Inhibitory neurons in the anterior piriform cortex of the mouse: Classification using molecular markers

Journal of Comparative Neurology

Volumn 518, Issue 10, 2010, Pages 1670-1687

  Suzuki, Norimitsu ^a   Bekkers, John M ^a  

^a Biology and Environment   (Australia)

Author keywords

Antibody; Cerebral cortex; GABA; GAD; Gfp; Olfactory

Indexed keywords

4 AMINOBUTYRIC ACID; CALBINDIN; CALRETININ; CHOLECYSTOKININ; GLUTAMATE DECARBOXYLASE 67; GREEN FLUORESCENT PROTEIN; MOLECULAR MARKER; NEUROPEPTIDE Y; PARVALBUMIN; SOMATOSTATIN; VASOACTIVE INTESTINAL POLYPEPTIDE;

4 AMINOBUTYRIC ACID RELEASE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL LABELING; CELL SIZE; CELL STRUCTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; FLUORESCENCE ANALYSIS; INTERNEURON; INTRACELLULAR RECORDING; MOUSE; NERVE CELL; NERVE PROJECTION; NONHUMAN; OLFACTORY CORTEX; OLFACTORY DISCRIMINATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRIFORM CORTEX; SENSORY EVALUATION; TRANSGENIC MOUSE;

ANIMALS; BIOLOGICAL MARKERS; GAMMA-AMINOBUTYRIC ACID; GLUTAMATE DECARBOXYLASE; GLUTAMIC ACID; GREEN FLUORESCENT PROTEINS; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURAL INHIBITION; NEURONS; OLFACTORY PATHWAYS; PATCH-CLAMP TECHNIQUES; RECOMBINANT FUSION PROTEINS;

EID: 77952231652     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22295     Document Type: Article

References (58)

1. Baraban SC, Tallent MK. 2004. Interneuronal neuropeptides- endogenous regulators of neuronal excitability. Trends Neurosci 27:135-142.
2. Barnes DC, Hofacer RD, Zaman AR, Rennaker RL, Wilson DA. 2008. Olfactory perceptual stability and discrimination. Nat Neurosci 11:1378-1380.
3. Bekkers JM. 2000. Properties of voltage-gated potassium currents in nucleated patches from large Layer 5 cortical pyramidal neurons of the rat. J Physiol 525:593-609.
4. Brown M, Renehan WE, Schweitzer L 2000. Changes in GABAimmunoreactrvity during development of the rostral subdivision of the nucleus of the solitary tract. Neuroscience 100: 849-859.
5. Buchán AM, Sikora LK, Levy JG, Mcintosh CH, Dyck I, Brown JC. 1985. An immunoeytochemical investigation with monoclonal antibodies to somatostatin. Histochemistry 83:175-180. (Pubitemid 15045710)
6. Celio MR, Baier W, Scharer L, de Viragh PA, Gerday C. 1988. Monoclonal antibodies directed against the calcium binding protein parvalbumin. Cell Calcium 9:81-86.
7. Chattopadhyaya B, Di Cristo G, Wu CZ, Knott G, Kuhlman S, Fu Y, Palmiter RD, Huang ZJ. 2007. GAD67-mediated GABA synthesis and signaling regulate inhibitory synaptic innervation in the visual cortex. Neuron 54:889-903. (Pubitemid 46907499)
8. Cho HJ, Takagi H. 1993. Cholecystokinin (CCK)-8-immunoreactivity in the piriform cortex of the rat with special reference to its fine structures. Osaka City Med J 39:75-92.
9. Cummings SL. 1997. Neuropeptide Y, somatostatin, and cholecystokinin of the anterior piriform cortex. Cell Tissue Res 289: 39-51.
10. Edwards RH. 2007. The neurotransmitter cycle and quantal size. Neuron 55:835-858.
11. Ekstrand JJ, Domroese ME, Feig SL, Illig KR, Haberly LB. 2001a. Immunoeytochemical analysis of basket cells in rat piriform cortex. J Comp Neurol 434:308-328.
12. Ekstrand JJ, Domroese ME, Johnson DM, Feig SL, Knodel SM, Behan M, Haberly LB. 2001b. A new subdivision of anterior piriform cortex and associated deep nucleus with novel features of interest for olfaction and epilepsy. J Comp Neurol 434:289-307. (Pubitemid 32402136)
13. Esclapez M, Tillakaratne NJ, Kaufman DL, Tobin AJ, Houser CR. 1994. Comparative localization of two forms of glutamic acid decarboxylase and their mRNAs in rat brain supports the concept of functional differences between the forms. J Neurosci 14:1834-1855. (Pubitemid 24080030)
14. Franks KM, Isaacson JS. 2006. Strong single-fiber sensory inputs to olfactory cortex: implications for olfactory coding. Neuron 49:357-363.
15. Frassoni C, Radici C, Spreafico R, de Curtis M. 1998. Calciumbinding protein immunoreactivity in the piriform cortex of the guinea-pig: selective staining of subsets of non-GABAergic neurons by calretinin. Neuroscience 83:229-237. (Pubitemid 28068052)
16. Freund TF. 2003. Interneuron diversity series: rhythm and mood in perisomatic inhibition. Trends Neurosci 26:489-495.
17. Glickfeld LL, Scanziani M. 2006. Distinct timing in the activity of cannabinoid-sensitive and cannabinoid-insensitive basket cells. Nat Neurosci 9:807-815.
18. Guillery RW. 2002. On counting and counting errors. J Comp Neurol 447:1-7.
19. Hartwich K, Pollak T, Klausberger T. 2009. Distinct firing patterns of identified basket and dendrite-targeting interneurons in the prefrontal cortex during hippocampal theta and local spindle oscillations. J Neurosci 29:9563-9574.
20. Hefft S, Jonas P. 2005. Asynchronous GABA release generates long-lasting inhibition at a hippocampal interneuron-principal neuron synapse. Nat Neurosci 8:1319-1328. (Pubitemid 41630419)
21. Heinke B, Ruscheweyh R, Forsthuber L, Wunderbaldinger G, Sandkuhler J. 2004. Physiological, neurochemical and morphological properties of a subgroup of GABAergic spinal lamina II neurones identified by expression of green fluorescent protein in mice. J Physiol 560:249-266. (Pubitemid 39406030)
22. Ikeda K, Yanagawa Y, BekkersJM. 2008. Distinctive quantal properties of neurotransmission at excitatory and inhibitory autapses revealed using variance-mean analysis. J Neurosci 28: 13563-13573.
23. A- mediated IPSCs in piriform cortex have fast and slow components with different properties and locations on pyramidal cells. J Neurophysiol 78:2531-2545.
24. Kawaguchi Y, Kubota Y. 1997. GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb Cortex 7:476-486. (Pubitemid 27353633)
25. Klausberger T, Marton LF, O'Neill J, Huck JH, Dalezios Y, Fuentealba P, Suen WY, Papp E, Kaneko T, Watanabe M, Csicsvari J, Somogyi P. 2005. Complementary roles of cholecystokinin- and parvalbumin-expressing GABAergic neurons in hippocampal network oscillations. J Neurosci 25:9782-9793. (Pubitemid 41510918)
26. Kubota Y, Jones EG. 1993. Co-localization of two calcium binding proteins in GABA cells of rat piriform cortex. Brain Res 600: 339-344. (Pubitemid 23035638)
27. Lopez-Bendito G, Sturgess K, Erdelyi F, Szabo G, Moinar Z, Paulsen O. 2004. Preferential origin and layer destination of GAD65-GFP cortical interneurons. Cereb Cortex 14:1122-1133.
28. Magistretti J, De Curtis M. 1998. Low-voltage activated T-type calcium currents are differently expressed in superficial and deep layers of guinea pig piriform cortex. J Neurophysiol 79: 808-816.
29. Markakis EA, Palmer TD, Randolph-Moore L, Rakic P, Gage FH. 2004. Novel neuronal phenotypes from neural progenitor cells. J Neurosci 24:2886-2897.
30. 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.
31. McBain CJ, Fisahn A. 2001. Interneurons unbound. Nat Rev Neurosci 2:11-23.
32. Nakamura M, Sato K, Fukaya M, Araishi K, Aiba A, Kano M, Watanabe M. 2004. Signaling complex formation of phospholipase Cß4 with metabotropic glutamate receptor type 1α and 1,4,5-trisphosphate receptor at the perisynapse and endoplasmic reticulum in the mouse brain. Eur J Neurosci 20: 2929-2944.
33. Neville KR, Haberly LB. 2004. Olfactory cortex. In: Shepherd GM, editor. The synaptic organization of the brain, 5th ed. New York: Oxford University Press, p 415-454.
34. Ohning GV, Wong HC, Walsh JH. 1994. Differential kinetics for immunoneutralization of circulating gastrin by gastrin monoclonal antibody and its Fab1 fragment in rats. Peptides 15: 417-423. (Pubitemid 124016315)
35. Ohning GV, Wong HC, Lloyd KC, Walsh JH. 1996. Gastrin mediates the gastric mucosal proliferative response to feeding. Am J Physiol 271:G470-476.
36. Ono M, Yanagawa Y, Koyano K. 2005. GABAergic neurons in inferior colliculus of the GAD67-GFP knock-in mouse: electrophysiological and morphological properties. Neurosci Res 51: 475-492. (Pubitemid 40299335)
37. Poo C, Isaacson JS. 2009. Odor representations in olfactory cortex: "sparse" coding, global inhibition, and oscillations. Neuron 62:850-861.
38. Pouille F, Scanziani M. 2004. Routing of spike series by dynamic circuits in the hippocampus. Nature 429:717-723. (Pubitemid 38833116)
39. Price CJ, Cauli B, Kovacs ER, Kulik A, Lambolez B, Shigemoto R, Capogna M. 2005. Neurogliaform neurons form a novel inhibitory network in the hippocampal CA1 area. J Neurosci 25: 6775-6786. (Pubitemid 41023145)
40. Sanides-Kohlrausch C, Wahle P. 1990. VIP- and PHIimmunoreactivity in olfactory centers of the adult cat. J Comp Neurol 294:325-339. (Pubitemid 20117249)
41. Schwaller B, Dick J, Dhoot G, Carroll S, Vrbová G, Nicotera P, Pette D, Wyss A, Bluethmann H, Hunziker W, Celio MR. 1999. Prolonged contraction-relaxation cycle of fasttwitch muscles in parvalbumin knockout mice. Am J Physiol 276:C395-403. (Pubitemid 29100563)
42. Sharp FR, Gonzalez MF, Sagar SM. 1987. Fetal frontal cortex transplanted to injured motor/sensory cortex of adult rats. II. VIP-, somatostatin-, and NPY-immunoreactive neurons. J Neurosci 7:3002-3015.
43. Smith PG, Hoffman TL, Reddy H. 1991. Sprouting of aberrant neuropeptide Y-immunoreactive sympathetic nerves into neonatally denervated smooth muscle. Regul Pept 35:103-113.
44. Suzuki N, Bekkers JM. 2006. Neural coding by two classes of principal cells in the mouse piriform cortex. J Neurosci 26: 11938-11947. (Pubitemid 44772105)
45. Suzuki N, Bekkers JM. 2007. Inhibitory interneurons in the piriform cortex. Clin Exp Pharmacol Physiol 34:1064-1069.
46. Tamamaki N, Yanagawa Y, Tomioka R, Miyazaki J, Obata K, Kaneko T. 2003. Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J Comp Neurol 467:60-79.
47. Tamás G, Lorincz A, Simon A, Szabadics J. 2003. Identified sources and targets of slow inhibition in the neocortex. Science 299:1902-1905.
48. Terada N, Banno Y, Ohno N, Fujii Y, Murate T, Sarna JR, Hawkes R, Zea Z, Baba T, Ohno S. 2004. Compartmentation of the mouse cerebellar cortex by sphingosine kinase. J Comp Neurol 469: 119-127.
49. Tseng G-F, Haberly LB. 1989. Deep neurons in piriform cortex. I. Morphology and synaptically evoked responses including a unique high-amplitude paired shock facilitation. J Neurophysiol 62:369-385.
50. Uematsu M, Hirai Y, Karube F, Ebihara S, Kato M, Abe K, Obata K, Yoshida S, Hirabayashi M, Yanagawa Y, Kawaguchi Y. 2008. Quantitative chemical composition of cortical GABAergic neurons revealed in transgenic venus-expressing rats. Cereb Cortex 18:315-330.
51. Westenbroek RE, Westrum LE, Hendrickson AE, Wu JY. 1987. Immunoeytochemical localization of cholecystokinin and glutamic acid decarboxylase during normal development in the prepyriform cortex of rats. Brain Res 431:191-206.
52. Wilson DA, Stevenson RJ. 2003. Olfactory perceptual learning: the critical role of memory in odor discrimination. Neurosci Biobehav Rev 27:307-328.
53. Winsky L, Isaacs KR, Jacobowitz DM. 1996. Calretinin mRNA and immunoreactivity in the medullary reticular formation of the rat colocalization with glutamate receptors. Brain Res 741: 123-133.
54. Wolansky T, Pagliardini S, Greer JJ, Dickson CT. 2007. Immunohistochemical characterization of substance P receptor (NK(1)R)-expressing interneurons in the entorhinal cortex. J Comp Neurol 502:427-441.
55. Wong HC, Sternini C, Lloyd K, De Giorgio R, Walsh JH. 1996. Monoclonal antibody to VIP: production, characterization, ¡mmunoneutralizing activity, and usefulness in cytochemical staining. Hybridoma 15:133-139.
56. Wyszynski M, Kharazia V, Shanghvi R, Rao A, Beggs AH, Craig AM, Weinberg R, Sheng M. 1998. Differential regional expression and ultrastructural localization of a-actinin-2, a putative NMDA receptor-anchoring protein, in rat brain. J Neurosci 18:1383-1392.
57. Yuste R. 2005. Origin and classification of neocortical interneurons. Neuron 48:524-527.
58. Zhang C, Szabo G, Erdelyi F, Rose JD, Sun QQ 2006. Novel interneuronal network in the mouse posterior piriform cortex. J Comp Neurol 499:1000-1015.