Functional imaging of cortical feedback projections to the olfactory bulb

Frontiers in Neural Circuits

Volumn 8, Issue JULY, 2014, Pages

  Rothermel, Markus ^a   Wachowiak, Matt ^a  

^a The Brain Institute at the University of Utah   (United States)

Author keywords

Anterior olfactory nucleus; Centrifugal systems; GCaMP; In vivo; Olfactory bulb

Indexed keywords

CALCIUM; CRE RECOMBINASE; VIRUS VECTOR; BUNGAROTOXIN RECEPTOR; CALMODULIN; CHRNA7 PROTEIN, MOUSE; GREEN FLUORESCENT PROTEIN; OLFACTORY MARKER PROTEIN; OMP PROTEIN, MOUSE;

ANESTHESIA; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BIOSENSOR; BRAIN CORTEX; CONTROLLED STUDY; FEEDBACK SYSTEM; FEMALE; FLUORESCENCE IMAGING; FOREBRAIN; FUNCTIONAL NEUROIMAGING; IN VIVO STUDY; MALE; MOUSE; NERVE CELL INHIBITION; NERVE CELL STIMULATION; NERVE ENDING; NEUROMODULATION; NONHUMAN; ODOR; OLFACTORY BULB; OLFACTORY NUCLEUS; STATE DEPENDENT LEARNING; STIMULUS RESPONSE; WAKEFULNESS; ADMINISTRATION AND DOSAGE; ANIMAL; CYTOLOGY; ELECTROSTIMULATION; GENE TRANSFER; GENE VECTOR; GENETICS; HEMISPHERIC DOMINANCE; METABOLISM; NEWBORN; OLFACTORY SYSTEM; OPTOGENETICS; PHYSIOLOGY; REACTION TIME; SENSORY NERVE CELL; TRANSGENIC MOUSE;

ALPHA7 NICOTINIC ACETYLCHOLINE RECEPTOR; ANIMALS; ANIMALS, NEWBORN; CALMODULIN; CEREBRAL CORTEX; ELECTRIC STIMULATION; FEEDBACK, PHYSIOLOGICAL; FUNCTIONAL LATERALITY; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; GREEN FLUORESCENT PROTEINS; MICE; MICE, TRANSGENIC; ODORS; OLFACTORY BULB; OLFACTORY MARKER PROTEIN; OLFACTORY PATHWAYS; OPTOGENETICS; REACTION TIME; SENSORY RECEPTOR CELLS;

EID: 84903788528     PISSN: 16625110     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncir.2014.00073     Document Type: Article

References (112)

1. Abraham, N. M., Vincis, R., Lagier, S., Rodriguez, I., Carleton, A., and Eichenbaum, H. (2014). Long term functional plasticity of sensory inputs mediated by olfactory learning. Elife 3:e02109. doi: 10.7554/elife.02109
2. Atasoy, D., Aponte, Y., Su, H. H., and Sternson, S. M. (2008). A FLEX switch targets Channelrhodopsin-2 to multiple cell types for imaging and long-range circuit mapping. J. Neurosci. 28, 7025-7030. doi: 10.1523/JNEUROSCI.1954-08.2008
3. Bathellier, B., Buhl, D. L., Accolla, R., and Carleton, A. (2008). Dynamic ensemble odor coding in the mammalian olfactory bulb: sensory information at different timescales. Neuron 57, 586-598. doi: 10.1016/j.neuron.2008.02.011
4. Betley, J. N., and Sternson, S. M. (2011). Adeno-associated viral vectors for mapping, monitoring and manipulating neural circuits. Hum. Gene Ther. 22, 669-677. doi: 10.1089/hum.2010.204
5. Boyd, A. M., Sturgill, J. F., Poo, C., and Isaacson, J. S. (2012). Cortical feedback control of olfactory bulb circuits. Neuron 76, 1161-1174. doi: 10.1016/j.neuron.2012.10.020
6. Bozza, T., Mcgann, J. P., Mombaerts, P., and Wachowiak, M. (2004). In vivo imaging of neuronal activity by targeted expression of a genetically encoded probe in the mouse. Neuron 42, 9-21. doi: 10.1016/S0896-6273(04)00144-8
7. Broadwell, R. D., and Jacobowitz, D. M. (1976). Olfactory relationships of the telencephalon and diencephalon in the rabbit. III. The ipsilateral centrifugal fibers to the olfactory bulbar and retrobulbar formations. J. Comp. Neurol. 170, 321-345. doi: 10.1002/cne.901700305
8. Brunjes, P. C., Illig, K. R., and Meyer, E. A. (2005). A field guide to the anterior olfactory nucleus (cortex). Brain Res. Brain Res. Rev. 50, 305-335. doi: 10.1016/j.brainresrev.2005.08.005
9. Brunjes, P. C., and Kenerson, M. C. (2010). The anterior olfactory nucleus: quantitative study of dendritic morphology. J. Comp. Neurol. 518, 1603-1616. doi: 10.1002/cne.22293
10. Burton, S. D., and Urban, N. N. (2014). Greater excitability and firing irregularity of tufted cells underlies distinct afferent-evoked activity of olfactory bulb mitral and tufted cells. J. Physiol. 592(Pt. 10), 2097-2118. doi: 10.1113/jphysiol.2013.269886
11. Canteras, N. S., Simerly, R. B., and Swanson, L. W. (1995). Organization of projections from the medial nucleus of the amygdala: a PHAL study in the rat. J. Comp. Neurol. 360, 213-245. doi: 10.1002/cne.903600203
12. Carey, R. M., Verhagen, J. V., Wesson, D. W., Pirez, N., and Wachowiak, M. (2009). Temporal structure of receptor neuron input to the olfactory bulb imaged in behaving rats. J. Neurophysiol. 101, 1073-1088. doi: 10.1152/jn.90902.2008
13. Carey, R. M., and Wachowiak, M. (2011). Effect of sniffing on the temporal structure of mitral/tufted cell output from the olfactory bulb. J. Neurosci. 31, 10615-10626. doi: 10.1523/JNEUROSCI.1805-11.2011
14. Carnes, K. M., Fuller, T. A., and Price, J. L. (1990). Sources of presumptive glutamatergic/aspartatergic afferents to the magnocellular basal forebrain in the rat. J. Comp. Neurol. 302, 824-852. doi: 10.1002/cne.903020413
15. Carson, K. A. (1984). Quantitative localization of neurons projecting to the mouse main olfactory bulb. Brain Res. Bull. 12, 629-634. doi: 10.1016/0361-9230(84)90143-6
16. Chaput, M. A. (1986). Respiratory-phase-related coding of olfactory information in the olfactory bulb of awake freely-breathing rabbits. Physiol. Behav. 36, 319-324. doi: 10.1016/0031-9384(86)90023-5
17. Chen, T.-W., Wardill, T. J., Sun, Y., Pulver, S. R., Renninger, S. L., Baohan, A., et al. (2013). Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499, 295-300. doi: 10.1038/nature12354
18. Cury, K. M., and Uchida, N. (2010). Robust odor coding via inhalation-coupled transient activity in the mammalian olfactory bulb. Neuron 68, 570-585. doi: 10.1016/j.neuron.2010.09.040
19. Davis, B. J., and Macrides, F. (1981). The organization of centrifugal projections from the anterior olfactory nucleus, ventral hippocampal rudiment and piriform cortex to the main olfactory bulb in the hamster: an autoradiographic study. J. Comp. Neurol. 203, 475-493. doi: 10.1002/cne.902030310
20. Davis, B. J., Macrides, F., Youngs, W. M., Schneider, S. P., and Rosene, D. L. (1978). Efferents and centrifugal afferents of the main and accessory olfactory bulbs in the hamster. Brain Res. Bull. 3, 59-72. doi: 10.1016/0361-9230(78)90062-x
21. De Carlos, J. A., Lopez-Mascaraque, L., and Valverde, F. (1989). Connections of the olfactory bulb and nucleus olfactorius anterior in the hedgehog (Erinaceus europaeus): fluorescent tracers and HRP study. J. Comp. Neurol. 279, 601-618. doi: 10.1002/cne.902790408
22. de Olmos, J., Hardy, H., and Heimer, L. (1978). The afferent connections of the main and the accessory olfactory bulb formations in the rat: an experimental HRP-study. J. Comp. Neurol. 181, 213-244. doi: 10.1002/cne.901810202
23. Dominguez del Toro, E., Juiz, J. M., Peng, X., Lindstrom, J., and Criado, M. (1994). Immunocytochemical localization of the alpha 7 subunit of the nicotinic acetylcholine receptor in the rat central nervous system. J. Comp. Neurol. 349, 325-342. doi: 10.1002/cne.903490302
24. Doucette, W., and Restrepo, D. (2008). Profound context-dependent plasticity of mitral cell responses in olfactory bulb. PLoS Biol. 6:e258. doi: 10.1371/journal.pbio.0060258
25. Ezeh, P. I., Wellis, D. P., and Scott, J. W. (1993). Organization of inhibition in the rat olfactory bulb external plexiform layer. J. Neurophysiol. 70, 263-274.
26. Fu, Y., Tucciarone, J. M., Espinosa, J. S., Sheng, N., Darcy, D. P., Nicoll, R. A., et al. (2014). A cortical circuit for gain control by behavioral state. Cell 156, 1139-1152. doi: 10.1016/j.cell.2014.01.050
27. Gahring, L. C., Enioutina, E. Y., Myers, E. J., Spangrude, G. J., Efimova, O. V., Kelley, T. W., et al. (2013). Nicotinic receptor alpha7 expression identifies a novel hematopoietic progenitor lineage. PLoS One 8:e57481. doi: 10.1371/journal.pone.0057481
28. Gaykema, R. P., Luiten, P. G., Nyakas, C., and Traber, J. (1990). Cortical projection patterns of the medial septum-diagonal band complex. J. Comp. Neurol. 293, 103-124. doi: 10.1002/cne.902930109
29. Ghosh, S., Larson, S. D., Hefzi, H., Marnoy, Z., Cutforth, T., Dokka, K., et al. (2011). Sensory maps in the olfactory cortex defined by long-range viral tracing of single neurons. Nature 472, 217-220. doi: 10.1038/nature09945
30. Glickfeld, L. L., Andermann, M. L., Bonin, V., and Reid, R. C. (2013). Cortico-cortical projections in mouse visual cortex are functionally target specific. Nat. Neurosci. 16, 219-226. doi: 10.1038/nn.3300
31. Gomez, D. M., and Newman, S. W. (1992). Differential projections of the anterior and posterior regions of the medial amygdaloid nucleus in the Syrian hamster. J. Comp. Neurol. 317, 195-218. doi: 10.1002/cne.903170208
32. Gong, S., Zheng, C., Doughty, M. L., Losos, K., Didkovsky, N., Schambra, U. B., et al. (2003). A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature 425, 917-925. doi: 10.1038/nature02033
33. Griff, E. R., Mafhouz, M., and Chaput, M. A. (2008). Comparison of identified mitral and tufted cells in freely breathing rats: II. Odor-evoked responses. Chem. Senses 33, 793-802. doi: 10.1093/chemse/bjn040
34. Grosmaitre, X., Santarelli, L. C., Tan, J., Luo, M., and Ma, M. (2007). Dual functions of mammalian olfactory sensory neurons as odor detectors and mechanical sensors. Nat. Neurosci. 10, 348-354. doi: 10.1038/nn1856
35. Haberly, L. B. (2001). Parallel-distributed processing in olfactory cortex: new insights from morphological and physiological analysis of neuronal circuitry. Chem. Senses 26, 551-576. doi: 10.1093/chemse/26.5.551
36. Haberly, L. B., and Price, J. L. (1977). The axonal projection patterns of the mitral and tufted cells of the olfactory bulb in the rat. Brain Res. 129, 152-157. doi: 10.1016/0006-8993(77)90978-7
37. Haberly, L. B., and Price, J. L. (1978). Association and commissural fiber systems of the olfactory cortex of the rat. J. Comp. Neurol. 178, 711-740. doi: 10.1002/cne.901780408
38. Hagiwara, A., Pal, S. K., Sato, T. F., Wienisch, M., and Murthy, V. N. (2012). Optophysiological analysis of associational circuits in the olfactory cortex. Front. Neural Circuits 6:18. doi: 10.3389/fncir.2012.00018
39. Ichikawa, T., and Hirata, Y. (1986). Organization of choline acetyltransferase-containing structures in the forebrain of the rat. J. Neurosci. 6, 281-292.
40. Illig, K. R., and Eudy, J. D. (2009). Contralateral projections of the rat anterior olfactory nucleus. J. Comp. Neurol. 512, 115-123. doi: 10.1002/cne.21900
41. Karpov, A. P. (1980). "Analysis of neuron activity in the rabbit's olfactory bulb during food-acquisition behavior, " in Neural Mechanisms of Goal-Directed Behavior and Learning, eds R. F. Thompson, L. H. Hicks and V. B. Shvyrkov (New York: Academic Press), 273-282.
42. Kass, M. D., Rosenthal, M. C., Pottackal, J., and Mcgann, J. P. (2013). Fear learning enhances neural responses to threat-predictive sensory stimuli. Science 342, 1389-1392. doi: 10.1126/science.1244916
43. Kato, H. K., Chu, M. W., Isaacson, J. S., and Komiyama, T. (2012). Dynamic sensory representations in the olfactory bulb: modulation by wakefulness and experience. Neuron 76, 962-975. doi: 10.1016/j.neuron.2012.09.037
44. Kay, R. B., and Brunjes, P. C. (2014). Diversity among principal and GABAergic neurons of the anterior olfactory nucleus. Front. Cell. Neurosci. 8:111. doi: 10.3389/fncel.2014.00111
45. Kay, L. M., and Laurent, G. (1999). Odor-and context-dependent modulation of mitral cell activity in behaving rats. Nat. Neurosci. 2, 1003-1009. doi: 10.1038/14801
46. Kay, R. B., Meyer, E. A., Illig, K. R., and Brunjes, P. C. (2011). Spatial distribution of neural activity in the anterior olfactory nucleus evoked by odor and electrical stimulation. J. Comp. Neurol. 519, 277-289. doi: 10.1002/cne.22519
47. Kikuta, S., Sato, K., Kashiwadani, H., Tsunoda, K., Yamasoba, T., and Mori, K. (2010). Neurons in the anterior olfactory nucleus pars externa detect right or left localization of odor sources. Proc. Natl. Acad. Sci. U S A 107, 12363-12368. doi: 10.1073/pnas.1003999107
48. Lei, H., Mooney, R., and Katz, L. C. (2006). Synaptic integration of olfactory information in mouse anterior olfactory nucleus. J. Neurosci. 26, 12023-12032. doi: 10.1523/jneurosci.2598-06.2006
49. Li, J., Ishii, T., Feinstein, P., and Mombaerts, P. (2004). Odorant receptor gene choice is reset by nuclear transfer from mouse olfactory sensory neurons. Nature 428, 393-399. doi: 10.1038/nature02433
50. Linster, C., Wyble, B. P., and Hasselmo, M. E. (1999). Electrical stimulation of the horizontal limb of the diagonal band of broca modulates population EPSPs in piriform cortex. J. Neurophysiol. 81, 2737-2742.
51. Luiten, P. G., Gaykema, R. P., Traber, J., and Spencer, D. G. Jr. (1987). Cortical projection patterns of magnocellular basal nucleus subdivisions as revealed by anterogradely transported Phaseolus vulgaris leucoagglutinin. Brain Res. 413, 229-250. doi: 10.1016/0006-8993(87)91014-6
52. Luskin, M. B., and Price, J. L. (1983). The topographic organization of associational fibers of the olfactory system in the rat, including centrifugal fibers to the olfactory bulb. J. Comp. Neurol. 216, 264-291. doi: 10.1002/cne.902160305
53. Ma, L., Qiu, Q., Gradwohl, S., Scott, A., Yu, E. Q., Alexander, R., et al. (2012). Distributed representation of chemical features and tunotopic organization of glomeruli in the mouse olfactory bulb. Proc. Natl. Acad. Sci. U S A 109, 5481-5486. doi: 10.1073/pnas.1117491109
54. Macrides, F., Davis, B. J., Youngs, W. M., Nadi, N. S., and Margolis, F. L. (1981). Cholinergic and catecholaminergic afferents to the olfactory bulb in the hamster: a neuroanatomical, biochemical and histochemical investigation. J. Comp. Neurol. 203, 495-514. doi: 10.1002/cne.902030311
55. Macrides, F., and Schneider, S. P. (1982). Laminar organization of mitral and tufted cells in the main olfactory bulb of the adult hamster. J. Comp. Neurol. 208, 419-430. doi: 10.1002/cne.902080410
56. Markopoulos, F., Rokni, D., Gire, D. H., and Murthy, V. N. (2012). Functional properties of cortical feedback projections to the olfactory bulb. Neuron 76, 1175-1188. doi: 10.1016/j.neuron.2012.10.028
57. Matsutani, S. (2010). Trajectory and terminal distribution of single centrifugal axons from olfactory cortical areas in the rat olfactory bulb. Neuroscience 169, 436-448. doi: 10.1016/j.neuroscience.2010.05.001
58. Matsutani, S., and Yamamoto, N. (2008). Centrifugal innervation of the mammalian olfactory bulb. Anat. Sci. Int. 83, 218-227. doi: 10.1111/j.1447-073x.2007.00223.x
59. Mclean, J. H., and Shipley, M. T. (1987). Serotonergic afferents to the rat olfactory bulb: I. Origins and laminar specificity of serotonergic inputs in the adult rat. J. Neurosci. 7, 3016-3028.
60. McLean, J. H., Shipley, M. T., Nickell, W. T., Aston-Jones, G., and Reyher, C. K. (1989). Chemoanatomical organization of the noradrenergic input from locus coeruleus to the olfactory bulb of the adult rat. J. Comp. Neurol. 285, 339-349. doi: 10.1002/cne.902850305
61. Meyer, E. A., Illig, K. R., and Brunjes, P. C. (2006). Differences in chemo-and cytoarchitectural features within pars principalis of the rat anterior olfactory nucleus suggest functional specialization. J. Comp. Neurol. 498, 786-795. doi: 10.1002/cne.21077
62. Meyer, F., and Louilot, A. (2012). Early prefrontal functional blockade in rats results in schizophrenia-related anomalies in behavior and dopamine. Neuropsychopharmacology 37, 2233-2243. doi: 10.1038/npp.2012.74
63. Miyamichi, K., Amat, F., Moussavi, F., Wang, C., Wickersham, I., Wall, N. R., et al. (2011). Cortical representations of olfactory input by trans-synaptic tracing. Nature 472, 191-196. doi: 10.1038/nature09714
64. Nagayama, S., Enerva, A., Fletcher, M. L., Masurkar, A. V., Igarashi, K. M., Mori, K., et al. (2010). Differential axonal projection of mitral and tufted cells in the mouse main olfactory system. Front. Neural Circuits 4:120. doi: 10.3389/fncir.2010.00120
65. Nagayama, S., Takahashi, Y. K., Yoshihara, Y., and Mori, K. (2004). Mitral and tufted cells differ in the decoding manner of odor maps in the rat olfactory bulb. J. Neurophysiol. 91, 2532-2540. doi: 10.1152/jn.01266.2003
66. Niell, C. M., and Stryker, M. P. (2010). Modulation of visual responses by behavioral state in mouse visual cortex. Neuron 65, 472-479. doi: 10.1016/j.neuron.2010.01.033
67. Nunez-Parra, A., Li, A., and Restrepo, D. (2014). Coding odor identity and odor value in awake rodents. Prog. Brain Res. 208, 205-222. doi: 10.1016/b978-0-444-63350-7.00008-5
68. Nunez-Parra, A., Maurer, R. K., Krahe, K., Smith, R. S., and Araneda, R. C. (2013). Disruption of centrifugal inhibition to olfactory bulb granule cells impairs olfactory discrimination. Proc. Natl. Acad. Sci. U S A 110, 14777-14782. doi: 10.1073/pnas.1310686110
69. Ojima, H., Yamasaki, T., Kojima, H., and Akashi, A. (1988). Cholinergic innervation of the main and the accessory olfactory bulbs of the rat as revealed by a monoclonal antibody against choline acetyltransferase. Anat. Embryol. (Berl) 178, 481-488. doi: 10.1007/bf00305035
70. Paxinos, G., and Franklin, K. B. J. (2001). The Mouse Brain in Stereotaxic Coordinates. 2nd Edn. San Diego: Academic Press.
71. Petreanu, L., Gutnisky, D. A., Huber, D., Xu, N. L., O'connor, D. H., Tian, L., et al. (2012). Activity in motor-sensory projections reveals distributed coding in somatosensation. Nature 489, 299-303. doi: 10.1038/nature11321
72. Petrovich, G. D., Risold, P. Y., and Swanson, L. W. (1996). Organization of projections from the basomedial nucleus of the amygdala: a PHAL study in the rat. J. Comp. Neurol. 374, 387-420. doi: 10.1002/(sici)1096-9861(19961021)374:3<387::aid-cne6>3.0.co;2-y
73. Petzold, G. C., Hagiwara, A., and Murthy, V. N. (2009). Serotonergic modulation of odor input to the mammalian olfactory bulb. Nat. Neurosci. 12, 784-791. doi: 10.1038/nn.2335
74. Pologruto, T., Sabatini, B., and Svoboda, K. (2003). ScanImage: flexible software for operating laser scanning microscopes. Biomed. Eng. Online 2:13. doi: 10.1186/1475-925X-2-13
75. Price, J. L., and Powell, T. P. (1970). An experimental study of the origin and the course of the centrifugal fibres to the olfactory bulb in the rat. J. Anat. 107, 215-237.
76. Rabbitt, R. D., and Brownell, W. E. (2011). Efferent modulation of hair cell function. Curr. Opin. Otolaryngol. Head Neck Surg. 19, 376-381. doi: 10.1097/MOO.0b013e32834a5be1
77. Reyher, C. K., Schwerdtfeger, W. K., and Baumgarten, H. G. (1988). Interbulbar axonal collateralization and morphology of anterior olfactory nucleus neurons in the rat. Brain Res. Bull. 20, 549-566. doi: 10.1016/0361-9230(88)90214-6
78. Rogers, S. W., and Gahring, L. C. (2012). Nicotinic receptor Alpha7 expression during tooth morphogenesis reveals functional pleiotropy. PLoS One 7:e36467. doi: 10.1371/journal.pone.0036467
79. Rogers, S. W., Myers, E. J., and Gahring, L. C. (2012a). The expression of nicotinic receptor alpha7 during cochlear development. Brain Behav. 2, 628-639. doi: 10.1002/brb3.84
80. Rogers, S. W., Tvrdik, P., Capecchi, M. R., and Gahring, L. C. (2012b). Prenatal ablation of nicotinic receptor alpha7 cell lineages produces lumbosacral spina bifida the severity of which is modified by choline and nicotine exposure. Am. J. Med. Genet. A 158A, 1135-1144. doi: 10.1002/ajmg.a.35372
81. Rothermel, M., Brunert, D., Zabawa, C., Díaz-Quesada, M., and Wachowiak, M. (2013). Transgene expression in target-defined neuron populations mediated by retrograde infection with adeno-associated viral vectors. J. Neurosci. 33, 15195-15206. doi: 10.1523/JNEUROSCI.1618-13.2013
82. Rothermel, M., Carey, R. M., Puche, A., Shipley, M. T., and Wachowiak, M. (2014). Cholinergic inputs from basal forebrain add an excitatory bias to odor coding in the olfactory bulb. J. Neurosci. 34, 4654-4664. doi: 10.1523/JNEUROSCI.5026-13.2014
83. Schneider, S. P., and Scott, J. W. (1983). Orthodromic response properties of rat olfactory bulb mitral and tufted cells correlate with their projection patterns. J. Neurophysiol. 50, 358-378.
84. Schoenfeld, T. A., and Macrides, F. (1984). Topographic organization of connections between the main olfactory bulb and pars externa of the anterior olfactory nucleus in the hamster. J. Comp. Neurol. 227, 121-135. doi: 10.1002/cne.902270113
85. Schoenfeld, T. A., Marchand, J. E., and Macrides, F. (1985). Topographic organization of tufted cell axonal projections in the hamster main olfactory bulb: an intrabulbar associational system. J. Comp. Neurol. 235, 503-518. doi: 10.1002/cne.902350408
86. Scott, J. W. (1981). Electrophysiological identification of mitral and tufted cells and distributions of their axons in olfactory system of the rat. J. Neurophysiol. 46, 918-931.
87. Scott, J. W., Mcbride, R. L., and Schneider, S. P. (1980). The organization of projections from the olfactory bulb to the piriform cortex and olfactory tubercle in the rat. J. Comp. Neurol. 194, 519-534. doi: 10.1002/cne.901940304
88. Scott, J. W., Ranier, E. C., Pemberton, J. L., Orona, E., and Mouradian, L. E. (1985). Pattern of rat olfactory bulb mitral and tufted cell connections to the anterior olfactory nucleus pars externa. J. Comp. Neurol. 242, 415-424. doi: 10.1002/cne.902420309
89. Shea, S. D., Katz, L. C., and Mooney, R. (2008). Noradrenergic induction of odor-specific neural habituation and olfactory memories. J. Neurosci. 28, 10711-10719. doi: 10.1523/JNEUROSCI.3853-08.2008
90. Shipley, M. T., and Adamek, G. D. (1984). The connections of the mouse olfactory bulb: a study using orthograde and retrograde transport of wheat germ agglutinin conjugated to horseradish peroxidase. Brain Res. Bull. 12, 669-688. doi: 10.1016/0361-9230(84)90148-5
91. Shipley, M. T., Halloran, F. J., and de la Torre, J. (1985). Surprisingly rich projection from locus coeruleus to the olfactory bulb in the rat. Brain Res. 329, 294-299. doi: 10.1016/0006-8993(85)90537-2
92. Shusterman, R., Smear, M. C., Koulakov, A. A., and Rinberg, D. (2011). Precise olfactory responses tile the sniff cycle. Nat. Neurosci. 14, 1039-1044. doi: 10.1038/nn.2877
93. Soria-Gómez, E., Bellocchio, L., Reguero, L., Lepousez, G., Martin, C., Bendahmane, M., et al. (2014). The endocannabinoid system controls food intake via olfactory processes. Nat. Neurosci. 17, 407-415. doi: 10.1038/nn.3647
94. Sosulski, D. L., Lissitsyna Bloom, M., Cutforth, T., Axel, R., and Datta, S. R. (2011). Distinct representations of olfactory information in different cortical centres. Nature 472, 213-216. doi: 10.1038/nature09868
95. Soucy, E. R., Albeanu, D. F., Fantana, A. L., Murthy, V. N., and Meister, M. (2009). Precision and diversity in an odor map on the olfactory bulb. Nat. Neurosci. 12, 210-220. doi: 10.1038/nn.2262
96. Spors, H., Wachowiak, M., Cohen, L. B., and Friedrich, R. W. (2006). Temporal dynamics and latency patterns of receptor neuron input to the olfactory bulb. J. Neurosci. 26, 1247-1259. doi: 10.1523/jneurosci.3100-05.2006
97. Stratford, T. R., and Wirtshafter, D. (2012). Effects of muscimol, amphetamine and DAMGO injected into the nucleus accumbens shell on food-reinforced lever pressing by undeprived rats. Pharmacol. Biochem. Behav. 101, 499-503. doi: 10.1016/j.pbb.2012.02.010
98. Strowbridge, B. W. (2009). Role of cortical feedback in regulating inhibitory microcircuits. Ann. N Y Acad. Sci. 1170, 270-274. doi: 10.1111/j.1749-6632.2009.04018.x
99. Swanson, L. W., and Cowan, W. M. (1977). An autoradiographic study of the organization of the efferent connections of the hippocampal formation in the rat. J. Comp. Neurol. 172, 49-84. doi: 10.1002/cne.901720104
100. Tian, L., Hires, S. A., Mao, T., Huber, D., Chiappe, M. E., Chalasani, S. H., et al. (2009). Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat. Methods 6, 875-881. doi: 10.1038/nmeth.1398
101. Valverde, F., Lopez-Mascaraque, L., and De Carlos, J. A. (1989). Structure of the nucleus olfactorius anterior of the hedgehog (Erinaceus europaeus). J. Comp. Neurol. 279, 581-600. doi: 10.1002/cne.902790407
102. van Groen, T., and Wyss, J. M. (1990). Extrinsic projections from area CA1 of the rat hippocampus: olfactory, cortical, subcortical and bilateral hippocampal formation projections. J. Comp. Neurol. 302, 515-528. doi: 10.1002/cne.903020308
103. Verhagen, J. V., Wesson, D. W., Netoff, T. I., White, J. A., and Wachowiak, M. (2007). Sniffing controls an adaptive filter of sensory input to the olfactory bulb. Nat. Neurosci. 10, 631-639. doi: 10.1038/nn1892
104. Wachowiak, M., and Cohen, L. B. (2001). Representation of odorants by receptor neuron input to the mouse olfactory bulb. Neuron 32, 723-735. doi: 10.1016/s0896-6273(01)00506-2
105. Wachowiak, M., Economo, M. N., Díaz-Quesada, M., Brunert, D., Wesson, D. W., White, J. A., et al. (2013). Optical dissection of odor information processing in vivo using GCaMPs expressed in specified cell types of the olfactory bulb. J. Neurosci. 33, 5285-5300. doi: 10.1523/JNEUROSCI.4824-12.2013
106. Weeg, M. S., Land, B. R., and Bass, A. H. (2005). Vocal pathways modulate efferent neurons to the inner ear and lateral line. J. Neurosci. 25, 5967-5974. doi: 10.1523/jneurosci.0019-05.2005
107. Wesson, D. W., Carey, R. M., Verhagen, J. V., and Wachowiak, M. (2008). Rapid encoding and perception of novel odors in the rat. PLoS Biol. 6:e82. doi: 10.1371/journal.pbio.0060082
108. Woolf, N. J., Eckenstein, F., and Butcher, L. L. (1984). Cholinergic systems in the rat brain: I. projections to the limbic telencephalon. Brain Res. Bull. 13, 751-784. doi: 10.1016/0361-9230(84)90236-3
109. Yan, Z., Tan, J., Qin, C., Lu, Y., Ding, C., and Luo, M. (2008). Precise circuitry links bilaterally symmetric olfactory maps. Neuron 58, 613-624. doi: 10.1016/j.neuron.2008.03.012
110. Zaborszky, L., Van Den Pol, A. N., and Gyengesi, E. (2012). "The basal forebrain cholinergic projection system in mice, " in The Mouse Nervous System, eds C. Watson, G. Paxinos and L. Puelles (Amsterdam: Elsevier), 684-718.
111. Zariwala, H. A., Borghuis, B. G., Hoogland, T. M., Madisen, L., Tian, L., De Zeeuw, C. I., et al. (2012). A cre-dependent GCaMP3 reporter mouse for neuronal imaging in vivo. J. Neurosci. 32, 3131-3141. doi: 10.1523/JNEUROSCI.4469-11.2012
112. Zhuravin, I. A., and Bures, J. (1991). Extent of the tetrodotoxin induced blockade examined by pupillary paralysis elicited by intracerebral injection of the drug. Exp. Brain Res. 83, 687-690. doi: 10.1007/bf00229849