Spiking patterns and their functional implications in the antennal lobe of the tobacco hornworm Manduca sexta

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Lei, Hong ^a   Reisenman, Carolina E ^a   Wilson, Caroline H ^b   Gabbur, Prasad ^c   Hildebrand, John G ^a  

^a UNIVERSITY OF ARIZONA   (United States)

^b UNIVERSITY OF ALASKA ANCHORAGE   (United States)

^c University of Arizona   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANTENNA (ORGAN); ARTICLE; BRAIN FUNCTION; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; IN VIVO STUDY; INTERNEURON; MANDUCA SEXTA; NERVE CELL; NONHUMAN; ODOR; OLFACTORY BULB; OLFACTORY SYSTEM; SENSORY STIMULATION; SMELLING; SPIKE WAVE; ANIMAL; CYTOLOGY; DRUG EFFECT; FEMALE; LEPIDOPTERA; MALE; NEUROPIL; PHYSIOLOGY;

HEXAPODA; LEPIDOPTERA; MANDUCA SEXTA;

BICUCULLINE; BICUCULLINE METHIODIDE; DRUG DERIVATIVE;

ANIMALS; BICUCULLINE; FEMALE; INTERNEURONS; MALE; MANDUCA; NEUROPIL; ODORS;

EID: 80052302761     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0023382     Document Type: Article

References (48)

1. Krahe R, Gabbiani F, (2004) Burst firing in sensory systems. Nat Rev Neurosci 5: 1-11.
2. Bobkov YV, Ache BW, (2007) Intrinsically Bursting Olfactory Receptor Neurons. J Neurophysiol 97: 1052-1057.
3. Hayar A, Karnup S, Shipley MT, Ennis M, (2004) Olfactory bulb glomeruli: external tufted cells intrinsically burst at theta frequency and are entrained by patterned olfactory input. J Neurosci 24: 1190-1199.
4. Cang JH, Isaacson JS, (2003) In vivo whole-cell recording of odor-evoked synaptic transmission in the rat olfactory bulb. J Neurosci 23: 4108-4116.
5. MacLeod NK, (1976) Spontaneous activity of single neurons in the olfactory bulb of the rainbow trout (Salmo gairdneri) and its modulation by olfactory stimulation with amino acids. Exp Brain Res 25: 267-278.
6. Suzuki N, Bekkers JM, (2006) Neural Coding by Two Classes of Principal Cells in the Mouse Piriform Cortex. J Neurosci 26: 11938-11947.
7. Hamilton KA, Heinbockel T, Ennis M, Szabo G, Erdelyi F, et al. (2005) Properties of external plexiform layer interneurons in mouse olfactory bulb slices. Neuroscience 133: 819-829.
8. Hildebrand JG, Shepherd G, (1997) Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Ann Rev Neurosci 20: 595-631.
9. Rospars JP, Hildebrand JG, (1992) Anatomical identification of glomeruli in the antennal lobes of the male sphinx moth Manduca sexta. Cell Tissue Res 270: 205-227.
10. Christensen TA, Hildebrand JG, (1987) Male-specific, sex pheromone-selective projection neurons in the antennal lobes of the moth Manduca sexta. J Comp Physiol A 160: 553-569.
11. Ro H, Muller D, Mustaparta H, (2007) Anatomical organization of antennal lobe projection neurons in the moth Heliothis virescens. J Comp Neurol 500: 658-675.
12. Sadek MM, Hansson BS, Rospars JP, Anton S, (2002) Glomerular representation of plant volatiles and sex pheromone components in the antennal lobe of the female Spodoptera littoralis. J Exp Biol 205: 1363-1376.
13. Varela N, Avilla J, Gemeno C, Anton S, (2011) Ordinary glomeruli in the antennal lobe of male and female tortricid moth Grapholita molesta (Busck) (Lepidoptera: Tortricidae) process sex pheromone and host-plant volatiles. J Exp Biol 214: 637-645.
14. Kanzaki R, Arbas EA, Strausfeld NJ, Hildebrand JG, (1989) Physiology and morphology of projection neurons in the antennal lobe of the male moth Manduca sexta. J Comp Physiol A 165: 427-453.
15. Root CM, Semmelhack JL, Wong AM, Flores J, Wang JW, (2007) Propagation of olfactory information in Drosophila. Proc Natl Acad Sci 104: 11826-11831.
16. Christensen TA, Waldrop BR, Harrow ID, Hildebrand JG, (1993) Local interneurons and information-processing in the olfactory glomeruli of the moth Manduca sexta. J Comp Physiol A 173: 385-399.
17. Husch A, Paehler M, Fusca D, Paeger L, Kloppenburg P, (2009) Distinct Electrophysiological Properties in Subtypes of Nonspiking Olfactory Local Interneurons Correlate With Their Cell Type-Specific Ca2+ Current Profiles. J Neurophysiol 102: 2834-2845.
18. Seki Y, Rybak J, Wicher D, Sachse S, Hansson BS, (2010) Physiological and Morphological Characterization of Local Interneurons in the Drosophila Antennal Lobe. J Neurophysiol 104: 1007-1019.
19. Huang J, Zhang W, Qiao W, Hu A, Wang Z, (2010) Functional Connectivity and Selective Odor Responses of Excitatory Local Interneurons in Drosophila Antennal Lobe. Neuron 67: 1021-1033.
20. Chou YH, Spletter ML, Yaksi E, Leong JCS, Wilson RI, et al. (2010) Diversity and wiring variability of olfactory local interneurons in the Drosophila antennal lobe. Nat Neurosci 13: 439-449.
21. Starratt AN, Dahm KH, Allen N, Hildebrand JG, Payne TL, et al. (1979) Bombykal, a sex pheromone of the sphinx moth Manduca sexta. Zeitschrift fur Naturforschung C-A Journal of Biosciences 34: 9-12.
22. Christensen TA, Hildebrand JG, Tumlinson JH, Doolittle RE, (1989) Sex pheromone blend of Manduca sexta: responses of central olfactory interneurons to antennal stimulation in male moths. Arch Insect Biochem Physiol 10: 281-289.
23. Laurent G, Seymour-Laurent KJ, Johnson K, (1993) Dendritic excitability and a voltage-gated calcium current in locust nonspiking local interneurons. J Neurophysiol 69: 1484-1498.
24. Mercer AR, Hildebrand JG, (2002) Developmental Changes in the Electrophysiological Properties and Response Characteristics of Manduca Antennal-Lobe Neurons. J Neurophysiol 87: 2650-2663.
25. King JR, Christensen TA, Hildebrand JG, (2000) Response characteristics of an identified, sexually dimorphic olfactory glomerulus. J Neurosci 20: 2391-2399.
26. Pinault D, (1996) A novel single-cell staining procedure performed in vivo under electrophysiological control: morpho-functional features of juxtacellularly labeled thalamic cells and other central neurons with biocytin or Neurobiotin. J Neurosci Methods 65: 113-136.
27. Lei H, Riffell JA, Gage SL, Hildebrand JG, (2009) Contrast enhancement of stimulus intermittency in a primary olfactory network and its behavioral significance. Journal of Biology 8: 21.
28. Tumlinson JH, Brennan MM, Doolittle RE, Mitchell ER, Brabham A, et al. (1989) Identification of a pheromone blend attractive to Manduca sexta (L.) males in a wind tunnel. Arch Insect Biochem Physiol 10: 255-271.
29. Tumlinson JH, Mitchell ER, Doolittle RE, Jackson DM, (1994) Field-tests of synthetic Manduca sexta sex-pheromone. J Chem Ecol 20: 579-591.
30. Kaissling KE, Hildebrand JG, Tumlinson JH, (1989) Pheromone receptor cells in the male moth Manduca sexta. Arch Insect Biochem Physiol 10: 273-279.
31. Lei H, Christensen TA, Hildebrand JG, (2002) Local inhibition modulates odor-evoked synchronization of glomerulus-specific output neurons. Nat Neurosci 5: 557-565.
32. Heinbockel T, Christensen TA, Hildebrand JG, (1999) Temporal tuning of odor responses in pheromone-responsive projection neurons in the brain of the sphinx moth Manduca sexta. J Comp Neurol 409: 1-12.
33. Heinbockel T, Christensen TA, Hildebrand JG, (2004) Representation of binary pheromone blends by glomerulus-specific olfactory projection neurons. J Comp Physiol A 190: 1023-1037.
34. Christensen TA, Waldrop BR, Hildebrand JG, (1998) Multitasking in the olfactory system: context-dependent responses to odors reveal dual GABA-regulated coding mechanisms in single olfactory projection neurons. J Neurosci 18: 5999-6008.
35. Mwilaria EK, Ghatak C, Daly KC, (2008) Disruption of GABAA in the insect antennal lobe generally increases odor detection and discrimination thresholds. Chem Senses 33: 267-281.
36. Khawaled R, Bruening-Wright A, Adelman JP, Maylie J, (1999) Bicuculline block of small-conductance calcium-activated potassium channels. Pflügers Archiv Eur J Physiol 438: 314-321.
37. Shinomoto S, Shima K, Tanji J, (2003) Differences in Spiking Patterns Among Cortical Neurons. Neural Comput 15: 2823-2842.
38. Legendy CR, Salcman M, (1985) Bursts and recurrences of bursts in the spike trains of spontaneously active striate cortex neurons. J Neurophysiol 53: 926-939.
39. Selchow KI, (1998) Processing of plant-associated odors by a subset of projection neurons in the antennal lobe of the female moth, Manduca sexta [dissertation] University of Arizona.
40. Tripathy SJ, Staudacher EM, Peters OJ, Kalwar FR, Hatfield MN, et al. (2010) Odors pulsed at wing beat frequencies are tracked by primary olfactory networks and enhance odor detection. Front Cell Neurosci 4 doi:10.3389/neuro.03.001.2010.
41. Hansson BS, Anton S, Christensen TA, (1994) Structure and function of antennal lobe neurons in the male turnip moth, Agrotis segetum (Lepidoptera, Noctuidae). J Comp Physiol A 175: 547-562.
42. Sun XJ, Fonta C, Masson C, (1993) Odor quality processing by bee antennal lobe interneurons. Chem Senses 18: 355-377.
43. Husch A, Paehler M, Fusca D, Paeger L, Kloppenburg P, (2009) Calcium Current Diversity in Physiologically Different Local Interneuron Types of the Antennal Lobe. J Neurosci 29: 716-726.
44. Lisman JE, (1997) Bursts as a unit of neural information: making unreliable synapses reliable. Trends Neurosci 20: 38-43.
45. Ji H, Shepard PD, (2006) SK Ca2+-activated K+ channel ligands alter the firing pattern of dopamine-containing neurons in vivo. Neuroscience 140: 623-633.
46. Toporikova N, Chacron MJ, (2009) SK Channels Gate Information Processing In Vivo by Regulating an Intrinsic Bursting Mechanism Seen In Vitro. J Neurophysiol 102: 2273-2287.
47. Dolzer J, Karannich S, Fisher K, Stengl M, (2001) Oscillations of the transeptithelial potential of moth olfactory sensilla are influenced by octopamine and serotonin. J Exp Biol 204: 2781-2794.
48. Mercer AR, Hildebrand JG, (2002) Developmental changes in the density of ionic currents in antennal-lobe neurons of the sphinx moth, Manduca sexta. J Neurophysiol 87: 2664-2675.