Distinctive classes of GABAergic interneurons provide layer-specific phasic inhibition in the anterior piriform cortex

Cerebral Cortex

Volumn 20, Issue 12, 2010, Pages 2971-2984

  Suzuki, Norimitsu ^a   Bekkers, John M ^a  

^a Biology and Environment   (Australia)

Author keywords

action potential; GABA; GAD67 GFP; olfaction; synaptic transmission

Indexed keywords

4 AMINOBUTYRIC ACID; MOLECULAR MARKER;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTERIOR PIRIFORM CORTEX; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; INTERNEURON; MORPHOLOGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PYRIFORM CORTEX; SMELLING; SYNAPTIC INHIBITION;

ANIMALS; GAMMA-AMINOBUTYRIC ACID; IMMUNOHISTOCHEMISTRY; INTERNEURONS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; NEURAL INHIBITION; OLFACTORY PATHWAYS; ORGAN CULTURE TECHNIQUES; PATCH-CLAMP TECHNIQUES; SMELL; SYNAPTIC TRANSMISSION;

EID: 77955464777     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhq046     Document Type: Article

References (58)

1. Ascoli GA, Alonso-Nanclares L, Anderson SA, Barrionuevo G, Benavides-Piccione R, Burkhalter A, Buzsaki G, Cauli B, Defelipe J, Fairen A, et al. 2008. Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat Rev Neurosci. 9:557-568.
2. Bathellier B, Margrie TW, Larkum ME. 2009. Properties of piriform cortex pyramidal cell dendrites: implications for olfactory circuit design. J Neurosci. 29:12641-12652.
3. Beierlein M, Gibson JR, Connors BW. 2003. Two dynamically distinct inhibitory networks in layer 4 of the neocortex. J Neurophysiol. 90:2987-3000.
4. Bekkers JM, Clements JD. 1999. Quantal amplitude and quantal variance of strontium-induced asynchronous EPSCs in rat dentate granule neurons. J Physiol. 516:227-248.
5. Buzsaki G, Draguhn A. 2004. Neuronal oscillations in cortical networks. Science. 304:1926-1929.
6. Cang J, Isaacson JS. 2003. In vivo whole-cell recording of odor-evoked synaptic transmission in the rat olfactory bulb. J Neurosci. 23:4108-4116.
7. Chiang E, Strowbridge BW. 2007. Diversity of neural signals mediated by multiple, burst-firing mechanisms in rat olfactory tubercle neurons. J Neurophysiol. 98:2716-2728.
8. Chu Z, Galarreta M, Hestrin S. 2003. Synaptic interactions of late-spiking neocortical neurons in layer 1. J Neurosci. 23:96-102.
9. DeFelipe J. 2002. Cortical interneurons: from Cajal to 2001. Prog Brain Res. 136:215-238.
10. Ekstrand JJ, Domroese ME, Feig SL, Illig KR, Haberly LB. 2001. Immunocytochemical analysis of basket cells in rat piriform cortex. J Comp Neurol. 434:308-328.
11. Franks KM, Isaacson JS. 2006. Strong single-fiber sensory inputs to olfactory cortex: implications for olfactory coding. Neuron. 49:357-363.
12. Freund TF, Katona I. 2007. Perisomatic inhibition. Neuron. 56:33-42.
13. Haberly LB. 1983. Structure of the piriform cortex of the opossum. I. Description of neuron types with Golgi methods. J Comp Neurol. 213:163-187.
14. Haider B, McCormick DA. 2009. Rapid neocortical dynamics: cellular and network mechanisms. Neuron. 62:171-189.
15. Halabisky B, Shen F, Huguenard JR, Prince DA. 2006. Electrophysiolog-ical classification of somatostatin-positive interneurons in mouse sensorimotor cortex. J Neurophysiol. 96:834-845.
16. Helmstaedter M, Sakmann B, Feldmeyer D. 2009. The relation between dendritic geometry, electrical excitability, and axonal projections of L2/3 interneurons in rat barrel cortex. Cereb Cortex. 19:938-950.
17. Hestrin S, Armstrong WE. 1996. Morphology and physiology of cortical neurons in layer I. J Neurosci. 16:5290-5300.
18. Ishikawa T, Sato T, Shimizu A, Tsutsui KI, de Curtis M, Iijima T. 2007. Odor-driven activity in the olfactory cortex of an in vitro isolated guinea-pig whole brain with olfactory epithelium. J Neurophysiol. 97:670-679.
19. Johenning FW, Beed PS, Trimbuch T, Bendels MH, Winterer J, Schmitz D. 2009. Dendritic compartment and neuronal output mode determine pathway-specific long-term potentiation in the piriform cortex. J Neurosci. 29:13649-13661.
20. Kapfer C, Glickfeld LL, Atallah BV, Scanziani M. 2007. Supralinear increase of recurrent inhibition during sparse activity in the somatosensory cortex. Nat Neurosci. 10:743-753.
21. A- mediated IPSCs in piriform cortex have fast and slow components with different properties and locations on pyramidal cells. J Neuro-physiol. 78:2531-2545.
22. Karagiannis A, Gallopin T, David C, Battaglia D, Geoffroy H, Rossier J, Hillman EM, Staiger JF, Cauli B. 2009. Classification of NPY-expressing neocortical interneurons. J Neurosci. 29:3642-3659.
23. Karube F, Kubota Y, Kawaguchi Y. 2004. Axon branching and synaptic bouton phenotypes in GABAergic nonpyramidal cell subtypes. J Neurosci. 24:2853-2865.
24. Kawaguchi Y, Kubota Y. 1996. 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.
25. Kawaguchi Y, Kubota Y. 1997. GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb Cortex. 7:476-486.
26. Kay LM, Beshel J, Brea J, Martin C, Rojas-Libano D, Kopell N. 2009. Olfactory oscillations: the what, how and what for. Trends Neurosci. 32:207-214.
27. Klausberger T, Somogyi P. 2008. Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science. 321:53-57.
28. Laurent G. 2002. Olfactory network dynamics and the coding of multidimensional signals. Nat Rev Neurosci. 3:884-895.
29. Litaudon P, Amat C, Bertrand B, Vigouroux M, Buonviso N. 2003. Piriform cortex functional heterogeneity revealed by cellular responses to odours. Eur J Neurosci. 17:2457-2461.
30. Luna VM, Schoppa NE. 2008. GABAergic circuits control input-spike coupling in the piriform cortex. J Neurosci. 28:8851-8859.
31. Maccaferri G, Lacaille JC. 2003. Interneuron Diversity series: Hippo-campal interneuron classifications\making things as simple as possible, not simpler. Trends Neurosci. 26:564-571.
32. 1B-adrenoceptor-mediated excitation of piriform cortical interneurons. Eur J Pharmacol. 305:95-100.
33. 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.
34. McBain CJ, Fisahn A. 2001. Interneurons unbound. Nat Rev Neurosci. 2:11-23.
35. Mott DD, Dingledine R. 2003. Interneuron diversity series: Interneuron research\challenges and strategies. Trends Neurosci. 26:484-488.
36. Neville KR, Haberly LB. 2003. Beta and gamma oscillations in the olfactory system of the urethane-anesthetized rat. J Neurophysiol. 90:3921-3930.
37. 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.
38. Olah S, Fule M, Komlosi G, Varga C, Baldi R, Barzo P, Tamas G. 2009. Regulation of cortical microcircuits by unitary GABA-mediated volume transmission. Nature. 461:1278-1281.
39. PooC,Isaacson JS. 2009. Odor representationsinolfactorycortex: "sparse" coding, global inhibition, and oscillations. Neuron. 62:850-861.
40. 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.
41. B receptor modulation of feedforward inhibition through hippocampal neuro-gliaform cells. J Neurosci. 28:6974-6982.
42. Protopapas AD, Bower JM. 2000. Physiological characterization of layer III non-pyramidal neurons in piriform (olfactory) cortex of rat. Brain Res. 865:1-11.
43. Rennaker RL, Chen CF, Ruyle AM, Sloan AM, Wilson DA. 2007. Spatial and temporal distribution of odorant-evoked activity in the piriform cortex. J Neurosci. 27:1534-1542.
44. Reyes A, Lujan R, Rozov A, Burnashev N, Somogyi P, Sakmann B. 1998. Target-cell-specific facilitation and depression in neocortical circuits. Nature Neurosci. 1:279-285.
45. Satou M, Mori K, Tazawa Y, Takagi SF. 1983. Interneurons mediating fast postsynaptic inhibition in pyriform cortex of the rabbit. J Neuro-physiol. 50:89-101.
46. Simon A, Olah S, Molnar G, Szabadics J, Tamas G. 2005. Gap-junctional coupling between neurogliaform cells and various interneuron types in the neocortex. J Neurosci. 25:6278-6285.
47. Stettler DD, Axel R. 2009. Representations of odor in the piriform cortex. Neuron. 63:854-864.
48. Suzuki N, Bekkers JM. 2006. Neural coding by two classes of principal cells in the mouse piriform cortex. J Neurosci. 26:11938-11947.
49. Suzuki N, Bekkers JM. 2007. Inhibitory interneurons in the piriform cortex. Clin Exp Pharm Physiol. 34:1064-1069.
50. Suzuki N, Bekkers JM. 2010. Inhibitory neurons in the anterior piriform cortex of the mouse: classification using molecular markers. J Comp Neurol. 518:1670-1687.
51. 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.
52. Tamas G, Buhl EH, Somogyi P. 1997. Fast IPSPs elicited via multiple synaptic release sites by different types of GABAergic neurone in the cat visual cortex. J Physiol. 500:715-738.
53. Tamas G, Lorincz A, Simon A, Szabadics J. 2003. Identified sources and targets of slow inhibition in the neocortex. Science. 299:1902-1905.
54. Uematsu M, Hirai Y, Karube F, Ebihara S, Kato M, Abe K, Obata K, Yoshida S, Hirabayashi M, Yanagawa Y, et al. 2008. Quantitative chemical composition of cortical GABAergic neurons revealed in transgenic venus-expressing rats. Cereb Cortex. 18:315-330.
55. Ward JH. 1963. Hierarchical grouping to optimize an objective function. J Am Stat Assoc. 58:236-244.
56. Wilson DA. 2001. Receptive fields in the rat piriform cortex. Chem Senses. 26:577-584.
57. Woodruff AR, Sah P. 2007. Networks of parvalbumin-positive inter-neurons in the basolateral amygdala. J Neurosci. 27:553-563.
58. Young A, Sun QQ. 2009. GABAergic inhibitory interneurons in the posterior piriform cortex of the GAD67-GFP mouse. Cereb Cortex. 19:3011-3029.