Comparison of glomerular activity patterns by fMRI and wide-field calcium imaging: Implications for principles underlying odor mapping

NeuroImage

Volumn 126, Issue , 2016, Pages 208-218

  Sanganahalli, Basavaraju G ^a,b   Rebello, Michelle R ^b,d   Herman, Peter ^a,b   Papademetris, Xenophon ^b,c   Shepherd, Gordon M ^b   Verhagen, Justus V ^b,d   Hyder, Fahmeed ^a,b,c  

^a YALE UNIVERSITY   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Yale University   (United States)

^d JOHN B PIERCE LABORATORY   (United States)

Author keywords

BOLD signal; Energetics; Functional hyperemia; Glutamate; Intrinsic signal; Olfaction

Indexed keywords

BUTYRIC ACID ETHYL ESTER; CALCIUM ION; DEOXYHEMOGLOBIN; FLUORESCENT DYE; METHYL VALERATE; UNCLASSIFIED DRUG; VALERIC ACID; CALCIUM; FRAGRANCE;

ANIMAL EXPERIMENT; ARTICLE; BRAIN DEPTH STIMULATION; BRAIN ELECTROPHYSIOLOGY; BRAIN FUNCTION; COMPARATIVE STUDY; CONCEPTUAL FRAMEWORK; CONTROLLED STUDY; EVOKED RESPONSE; FLUORESCENCE IMAGING; FUNCTIONAL ASSESSMENT; FUNCTIONAL MAGNETIC RESONANCE IMAGING; IMAGING SYSTEM; NERVE CELL NETWORK; NEUROPIL; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SCANNER; OLFACTORY BULB; OLFACTORY BULB GLOMERULUS; OLFACTORY DISCRIMINATION; PRIORITY JOURNAL; RAT; REPRODUCIBILITY; SPATIOTEMPORAL ANALYSIS; SYNAPSE; WIDE-FIELD CALCIUM IMAGING; ANIMAL; BRAIN MAPPING; NUCLEAR MAGNETIC RESONANCE IMAGING; ODOR; PHYSIOLOGY; PROCEDURES; SPRAGUE DAWLEY RAT;

ANIMALS; BRAIN MAPPING; CALCIUM; MAGNETIC RESONANCE IMAGING; ODORANTS; OLFACTORY BULB; OPTICAL IMAGING; RATS; RATS, SPRAGUE-DAWLEY; SMELL;

EID: 84949267015     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2015.11.048     Document Type: Article

References (62)

1. Belluscio L., Katz L.C. Symmetry, stereotypy, and topography of odorant representations in mouse olfactory bulbs. J. Neurosci. 2001, 21:2113-2122.
2. Bojsen-Moller F., Fahrenkrug J. Nasal swell-bodies and cyclic changes in the air passage of the rat and rabbit nose. J. Anat. 1971, 110:25-37.
3. Bozza T., McGann J.P., Mombaerts P., Wachowiak M. In vivo imaging of neuronal activity by targeted expression of a genetically encoded probe in the mouse. Neuron 2004, 42:9-21.
4. Chaigneau E., Tiret P., Lecoq J., Ducros M., Knopfel T., Charpak S. The relationship between blood flow and neuronal activity in the rodent olfactory bulb. J. Neurosci. 2007, 27:6452-6460.
5. Charpak S., Mertz J., Beaurepaire E., Moreaux L., Delaney K. Odor-evoked calcium signals in dendrites of rat mitral cells. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:1230-1234.
6. Friedrich R.W., Korsching S.I. Combinatorial and chemotopic odorant coding in the zebrafish olfactory bulb visualized by optical imaging. Neuron 1997, 18:737-752.
7. Gautam S.H., Verhagen J.V. Evidence that the sweetness of odors depends on experience in rats. Chem. Senses 2010, 35:767-776.
8. Gautam S.H., Verhagen J.V. Direct behavioral evidence for retronasal olfaction in rats. PLoS One 2012, 7.
9. Gautam S.H., Short S.M., Verhagen J.V. Retronasal odor concentration coding in glomeruli of the rat olfactory bulb. Front. Integr. Neurosci. 2014, 8:81.
10. Goense J.B., Logothetis N.K. Neurophysiology of the BOLD fMRI signal in awake monkeys. Curr. Biol. 2008, 18:631-640.
11. Gurden H., Uchida N., Mainen Z.F. Sensory-evoked intrinsic optical signals in the olfactory bulb are coupled to glutamate release and uptake. Neuron 2006, 52:335-345.
12. Guthrie K.M., Gall C.M. Odors increase Fos in olfactory bulb neurons including dopaminergic cells. Neuroreport 1995, 6:2145-2149. (discussion 2103).
13. Guthrie K.M., Holmes J., Leon M. Focal 2-DG uptake persists following olfactory bulb lesions. Brain Res. Bull. 1995, 38:129-134.
14. Hirano Y., Stefanovic B., Silva A.C. Spatiotemporal evolution of the functional magnetic resonance imaging response to ultrashort stimuli. J. Neurosci. 2011, 31:1440-1447.
15. Hoge R.D. Calibrated FMRI. NeuroImage 2012, 62:930-937.
16. Homma R., Baker B.J., Jin L., Garaschuk O., Konnerth A., Cohen L.B., Zecevic D. Wide-field and two-photon imaging of brain activity with voltage- and calcium-sensitive dyes. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2009, 364:2453-2467.
17. Hyder F., Rothman D.L. Quantitative fMRI and oxidative neuroenergetics. NeuroImage 2012, 62:985-994.
18. Hyder F., Rothman D.L., Bennett M.R. Cortical energy demands of signaling and nonsignaling components in brain are conserved across mammalian species and activity levels. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:3549-3554.
19. Johnson B.A., Leon M. Modular representations of odorants in the glomerular layer of the rat olfactory bulb and the effects of stimulus concentration. J. Comp. Neurol. 2000, 422:496-509.
20. Joshi A., Scheinost D., Okuda H., Belhachemi D., Murphy I., Staib L.H., Papademetris X. Unified framework for development, deployment and robust testing of neuroimaging algorithms. Neuroinformatics 2011, 9:69-84.
21. Juchem C., Herman P., Sanganahalli B.G., Brown P.B., McIntyre S., Nixon T.W., Green D., Hyder F., de Graaf R.A. DYNAmic Multi-coIl TEchnique (DYNAMITE) shimming of the rat brain at 11.7T. NMR Biomed. 2014, 27:897-906.
22. Jukovskaya N., Tiret P., Lecoq J., Charpak S. What does local functional hyperemia tell about local neuronal activation?. J. Neurosci. 2011, 31:1579-1582.
23. Karbowski J. Constancy and trade-offs in the neuroanatomical and metabolic design of the cerebral cortex. Front. Neurol. Circuits 2014, 8:9.
24. Kauer J.S. Contributions of topography and parallel processing to odor coding in the vertebrate olfactory pathway. Trends Neurosci. 1991, 14:79-85.
25. Kida I., Xu F., Shulman R.G., Hyder F. Mapping at glomerular resolution: fMRI of rat olfactory bulb. Magn. Reson. Med. 2002, 48:570-576.
26. Kikuta S., Kashiwadani H., Mori K. Compensatory rapid switching of binasal inputs in the olfactory cortex. J. Neurosci. 2008, 28:11989-11997.
27. Lam Y.W., Cohen L.B., Wachowiak M., Zochowski M.R. Odors elicit three different oscillations in the turtle olfactory bulb. J. Neurosci. 2000, 20:749-762.
28. Lauritzen M. Relationship of spikes, synaptic activity, and local changes of cerebral blood flow. J. Cereb. Blood Flow Metab. 2001, 21:1367-1383.
29. Li B., Gong L., Wu R., Li A., Xu F. Complex relationship between BOLD-fMRI and electrophysiological signals in different olfactory bulb layers. NeuroImage 2014, 95:29-38.
30. Logothetis N.K., Pauls J., Augath M., Trinath T., Oeltermann A. Neurophysiological investigation of the basis of the fMRI signal. Nature 2001, 412:150-157.
31. Maandag N.J., Coman D., Sanganahalli B.G., Herman P., Smith A.J., Blumenfeld H., Shulman R.G., Hyder F. Energetics of neuronal signaling and fMRI activity. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:20546-20551.
32. Moreaux L., Laurent G. Estimating firing rates from calcium signals in locust projection neurons in vivo. Front. Neurol. Circuits 2007, 1:2.
33. Mukamel R., Gelbard H., Arieli A., Hasson U., Fried I., Malach R. Coupling between neuronal firing, field potentials, and FMRI in human auditory cortex. Science 2005, 309:951-954.
34. Nawroth J.C., Greer C.A., Chen W.R., Laughlin S.B., Shepherd G.M. An energy budget for the olfactory glomerulus. J. Neurosci. 2007, 27:9790-9800.
35. Osmanski B.F., Martin C., Montaldo G., Laniece P., Pain F., Tanter M., Gurden H. Functional ultrasound imaging reveals different odor-evoked patterns of vascular activity in the main olfactory bulb and the anterior piriform cortex. NeuroImage 2014, 95:176-184.
36. Petzold G.C., Albeanu D.F., Sato T.F., Murthy V.N. Coupling of neural activity to blood flow in olfactory glomeruli is mediated by astrocytic pathways. Neuron 2008, 58:897-910.
37. Poplawsky A.J., Kim S.G. Layer-dependent BOLD and CBV-weighted fMRI responses in the rat olfactory bulb. NeuroImage 2014, 91:237-251.
38. Qureshy A., Kawashima R., Imran M.B., Sugiura M., Goto R., Okada K., Inoue K., Itoh M., Schormann T., Zilles K., Fukuda H. Functional mapping of human brain in olfactory processing: a PET study. J. Neurophysiol. 2000, 84:1656-1666.
39. Ratzlaff E.H., Grinvald A. A tandem-lens epifluorescence macroscope: hundred-fold brightness advantage for wide-field imaging. J. Neurosci. Methods 1991, 36:127-137.
40. Rees G., Friston K., Koch C. A direct quantitative relationship between the functional properties of human and macaque V5. Nat. Neurosci. 2000, 3:716-723.
41. Rubin B.D., Katz L.C. Optical imaging of odorant representations in the mammalian olfactory bulb. Neuron 1999, 23:499-511.
42. Sanganahalli B.G., Bailey C.J., Herman P., Hyder F. Tactile and non-tactile sensory paradigms for fMRI and neurophysiologic studies in rodents. Methods Mol. Biol. 2009, 489:213-242.
43. Sanganahalli B.G., Herman P., Blumenfeld H., Hyder F. Oxidative neuroenergetics in event-related paradigms. J. Neurosci. 2009, 29:1707-1718.
44. Schafer J.R., Kida I., Rothman D.L., Hyder F., Xu F. Adaptation in the rodent olfactory bulb measured by fMRI. Magn. Reson. Med. 2005, 54:443-448.
45. Schafer J.R., Kida I., Xu F., Rothman D.L., Hyder F. Reproducibility of odor maps by fMRI in rodents. NeuroImage 2006, 31:1238-1246.
46. Schulz K., Sydekum E., Krueppel R., Engelbrecht C.J., Schlegel F., Schroter A., Rudin M., Helmchen F. Simultaneous BOLD fMRI and fiber-optic calcium recording in rat neocortex. Nat. Methods 2012, 9:597-602.
47. Sharp F.R., Kauer J.S., Shepherd G.M. Local sites of activity-related glucose metabolism in rat olfactory bulb during olfactory stimulation. Brain Res. 1975, 98:596-600.
48. Smith A.J., Blumenfeld H., Behar K.L., Rothman D.L., Shulman R.G., Hyder F. Cerebral energetics and spiking frequency: the neurophysiological basis of fMRI. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:10765-10770.
49. Stewart W.B., Kauer J.S., Shepherd G.M. Functional organization of rat olfactory bulb analysed by the 2-deoxyglucose method. J. Comp. Neurol. 1979, 185:715-734.
50. Uchida N., Takahashi Y.K., Tanifuji M., Mori K. Odor maps in the mammalian olfactory bulb: domain organization and odorant structural features. Nat. Neurosci. 2000, 3:1035-1043.
51. Verhagen J.V., Wesson D.W., Netoff T.I., White J.A., Wachowiak M. Sniffing controls an adaptive filter of sensory input to the olfactory bulb. Nat. Neurosci. 2007, 10:631-639.
52. Wachowiak M., Cohen L.B. Presynaptic afferent inhibition of lobster olfactory receptor cells: reduced action-potential propagation into axon terminals. J. Neurophysiol. 1998, 80:1011-1015.
53. Wachowiak M., Cohen L.B. Representation of odorants by receptor neuron input to the mouse olfactory bulb. Neuron 2001, 32:723-735.
54. Wachowiak M., Cohen L.B. Correspondence between odorant-evoked patterns of receptor neuron input and intrinsic optical signals in the mouse olfactory bulb. J. Neurophysiol. 2003, 89:1623-1639.
55. Wachowiak M., Cohen L.B., Ache B.W. Presynaptic inhibition of olfactory receptor neurons in crustaceans. Microsc. Res. Tech. 2002, 58:365-375.
56. Wachowiak M., Cohen L.B., Zochowski M.R. Distributed and concentration-invariant spatial representations of odorants by receptor neuron input to the turtle olfactory bulb. J. Neurophysiol. 2002, 87:1035-1045.
57. Wachowiak M., Economo M.N., Diaz-Quesada M., Brunert D., Wesson D.W., White J.A., Rothermel M. Optical dissection of odor information processing in vivo using GCaMPs expressed in specified cell types of the olfactory bulb. J. Neurosci. 2013, 33:5285-5300.
58. Xu F., Kida I., Hyder F., Shulman R.G. Assessment and discrimination of odor stimuli in rat olfactory bulb by dynamic functional MRI. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:10601-10606.
59. Xu F., Liu N., Kida I., Rothman D.L., Hyder F., Shepherd G.M. Odor maps of aldehydes and esters revealed by functional MRI in the glomerular layer of the mouse olfactory bulb. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:11029-11034.
60. 2+ imaging. Nat. Methods 2006, 3:377-383.
61. Yang X., Renken R., Hyder F., Siddeek M., Greer C.A., Shepherd G.M., Shulman R.G. Dynamic mapping at the laminar level of odor-elicited responses in rat olfactory bulb by functional MRI. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:7715-7720.
62. Youngentob S.L., Mozell M.M., Sheehe P.R., Hornung D.E. A quantitative analysis of sniffing strategies in rats performing odor detection tasks. Physiol. Behav. 1987, 41:59-69.