALE; PATCH-CLAMP TECHNIQUES; POTASSIUM CHANNEL BLOCKERS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, CHOLECYSTOKININ B; SODIUM CHANNEL BLOCKERS; TETRAETHYLAMMONIUM; TETRODOTOXIN;

EID: 67649619178     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.90769.2008     Document Type: Article

References (64)

1. Ascoli GA, Alonso-Nanclares L, Anderson SA, Barrionuevo G, Benavides- Piccione R, Burkhalter A, Buzsáki G, Cauli B, Defelipe J, Fairen A, Feldmeyer D, Fishell G, Fregnac Y, Freund TF, Gardner D, Gardner EP, Goldberg JH, Helmstaedter M, Hestrin S, Karube F, Kisvarday ZF, Lambolez B, Lewis DA, Marin O, Markram H, Munoz A, Packer A, Petersen CC, Rockland KS, Rossier J, Rudy B, Somogyi P, Staiger JF, Tamas G, Thomson AM, Toledo-Rodriguez M, Wang Y, West DC, Yuste R. Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat Rev Neurosci 9: 557-568, 2008. (Pubitemid 351873463)
2. Chu Z, Galarreta M, Hestrin S. Synaptic interactions of late-spiking neocortical neurons in layer 1. J Neurosci 23: 96-102, 2003. (Pubitemid 36050408)
3. Chung L, Moore SD. Cholecystokinin excites local interneurons in rat basolateral amygdala through CCKB receptors. Soc Neurosci Abstr 145.17, 2007a.
4. Chung L, Moore SD. Cholecystokinin enhances GABAergic inhibitory transmission in basolateral amygdala. Neuropeptides 41: 453-463, 2007b. (Pubitemid 350101822)
5. + conductance. J Neurophysiol 74: 990-1000, 1995.
6. Davis M. The role of the amygdala in conditioned and unconditioned fear and anxiety. In: The Amygdala, edited by Aggleton JP. New York: Oxford Univ. Press, 2000, p. 213-287.
7. Davis M, Rainnie D, Cassell M. Neurotransmission in the rat amygdala related to fear and anxiety. Trends Neurosci 17: 208-214, 1994. (Pubitemid 24128464)
8. Dodd J, Kelly JS. The actions of cholecystokinin and related peptides on pyramidal neurones of the mammalian hippocampus. Brain Res 205: 337-350, 1981. (Pubitemid 11209816)
9. Faber ES, Sedlak P, Vidovic M, Sah P. Synaptic activation of transient receptor potential channels by metabotropic glutamate receptors in the lateral amygdala. Neuroscience 137: 781-794, 2006. (Pubitemid 43053943)
10. Foehring RC, Scroggs RS. Multiple high-threshold calcium currents in acutely isolated rat amygdaloid pyramidal cells. J Neurophysiol 71: 433-436, 1994. (Pubitemid 24058868)
11. Frankland PW, Josselyn SA, Bradwejn J, Vaccarino FJ, Yeomans JS. Activation of amygdala cholecystokininB receptors potentiates the acoustic startle response in the rat. J Neurosci 17: 1838-1847, 1997. (Pubitemid 27089828)
12. Freund TF, Buzsáki G. Interneurons of the hippocampus. Hippocampus 6: 347-470, 1996. (Pubitemid 126682925)
13. Gittis AH, du Lac S. Firing properties of GABAergic vs. non-GABAergic vestibular nucleus neurons conferred by a differential balance of potassium currents. J Neurophysiol 97: 3986-3996, 2007. (Pubitemid 47080633)
14. Haj-Dahmane S, Andrade R. Muscarinic activation of a voltage-dependent cation nonselective current in rat association cortex. J Neurosci 16: 3848-3861, 1996. (Pubitemid 26176049)
15. Halabisky B, Shen F, Huguenard JR, Prince DA. Electrophysiological classification of somatostatin-positive interneurons in mouse sensorimotor cortex. J Neurophysiol 96: 834-845, 2006. (Pubitemid 44155221)
16. Hodges H, Green S, Glenn B. Evidence that the amygdala is involved in benzodiazepine and serotonergic effects on punished responding but not on discrimination. Psychopharmacology (Berl) 92: 491-504, 1987. (Pubitemid 17105248)
17. Ivy AC, Oldberg E. A hormone mechanism for gall-bladder contraction and evacuation. Am J Physiol 86: 599-613, 1928.
18. Kawaguchi Y. Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex. J Neurosci 15: 2638-2655, 1995.
19. Kawaguchi Y, Kubota Y. Physiological and morphological identification of somatostatin- or vasoactive intestinal polypeptide-containing cells among GABAergic cell subtypes in rat frontal cortex. J Neurosci 16: 2701-2715, 1996. (Pubitemid 26122686)
20. Kim M, Campeau S, Falls WA, Davis M. Infusion of the non-NMDA receptor antagonist CNQX into the amygdala blocks the expression of fear-potentiated startle. Behav Neural Biol 59: 5-8, 1993. (Pubitemid 23092518)
21. Lang EJ, Paré D. Similar inhibitory processes dominate the responses of cat lateral amygdaloid projection neurons to their various afferents. J Neurophysiol 77: 341-352, 1997. (Pubitemid 27053788)
22. LeDoux JE. Emotion circuits in the brain. Annu Rev Neurosci 23: 155-184, 2000.
23. Likhtik E, Popa D, Apergis-Schoute J, Fidacaro GA, Paré D. Amygdala intercalated neurons are required for expression of fear extinction. Nature 454: 642-645, 2008.
24. Lowry CA, Johnson PL, Hay-Schmidt A, Mikkelsen J, Shekhar A. Modulation of anxiety circuits by serotonergic systems. Stress 8: 233-246, 2005. (Pubitemid 43163256)
25. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C. Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5: 793-807, 2004. (Pubitemid 39336216)
26. Mascagni F, McDonald AJ. Immunohistochemical characterization of cholecystokinin containing neurons in the rat basolateral amygdala. Brain Res 976: 171-184, 2003. (Pubitemid 36570453)
27. Mascagni F, McDonald AJ. A novel subpopulation of 5-HT type 3A receptor subunit immunoreactive interneurons in the rat basolateral amygdala. Neuroscience 144: 1015-1024, 2007. (Pubitemid 46013989)
28. McDonald AJ. Neuronal organization of the lateral and basolateral amygdaloid nuclei in the rat. J Comp Neurol 222: 589-606, 1984. (Pubitemid 14198627)
29. McDonald AJ. Glutamate and aspartate immunoreactive neurons of the rat basolateral amygdala: colocalization of excitatory amino acids and projections to the limbic circuit. J Comp Neurol 365: 367-379, 1996. (Pubitemid 26044058)
30. McDonald AJ, Mascagni F. Colocalization of calcium-binding proteins and GABA in neurons of the rat basolateral amygdala. Neuroscience 105: 681-693, 2001. (Pubitemid 32769832)
31. Meis S, Munsch T, Sosulina L, Pape HC. Postsynaptic mechanisms underlying responsiveness of amygdaloid neurons to cholecystokinin are mediated by a transient receptor potential-like current. Mol Cell Neurosci 35: 356-367, 2007. (Pubitemid 46843571)
32. + conductance in hippocampal interneurons. J Neurosci 17: 4994-5003, 1997.
33. Miserendino MJ, Sananes CB, Melia KR, Davis M. Blocking of acquisition but not expression of conditioned fear-potentiated startle by NMDA antagonists in the amygdala. Nature 345: 716-718, 1990. (Pubitemid 20186547)
34. Miyoshi G, Butt SJ, Takebayashi H, Fishell G. Physiologically distinct temporal cohorts of cortical interneurons arise from telencephalic Olig2- expressing precursors. J Neurosci 27: 7786-7798, 2007. (Pubitemid 47093809)
35. Noble F, Wank SA, Crawley JN, Bradwejn J, Seroogy KB, Hamon M, Roques BP. International Union of Pharmacology. XXI. Structure, distribution, and functions of cholecystokinin receptors. Pharmacol Rev 51: 745-781, 1999.
36. Paré D, 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: 3334-3350, 1996. (Pubitemid 26142366)
37. Phelps EA, LeDoux JE. Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron 48: 175-187, 2005. (Pubitemid 41476352)
38. Price CJ, Cauli B, Kovacs ER, Kulik A, Lambolez B, Shigemoto R, Capogna M. Neurogliaform neurons form a novel inhibitory network in the hippocampal CA1 area. J Neurosci 25: 6775-6786, 2005. (Pubitemid 41023145)
39. Quirk GJ, Likhtik E, Pelletier JG, Paré D. Stimulation of medial prefrontal cortex decreases the responsiveness of central amygdala output neurons. J Neurosci 23: 8800-8807, 2003. (Pubitemid 37176661)
40. Rainnie DG. Serotonergic modulation of neurotransmission in the rat basolateral amygdala. J Neurophysiol 82: 69-85, 1999. (Pubitemid 29330062)
41. Rainnie DG, Mania I, Mascagni F, McDonald AJ. Physiological and morphological characterization of parvalbumin-containing interneurons of the rat basolateral amygdala. J Comp Neurol 498: 142-161, 2006. (Pubitemid 44198739)
42. Ramsey IS, Delling M, Clapham DE. An introduction to TRP channels. Annu Rev Physiol 68: 619-647, 2006.
43. Ratzliff AD, Soltesz I. Differential immunoreactivity for alpha-actinin-2, an N-methyl-D-aspartate-receptor/actin binding protein, in hippocampal interneurons. Neuroscience 103: 337-349, 2001. (Pubitemid 32201921)
44. Riccio A, Medhurst AD, Mattei C, Kelsell RE, Calver AR, Randall AD, Benham CD, Pangalos MN. mRNA distribution analysis of human TRPC family in CNS and peripheral tissues. Brain Res Mol Brain Res 109: 95-104, 2002. (Pubitemid 36082877)
45. Rotzinger S, Vaccarino FJ. Cholecystokinin receptor subtypes: role in the modulation of anxiety-related and reward-related behaviours in animal models. J Psychiatry Neurosci 28: 171-181, 2003. (Pubitemid 36836443)
46. + channels designed for high-frequency repetitive firing. Trends Neurosci 24: 517-526, 2001.
47. Sajdyk TJ, Johnson PL, Leitermann RJ, Fitz SD, Dietrich A, Morin M, Gehlert DR, Urban JH, Shekhar A. Neuropeptide Y in the amygdala induces long-term resilience to stress-induced reductions in social responses but not hypothalamic-adrenal-pituitary axis activity or hyperthermia. J Neurosci 28: 893-903, 2008. (Pubitemid 351159007)
48. Sajdyk TJ, Schober DA, Gehlert DR. Neuropeptide Y receptor subtypes in the basolateral nucleus of the amygdala modulate anxiogenic responses in rats. Neuropharmacology 43: 1165-1172, 2002. (Pubitemid 36009370)
49. Sajdyk TJ, Shekhar A. Excitatory amino acid receptor antagonists block the cardiovascular and anxiety responses elicited by gamma-aminobutyric acidA receptor blockade in the basolateral amygdala of rats. J Pharmacol Exp Ther 283: 969-977, 1997. (Pubitemid 27514662)
50. Scheel-Kruger J, Petersen EN. Anticonflict effect of the benzodiazepines mediated by a GABAergic mechanism in the amygdala. Eur J Pharmacol 82: 115-116, 1982. (Pubitemid 12039155)
51. Sherrin T, Todorovic C, Zeyda T, Tan CH, Hon PW, Zhu YZ, Spiess J. Chronic stimulation of corticotropin-releasing factor receptor 1 enhances the anxiogenic response of the cholecystokinin system. Mol Psychiatry 14: 291-307, 2009.
52. Sosulina L, Meis S, Seifert G, Steinhauser C, Pape HC. Classification of projection neurons and interneurons in the rat lateral amygdala based upon cluster analysis. Mol Cell Neurosci 33: 57-67, 2006. (Pubitemid 44291590)
53. Strubing C, Krapivinsky G, Krapivinsky L, Clapham DE. TRPC1 and TRPC5 form a novel cation channel in mammalian brain. Neuron 29: 645-655, 2001. (Pubitemid 32323938)
54. Sugita S, Tanaka E, North RA. Membrane properties and synaptic potentials of three types of neurone in rat lateral amygdala. J Physiol 460: 705-718, 1993. (Pubitemid 23058074)
55. Thorn P, Petersen OH. Activation of nonselective cation channels by physiological cholecystokinin concentrations in mouse pancreatic acinar cells. J Gen Physiol 100: 11-25, 1992.
56. Tsujino N, Yamanaka A, Ichiki K, Muraki Y, Kilduff TS, Yagami K, Takahashi S, Goto K, Sakurai T. Cholecystokinin activates orexin/hypocretin neurons through the cholecystokinin A receptor. J Neurosci 25: 7459-7469, 2005. (Pubitemid 41129819)
57. Uematsu M, Hirai Y, Karube F, Ebihara S, Kato M, Abe K, Obata K, Yoshida S, Hirabayashi M, Yanagawa Y, Kawaguchi Y. Quantitative chemical composition of cortical GABAergic neurons revealed in transgenic venus-expressing rats. Cereb Cortex 18: 315-330, 2008. (Pubitemid 351197789)
58. Vanderhaeghen JJ, Signeau JC, Gepts W. New peptide in the vertebrate CNS reacting with antigastrin antibodies. Nature 257: 604-605, 1975.
59. Wang B, Sims SM. CCK regulates nonselective cation channels in guinea pig gastric smooth muscle cells. Am J Physiol Gastrointest Liver Physiol 274: G709-G717, 1998. (Pubitemid 28217727)
60. Wank SA. Cholecystokinin receptors. Am J Physiol Gastrointest Liver Physiol 269: G628-G646, 1995. (Pubitemid 3005920)
61. Woodruff AR, Sah P. Inhibition and synchronization of basal amygdala principal neuron spiking by parvalbumin-positive interneurons. J Neurophysiol 98: 2956-2961, 2007a. (Pubitemid 350127953)
62. Woodruff AR, Sah P. Networks of parvalbumin-positive interneurons in the basolateral amygdala. J Neurosci 27: 553-563, 2007b. (Pubitemid 46143759)
63. Yang YM, Chung JM, Rhim H. Cholecystokinin-8S-induced intracellular calcium signaling in acutely isolated periaqueductal gray neurons of the rat. Biol Pharm Bull 30: 297-302, 2007. (Pubitemid 46255365)
64. Zhang C, Roepke TA, Kelly MJ, Ronnekleiv OK. Kisspeptin depolarizes gonadotropin-releasing hormone neurons through activation of TRPC-like cationic channels. J Neurosci 28: 4423-4434, 2008.