A population of glomerular glutamatergic neurons controls sensory information transfer in the mouse olfactory bulb

Nature Communications

Volumn 5, Issue , 2014, Pages

  Tatti, Roberta ^a   Bhaukaurally, Khaleel ^a   Gschwend, Olivier ^a   Seal, Rebecca P ^b   Edwards, Robert H ^c   Rodriguez, Ivan ^a   Carleton, Alan ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VESICULAR GLUTAMATE TRANSPORTER 3; 4 AMINOBUTYRIC ACID RECEPTOR; AMINO ACID TRANSPORTER; VESICULAR GLUTAMATE TRANSPORTER 3, MOUSE;

NEUROLOGY; OLFACTION; PHYSIOLOGY; RODENT; TRANSFER FUNCTION;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MOUSE; MULTIPHOTON MICROSCOPY; NERVE CELL STIMULATION; NONHUMAN; ODOR; OLFACTORY BULB; OPTOGENETICS; PERIPHERAL NERVOUS SYSTEM FUNCTION; PHOTOSTIMULATION; SENSORY NERVE CELL; SENSORY SYSTEM ELECTROPHYSIOLOGY; SEROTONINERGIC TRANSMISSION; SMELLING; SYNAPSE; ANIMAL; C57BL MOUSE; ELECTROPHYSIOLOGY; OLFACTORY SYSTEM; PHYSIOLOGY; SENSATION; TRANSGENIC MOUSE;

AMINO ACID TRANSPORT SYSTEMS, ACIDIC; ANIMALS; ELECTROPHYSIOLOGICAL PHENOMENA; GABAERGIC NEURONS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; ODORS; OLFACTORY BULB; OLFACTORY PATHWAYS; OLFACTORY PERCEPTION; SENSATION; SENSORY RECEPTOR CELLS;

EID: 84900023366     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms4791     Document Type: Article

References (68)

1. Ressler, K. J., Sullivan, S. L. & Buck, L. B. Information coding in the olfactory system: Evidence for a stereotyped and highly organized epitope map in the olfactory bulb. Cell 79, 1245-1255 (1994).
2. Vassar, R. et al. Topographic organization of sensory projections to the olfactory bulb. Cell 79, 981-991 (1994).
3. De Saint Jan, D., Hirnet, D., Westbrook, G. L. & Charpak, S. External tufted cells drive the output of olfactory bulb glomeruli. J. Neurosci. 29, 2043-2052 (2009).
4. Gire, D. H. & Schoppa, N. E. Control of on/off glomerular signaling by a local GABAergic microcircuit in the olfactory bulb. J. Neurosci. 29, 13454-13464 (2009).
5. Najac, M., De Saint Jan, D., Reguero, L., Grandes, P. & Charpak, S. Monosynaptic and polysynaptic feed-forward inputs to mitral cells from olfactory sensory neurons. J. Neurosci. 31, 8722-8729 (2011).
6. Gire, D. H. et al. Mitral cells in the olfactory bulb are mainly excited through a multistep signaling path. J. Neurosci. 32, 2964-2975 (2012).
7. Bellocchio, E. E., Reimer, R. J., Fremeau, Jr R. T. & Edwards, R. H. Uptake of glutamate into synaptic vesicles by an inorganic phosphate transporter. Science 289, 957-960 (2000).
8. Takamori, S., Rhee, J. S., Rosenmund, C. & Jahn, R. Identification of a vesicular glutamate transporter that defines a glutamatergic phenotype in neurons. Nature 407, 189-194 (2000).
9. Aihara, Y. et al. Molecular cloning of a novel brain-type Na()-dependent inorganic phosphate cotransporter. J. Neurochem. 74, 2622-2625 (2000).
10. Bai, L., Xu, H., Collins, J. F. & Ghishan, F. K. Molecular and functional analysis of a novel neuronal vesicular glutamate transporter. J. Biol. Chem. 276, 36764-36769 (2001).
11. Fremeau, Jr R. T. et al. The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron 31, 247-260 (2001).
12. Herzog, E. et al. The existence of a second vesicular glutamate transporter specifies subpopulations of glutamatergic neurons. J. Neurosci. 21, art. no.-RC181 (2001).
13. Fremeau, Jr R. T. et al. The identification of vesicular glutamate transporter 3 suggests novel modes of signaling by glutamate. Proc. Natl Acad. Sci. USA 99, 14488-14493 (2002).
14. Gras, C. et al. A third vesicular glutamate transporter expressed by cholinergic and serotoninergic neurons. J. Neurosci. 22, 5442-5451 (2002).
15. Schafer, M. K., Varoqui, H., Defamie, N., Weihe, E. & Erickson, J. D. Molecular cloning and functional identification of mouse vesicular glutamate transporter 3 and its expression in subsets of novel excitatory neurons. J. Biol. Chem. 277, 50734-50748 (2002).
16. Takamori, S., Malherbe, P., Broger, C. & Jahn, R. Molecular cloning and functional characterization of human vesicular glutamate transporter 3. EMBO Rep. 3, 798-803 (2002).
17. Nakamura, K., Hioki, H., Fujiyama, F. & Kaneko, T. Postnatal changes of vesicular glutamate transporter (VGluT)1 and VGluT2 immunoreactivities and their colocalization in the mouse forebrain. J. Comp. Neurol. 492, 263-288 (2005).
18. Ohmomo, H. et al. Postnatal changes in expression of vesicular glutamate transporters in the main olfactory bulb of the rat. Neuroscience 160, 419-426 (2009).
19. Gabellec, M. M., Panzanelli, P., Sassoe-Pognetto, M. & Lledo, P. M. Synapse-specific localization of vesicular glutamate transporters in the rat olfactory bulb. Eur. J. Neurosci. 25, 1373-1383 (2007).
20. Kosaka, T. & Kosaka, K. Heterogeneity of calbindin-containing neurons in the mouse main olfactory bulb: I. General description. Neurosci. Res. 67, 275-292 (2010).
21. Kosaka, K. & Kosaka, T. Chemical properties of type 1 and type 2 periglomerular cells in the mouse olfactory bulb are different from those in the rat olfactory bulb. Brain Res. 1167, 42-55 (2007).
22. Hayar, A., Karnup, S., Shipley, M. T. & Ennis, M. Olfactory bulb glomeruli: External tufted cells intrinsically burst at theta frequency and are entrained by patterned olfactory input. J. Neurosci. 24, 1190-1199 (2004).
23. Liu, S. & Shipley, M. T. Multiple conductances cooperatively regulate spontaneous bursting in mouse olfactory bulb external tufted cells. J. Neurosci. 28, 1625-1639 (2008).
24. Hayar, A., Karnup, S., Ennis, M. & Shipley, M. T. External tufted cells: A major excitatory element that coordinates glomerular activity. J. Neurosci. 24, 6676-6685 (2004).
25. Hayar, A., Shipley, M. T. & Ennis, M. Olfactory bulb external tufted cells are synchronized by multiple intraglomerular mechanisms. J. Neurosci. 25, 8197-8208 (2005).
26. McQuiston, A. R. & Katz, L. C. Electrophysiology of interneurons in the glomerular layer of the rat olfactory bulb. J. Neurophysiol. 86, 1899-1907 (2001).
27. Antal, M., Eyre, M., Finklea, B. & Nusser, Z. External tufted cells in the main olfactory bulb form two distinct subpopulations. Eur. J. Neurosci. 24, 1124-1136 (2006).
28. Macrides, F. & Schneider, S. P. Laminar organization of mitral and tufted cells in the main olfactory bulb of the adult hamster. J. Comp. Neurol. 208, 419-430 (1982).
29. Liu, S., Aungst, J. L., Puche, A. C. & Shipley, M. T. Serotonin modulates the population activity profile of olfactory bulb external tufted cells. J. Neurophysiol. 107, 473-483 (2012).
30. Hsia, A. Y., Vincent, J. D. & Lledo, P. M. Dopamine depresses synaptic inputs into the olfactory bulb. J. Neurophysiol. 82, 1082-1085 (1999).
31. Wachowiak, M. et al. Inhibition [corrected] of olfactory receptor neuron input to olfactory bulb glomeruli mediated by suppression of presynaptic calcium influx. J. Neurophysiol. 94, 2700-2712 (2005).
32. Nickell, W. T., Behbehani, M. M. & Shipley, M. T. Evidence for GABABmediated inhibition of transmission from the olfactory nerve to mitral cells in the rat olfactory bulb. Brain Res. Bull. 35, 119-123 (1994).
33. Bathellier, B., Buhl, D. L., Accolla, R. & Carleton, A. Dynamic ensemble odour coding in the mammalian olfactory bulb: Sensory information at different timescales. Neuron 57, 586-598 (2008).
34. Gschwend, O., Beroud, J. & Carleton, A. Encoding odorant identity by spiking packets of rate-invariant neurons in awake mice. PLoS ONE 7, e30155 (2012).
35. Patterson, M. A., Lagier, S. & Carleton, A. Odor representations in the olfactory bulb evolve after the first breath and persist as an odor afterimage. Proc. Natl Acad. Sci. USA 110, E3340-E3349 (2013).
36. Fremeau, Jr R. T. et al. Vesicular glutamate transporters 1 and 2 target to functionally distinct synaptic release sites. Science 304, 1815-1819 (2004).
37. Mendez, J. A. et al. Developmental and target-dependent regulation of vesicular glutamate transporter expression by dopamine neurons. J. Neurosci. 28, 6309-6318 (2008).
38. Noh, J., Seal, R. P., Garver, J. A., Edwards, R. H. & Kandler, K. Glutamate co-release at GABA/glycinergic synapses is crucial for the refinement of an inhibitory map. Nat. Neurosci. 13, 232-238 (2010).
39. Brill, M. S. et al. Adult generation of glutamatergic olfactory bulb interneurons. Nat. Neurosci. 12, 1524-1533 (2009).
40. Carleton, A., Petreanu, L. T., Lansford, R., Alvarez-Buylla, A. & Lledo, P. M. Becoming a new neuron in the adult olfactory bulb. Nat. Neurosci. 6, 507-518 (2003).
41. Carleton, A. et al. Making scents of olfactory neurogenesis. J. Physiol. Paris 96, 115-122 (2002).
42. Winpenny, E. et al. Sequential generation of olfactory bulb glutamatergic neurons by Neurog2-expressing precursor cells. Neural. Develop. 6, 12 (2011).
43. El Mestikawy, S., Wallen-Mackenzie, A., Fortin, G. M., Descarries, L. & Trudeau, L. E. From glutamate co-release to vesicular synergy: Vesicular glutamate transporters. Nat. Rev. Neurosci. 12, 204-216 (2011).
44. Boulland, J. L. et al. Expression of the vesicular glutamate transporters during development indicates the widespread corelease of multiple neurotransmitters. J. Comp. Neurol. 480, 264-280 (2004).
45. Somogyi, J. et al. GABAergic basket cells expressing cholecystokinin contain vesicular glutamate transporter type 3 (VGLUT3) in their synaptic terminals in hippocampus and isocortex of the rat. Eur. J. Neurosci. 19, 552-569 (2004).
46. Shutoh, F., Ina, A., Yoshida, S., Konno, J. & Hisano, S. Two distinct subtypes of serotonergic fibers classified by co-expression with vesicular glutamate transporter 3 in rat forebrain. Neurosci. Lett. 432, 132-136 (2008).
47. Kao, Y. H. et al. Evidence that certain retinal bipolar cells use both glutamate and GABA. J. Comp. Neurol. 478, 207-218 (2004).
48. Kato, H. K., Gillet, S. N., Peters, A. J., Isaacson, J. S. & Komiyama, T. Parvalbumin-expressing interneurons linearly control olfactory bulb output. Neuron 80, 1218-1231 (2013).
49. Miyamichi, K. et al. Dissecting local circuits: Parvalbumin interneurons underlie broad feedback control of olfactory bulb output. Neuron 80, 1232-1245 (2013).
50. Fukunaga, I., Berning, M., Kollo, M., Schmaltz, A. & Schaefer, A. T. Two distinct channels of olfactory bulb output. Neuron 75, 320-329 (2012).
51. Igarashi, K. M. et al. Parallel mitral and tufted cell pathways route distinct odor information to different targets in the olfactory cortex. J. Neurosci. 32, 7970-7985 (2012).
52. Petzold, G. C., Hagiwara, A. & Murthy, V. N. Serotonergic modulation of odor input to the mammalian olfactory bulb. Nat. Neurosci. 12, 784-791 (2009).
53. Grimes, W. N., Seal, R. P., Oesch, N., Edwards, R. H. & Diamond, J. S. Genetic targeting and physiological features of VGLUT3 amacrine cells. Vis. Neurosci. 28, 381-392 (2011).
54. Madisen, L. et al. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci. 13, 133-140 (2010).
55. Madisen, L. et al. A toolbox of Cre-dependent optogenetic transgenic mice for light-induced activation and silencing. Nat. Neurosci. 15, 793-802 (2012).
56. Zariwala, H. A. et al. A Cre-dependent GCaMP3 reporter mouse for neuronal imaging in vivo. J. Neurosci. 32, 3131-3141 (2012).
57. Tamamaki, N. et al. Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J. Comp. Neurol. 467, 60-79 (2003).
58. Castillo, P. E., Carleton, A., Vincent, J. D. & Lledo, P. M. Multiple and opposing roles of cholinergic transmission in the main olfactory bulb. J. Neurosci. 19, 9180-9191 (1999).
59. Didier, A. et al. A dendrodendritic reciprocal synapse provides a recurrent excitatory connection in the olfactory bulb. Proc. Natl Acad. Sci. USA 98, 6441-6446 (2001).
60. Bathellier, B., Van De Ville, D., Blu, T., Unser, M. & Carleton, A. Wavelet-based multi-resolution statistics for optical imaging signals: Application to automated detection of odour activated glomeruli in the mouse olfactory bulb. Neuroimage 34, 1020-1035 (2007).
61. Pologruto, T. A., Sabatini, B. L. & Svoboda, K. ScanImage: Flexible software for operating laser scanning microscopes. Biomed. Eng. Online 2, 13 (2003).
62. Vincis, R., Gschwend, O., Bhaukaurally, K., Beroud, J. & Carleton, A. Dense representation of natural odorants in the mouse olfactory bulb. Nat. Neurosci. 15, 537-539 (2012).
63. Rinberg, D., Koulakov, A. & Gelperin, A. Sparse odour coding in awake behaving mice. J. Neurosci. 26, 8857-8865 (2006).
64. Fantana, A. L., Soucy, E. R. & Meister, M. Rat olfactory bulb mitral cells receive sparse glomerular inputs. Neuron 59, 802-814 (2008).
65. Cury, K. M. & Uchida, N. Robust odor coding via inhalation-coupled transient activity in the mammalian olfactory bulb. Neuron 68, 570-585 (2010).
66. Shusterman, R., Smear, M. C., Koulakov, A. A. & Rinberg, D. Precise olfactory responses tile the sniff cycle. Nat. Neurosci. 14, 1039-1044 (2011).
67. Harris, K. D., Henze, D. A., Csicsvari, J., Hirase, H. & Buzsaki, G. Accuracy of tetrode spike separation as determined by simultaneous intracellular and extracellular measurements. J. Neurophysiol. 84, 401-414 (2000).
68. Hazan, L., Zugaro, M. & Buzsaki, G. Klusters, NeuroScope, NDManager: A free software suite for neurophysiological data processing and visualization. J. Neurosci. Methods. 155, 207-216 (2006).