Distinct electrophysiological properties in subtypes of nonspiking olfactory local interneurons correlate with their cell type-specific Ca 2+ current profiles

Journal of Neurophysiology

Volumn 102, Issue 5, 2009, Pages 2834-2845

  Husch, Andreas ^a   Paehler, Moritz ^a   Fusca, Debora ^a   Paeger, Lars ^a   Kloppenburg, Peter ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL TISSUE; ARTICLE; CALCIUM CURRENT; CELL TYPE; ELECTRIC POTENTIAL; ELECTROPHYSIOLOGY; GLOMERULUS; INTERNEURON; NONHUMAN; OLFACTORY DISCRIMINATION; OLFACTORY NERVE; PERIPLANETA; PRIORITY JOURNAL;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; BIOPHYSICAL PHENOMENA; BIOPHYSICS; BRAIN MAPPING; CADMIUM CHLORIDE; CALCIUM; CALCIUM CHANNELS; ELECTRIC STIMULATION; INTERNEURONS; LYSINE; NERVE NET; ODORS; OLFACTORY PATHWAYS; PATCH-CLAMP TECHNIQUES; PERIPLANETA;

EID: 70449433629     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00627.2009     Document Type: Article

References (52)

1. Angstadt JD, Calabrese RL. Calcium currents and graded synaptic transmission between heart interneurons of the leech. J Neurosci 11: 746-759, 1991.
2. Armstrong CM, Bezanilla F. Charge movement associated with the opening and closing of the activation gates of the Na channels. J Gen Physiol 63: 533-552, 1974.
3. + currents in lamina cells of the desert locust schistocerca gregaria. J Exp Biol 202: 1939-1951, 1999.
4. 2+ currents in embryonic cockroach brain neurons. J Neurophysiol 82: 2284-2293, 1999.
5. Burrows M. The Neurobiology of an Insect Brain. New York: Oxford, 1996.
6. Byerly L, Leung HT. Ionic currents of Drosophila neurons in embryonic cultures. J Neurosci 8: 4379-4393, 1988. (Pubitemid 19017418)
7. Davis RL. Olfactory learning. Neuron 44: 31-48, 2004.
8. Demmer H, Kloppenburg P. Intrinsic membrane properties and inhibitory synaptic input of Kenyon cells as mechanisms for sparse coding? J Neurophysiol 102: 1538-1550, 2009.
9. Distler PG, Boeckh J. Synaptic connections between identified neuron types in the antennal lobe glomeruli of the cockroach, Periplaneta americana. II. Local multiglomerular interneurons. J Comp Neurol 383: 529-540, 1997. (Pubitemid 27290839)
10. Distler PG, Gruber C, Boeckh J. Synaptic connections between GABA-immunoreactive neurons and uniglomerular projection neurons within the antennal lobe of the cockroach, Periplaneta americana Synapse 29: 1-13, 1998. (Pubitemid 28155701)
11. Dodt HU, Zieglgänsberger W. Infrared videomicroscopy: a new look at neuronal structure and function. Trends Neurosci 17: 453-458, 1994. (Pubitemid 24321943)
12. Ertel EA, Campbell KP, Harpold MM, Hofmann F, Mori Y, Perez-Reyes E, Schwartz A, Snutch TP, Tanabe T, Birnbaumer L, Tsien RW, Catterall WA. Nomenclature of voltage-gated calcium channels. Neuron 25: 533-535, 2000.
13. Evers JF, Schmitt S, Sibila M, Duch C. Progress in functional neuroanatomy: precise automatic geometric reconstruction of neuronal morphology from confocal image stacks. J Neurophysiol 93: 2331-2342, 2004. (Pubitemid 40404425)
14. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pfluegers 391: 85-100, 1981. (Pubitemid 11012976)
15. Hayashi JH, Levine RB. Calcium and potassium currents in leg motoneurons during postembryonic development in the hawkmoth Manduca sexta. J Exp Biol 171: 15-42, 1992.
16. Heidel E, Pflüger HJ. Ion currents and spiking properties of identified subtypes of locust octopaminergic dorsal unpaired median neurons. Eur J Neurosci 23: 1189-1206, 2006.
17. Hildebrand JG, Shepherd GM. Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu Rev Neurosci 20: 595-631, 1997.
18. Hille B. Ion Channels of Excitable Membranes: Sinauer Associates, Sunderland 2001.
19. Hodgkin AL, Huxley AF. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 117: 500-544, 1952.
20. Homberg U, Müller U. Neuroactive substances in the antennal lobe. In: Insect Olfaction, edited by Hansson BS. New York: Springer, 1999, p. 181-206.
21. 2+ currents from olfactory interneurons in the antennal lobe of Periplaneta americana. J Neurophysiol 99: 320-332, 2008.
22. Husch A, Paehler M, Fusca D, Paeger L, Kloppenburg P. Calcium current diversity in physiologically different local interneuron types of the antennal lobe. J Neurosci 29: 716-726, 2009.
23. 2+ dynamics during spontaneous and evoked activity of leech heart interneurons: low-threshold Ca currents and graded synaptic transmission. J Neurosci 20: 4930-4943, 2000.
24. Ivanov AI, Calabrese RL. Graded inhibitory synaptic transmission between leech interneurons: assessing the roles of two kinetically distinct low-threshold Ca currents. J Neurophysiol 96: 218-234, 2006.
25. King GF. Modulation of insect Cav channels by peptidic spider toxins. Toxicon 49: 513-530, 2007.
26. Kloppenburg P, Ferns D, Mercer AR. Serotonin enhances central olfactory neuron responses to female sex pheromone in the male sphinx moth Manduca sexta. J Neurosci 19: 8172-8181, 1999a. (Pubitemid 30226737)
27. Kloppenburg P, Hörner M. Voltage-activated currents in identified giant interneurons isolated from adult crickets Gryllus bimaculatus. J Exp Biol 201: 2529-2541, 1998. (Pubitemid 28456194)
28. Kloppenburg P, Kirchhof BS, Mercer AR. Voltage-activated currents from adult honeybee (Apis mellifera) antennal motor neurons recorded in vitro and in situ. J Neurophysiol 81: 39-48, 1999b. (Pubitemid 29264152)
29. Laurent G, Seymour-Laurent KJ, Johnson K. Dendritic excitability and a voltage-gated calcium current in locust nonspiking local interneurons. J Neurophysiol 69: 1484-1498, 1993. (Pubitemid 23162394)
30. 2+ currents in graded and spike-mediated synaptic transmission between leech heart interneurons. J Neurophysiol 77: 1779-1794, 1997.
31. Nässel DR, Homberg U. Neuropeptides in interneurons of the insect brain. Cell Tissue Res 326: 1-24, 2006.
32. Olsen SR, Bhandawat V, Wilson RI. Excitatory interactions between olfactory processing channels in the Drosophila antennal lobe. Neuron 54: 89-103, 2007. (Pubitemid 46498691)
33. Olsen SR, Wilson RI. Lateral presynaptic inhibition mediates gain control in an olfactory circuit. Nature 452: 956-960, 2008. (Pubitemid 351589620)
34. Pearson HA, Lees G, Wray D. Calcium-channel currents in neurons from locust (Schistocerca gregaria) thoracic ganglia. J Exp Biol 177: 201-221, 1993.
35. Root CM, Semmelhack JL, Wong AM, Flores J, Wang JW. Propagation of olfactory information in Drosophila. Proc Natl Acad Sci USA 104: 11826-11831, 2007.
36. Sachse S, Galizia CG. Role of inhibition for temporal and spatial odor representation in olfactory output neurons: a calcium imaging study. J Neurophysiol 87: 1106-1117, 2002. (Pubitemid 34670872)
37. Saito M, Wu CF. Expression of ion channels and mutational effects in giant Drosophila neurons differentiated from cell division-arrested embryonic neuroblasts. J Neurosci 11: 2135-2150, 1991.
38. Schachtner J, Schmidt M, Homberg U. Organization and evolutionary trends of primary olfactory brain centers in Tetraconata (Crustacea plus Hexapoda). Arthropod Struct Dev 34: 257-299, 2005. (Pubitemid 41253545)
39. Schäfer S, Rosenboom H, Menzel R. Ionic currents of Kenyon cells from the mushroom body of the honeybee. J Neurosci 14: 4600-4612, 1994. (Pubitemid 24237886)
40. Shang Y, Claridge-Chang A, Sjulson L, Pypaert M, Miesenbock G. Excitatory local circuits and their implications for olfactory processing in the fly antennal lobe. Cell 128: 601-612, 2007. (Pubitemid 46198891)
41. Silbering AF, Galizia CG. Processing of odor mixtures in the Drosophila antennal lobe reveals both global inhibition and glomerulus-specific interactions. J Neurosci 27: 11966-11977, 2007.
42. Stopfer M, Bhagavan S, Smith BH, Laurent G. Impaired odour discrimination on desynchronization of odour-encoding neural assemblies. Nature 390: 70-74, 1997. (Pubitemid 27494757)
43. Strausfeld NJ, Hildebrand JG. Olfactory systems: common design, uncommon origins? Curr Opin Neurobiol 9: 634-639, 1999.
44. Tanaka NK, Ito K, Stopfer M. Odor-evoked neural oscillations in Drosophila are mediated by widely branching interneurons. J Neurosci 29: 8595-8603, 2009.
45. Triggle DJ. L-type calcium channels. Curr Pharm Des 12: 443-457, 2006.
46. Vosshall LB, Stocker RE. Molecular architecture of smell and taste in Drosophila. Annu Rev Neurosci 30: 505-533, 2007.
47. 2+ currents in cockroach neurones: properties and modulation by neurohormone D. Neuroreport 5: 1023-1026, 1994.
48. 2+ currents in central insect neurons: electrophysiological and pharmacological properties. J Neurophysiol 77: 186-199, 1997.
49. Wilson RI. Neural and behavioral mechanisms of olfactory perception. Curr Opin Neurobiol 18: 408-412, 2008.
50. Wilson RI, Laurent G. Role of GABAergic inhibition in shaping odor-evoked spatiotemporal patterns in the Drosophila antennal lobe. J Neurosci 25: 9069-9079, 2005. (Pubitemid 41500816)
51. Wilson RI, Mainen ZF. Early events in olfactory processing. Annu Rev Neurosci 29: 163-201, 2006.
52. Wilson RI, Turner GC, Laurent G. Transformation of olfactory representations in the Drosophila antennal lobe. Science 303: 366-370, 2004. (Pubitemid 38095775)