Complex relationship between BOLD-fMRI and electrophysiological signals in different olfactory bulb layers

NeuroImage

Volumn 95, Issue , 2014, Pages 29-38

  Li, Bo ^a,c   Gong, Ling ^a,c   Wu, Ruiqi ^a,c   Li, Anan ^a   Xu, Fuqiang ^a,b  

^a Wuhan National Laboratory for Optoelectronics   (China)

^b HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^c UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

Blood oxygenation level dependent (BOLD); Functional MRI; Layer dependent; Local field potentials (LFP); Olfactory bulb

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BOLD SIGNAL; CONTROLLED STUDY; ELECTRIC POTENTIAL; EVOKED RESPONSE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GAMMA RHYTHM; GLOMERULAR LAYER; GRANULAR CELL; GRANULE CELL LAYER; MITRAL CELL; NONHUMAN; ODOR; OLFACTORY BULB; OLFACTORY NERVE; PRIORITY JOURNAL; RAT; SENSORY STIMULATION; STIMULUS RESPONSE; ACTION POTENTIAL; ANIMAL; BLOOD; BRAIN MAPPING; ELECTROPHYSIOLOGY; IMAGE PROCESSING; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; PROCEDURES; SPRAGUE DAWLEY RAT;

OXYGEN;

ACTION POTENTIALS; ANIMALS; BRAIN MAPPING; ELECTROPHYSIOLOGICAL PHENOMENA; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; OLFACTORY BULB; OXYGEN; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84899810455     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2014.03.052     Document Type: Article

References (75)

1. Alonso M., Lepousez G., Sebastien W., Bardy C., Gabellec M.M., Torquet N., Lledo P.M. Activation of adult-born neurons facilitates learning and memory. Nat. Neurosci. 2012, 15:897-904.
2. Bailey C.J., Sanganahalli B.G., Herman P., Blumenfeld H., Gjedde A., Hyder F. Analysis of time and space invariance of BOLD responses in the rat visual system. Cereb. Cortex 2013, 23:210-222.
3. Bandettini P.A. Twenty years of functional MRI: the science and the stories. Neuroimage 2012, 62:575-588.
4. Borowsky I.W., Collins R.C. Metabolic anatomy of brain: a comparison of regional capillary density, glucose metabolism, and enzyme activities. J. Comp. Neurol. 1989, 288:401-413.
5. Buzsaki G. Neural syntax: cell assemblies, synapsembles, and readers. Neuron 2010, 68:362-385.
6. Buzsaki G., Anastassiou C.A., Koch C. The origin of extracellular fields and currents-EEG, ECoG, LFP and spikes. Nat. Rev. Neurosci. 2012, 13:407-420.
7. Cenier T., David F., Litaudon P., Garcia S., Amat C., Buonviso N. Respiration-gated formation of gamma and beta neural assemblies in the mammalian olfactory bulb. Eur. J. Neurosci. 2009, 29:921-930.
8. Chaudhury D., Manella L., Arellanos A., Escanilla O., Cleland T.A., Linster C. Olfactory bulb habituation to odor stimuli. Behav. Neurosci. 2010, 124:490-499.
9. Cleland T.A., Johnson B.A., Leon M., Linster C. Relational representation in the olfactory system. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:1953-1958.
10. DeSalvo M.N., Schridde U., Mishra A.M., Motelow J.E., Purcaro M.J., Danielson N., Bai X., Hyder F., Blumenfeld H. Focal BOLD fMRI changes in bicuculline-induced tonic-clonic seizures in the rat. Neuroimage 2010, 50:902-909.
11. Doucette W., Restrepo D. Profound context-dependent plasticity of mitral cell responses in olfactory bulb. PLoS Biol. 2008, 6:e258.
12. Doucette W., Gire D.H., Whitesell J., Carmean V., Lucero M.T., Restrepo D. Associative cortex features in the first olfactory brain relay station. Neuron 2011, 69:1176-1187.
13. Febo M. Technical and conceptual considerations for performing and interpreting functional MRI studies in awake rats. Front. Psychiatry 2011, 2:43.
14. Gao J.H., Liu H.L. Inflow effects on functional MRI. Neuroimage 2012, 62:1035-1039.
15. Gervais R., Buonviso N., Martin C., Ravel N. What do electrophysiological studies tell us about processing at the olfactory bulb level?. J. Physiol. Paris 2007, 101:40-45.
16. Gheusi G., Cremer H., McLean H., Chazal G., Vincent J.D., Lledo P.M. Importance of newly generated neurons in the adult olfactory bulb for odor discrimination. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:1823-1828.
17. Goense J.B., Logothetis N.K. Neurophysiology of the BOLD fMRI signal in awake monkeys. Curr. Biol. 2008, 18:631-640.
18. 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.
19. Herman P., Sanganahalli B.G., Blumenfeld H., Rothman D.L., Hyder F. Quantitative basis for neuroimaging of cortical laminae with calibrated functional MRI. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:15115-15120.
20. Huttunen J.K., Grohn O., Penttonen M. Coupling between simultaneously recorded BOLD response and neuronal activity in the rat somatosensory cortex. Neuroimage 2008, 39:775-785.
21. Hyder F., Rothman D.L., Shulman R.G. Total neuroenergetics support localized brain activity: implications for the interpretation of fMRI. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:10771-10776.
22. Igarashi K.M., Mori K. Spatial representation of hydrocarbon odorants in the ventrolateral zones of the rat olfactory bulb. J. Neurophysiol. 2005, 93:1007-1019.
23. Johnson B.A., Leon M. Chemotopic odorant coding in a mammalian olfactory system. J. Comp. Neurol. 2007, 503:1-34.
24. Johnson B.A., Woo C.C., Hingco E.E., Pham K.L., Leon M. Multidimensional chemotopic responses to n-aliphatic acid odorants in the rat olfactory bulb. J. Comp. Neurol. 1999, 409:529-548.
25. Johnson B.A., Xu Z., Ali S.S., Leon M. Spatial representations of odorants in olfactory bulbs of rats and mice: similarities and differences in chemotopic organization. J. Comp. Neurol. 2009, 514:658-673.
26. Kahn I., Knoblich U., Desai M., Bernstein J., Graybiel A.M., Boyden E.S., Buckner R.L., Moore C.I. Optogenetic drive of neocortical pyramidal neurons generates fMRI signals that are correlated with spiking activity. Brain Res. 2013, 1511:33-45.
27. Kay L.M., Beshel J., Brea J., Martin C., Rojas-Libano D., Kopell N. Olfactory oscillations: the what, how and what for. Trends Neurosci. 2009, 32:207-214.
28. Kayser C., Petkov C.I., Logothetis N.K. Multisensory interactions in primate auditory cortex: fMRI and electrophysiology. Hear. Res. 2009, 258:80-88.
29. Lang J., Li A., Luo W., Wu R., Li P., Xu F. Odor representation in the olfactory bulb under different brain states revealed by intrinsic optical signals imaging. Neuroscience 2013, 243:54-63.
30. Lazarini F., Lledo P.M. Is adult neurogenesis essential for olfaction?. Trends Neurosci. 2011, 34:20-30.
31. Lecoq J., Tiret P., Charpak S. Peripheral adaptation codes for high odor concentration in glomeruli. J. Neurosci. 2009, 29:3067-3072.
32. Li A.A., Gong L., Liu Q., Li X., Xu F. State-dependent coherences between the olfactory bulbs for delta and theta oscillations. Neurosci. Lett. 2010, 480:44-48.
33. Li A., Gong L., Xu F. Brain-state-independent neural representation of peripheral stimulation in rat olfactory bulb. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:5087-5092.
34. Li A., Zhang L., Liu M., Gong L., Liu Q., Xu F. Effects of different anesthetics on oscillations in the rat olfactory bulb. J. Am. Assoc. Lab. Anim. Sci. 2012, 51:458-463.
35. Lippert M.T., Steudel T., Ohl F., Logothetis N.K., Kayser C. Coupling of neural activity and fMRI-BOLD in the motion area MT. Magn. Reson. Imaging 2010, 28:1087-1094.
36. Liu N., Xu F., Miller P.L., Shepherd G.M. OdorMapComparer: an application for quantitative analyses and comparisons of fMRI brain odor maps. Neuroinformatics 2007, 5:105-114.
37. Liu H.L., Wei P.S., Wai Y.Y., Kuan W.C., Huang C.M., Wu C.W., Buckle C., Wan Y.L., Gao J.H. Inflow effects on hemodynamic responses characterized by event-related fMRI using gradient-echo EPI sequences. Med. Phys. 2008, 35:4300-4307.
38. Logothetis N.K. What we can do and what we cannot do with fMRI. Nature 2008, 453:869-878.
39. Logothetis N.K., Wandell B.A. Interpreting the BOLD signal. Annu. Rev. Physiol. 2004, 66:735-769.
40. 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.
41. 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.
42. Magri C., Schridde U., Murayama Y., Panzeri S., Logothetis N.K. The amplitude and timing of the BOLD signal reflects the relationship between local field potential power at different frequencies. J. Neurosci. 2012, 32:1395-1407.
43. Maier A., Wilke M., Aura C., Zhu C., Ye F.Q., Leopold D.A. Divergence of fMRI and neural signals in V1 during perceptual suppression in the awake monkey. Nat. Neurosci. 2008, 11:1193-1200.
44. Mandairon N., Stack C., Kiselycznyk C., Linster C. Broad activation of the olfactory bulb produces long-lasting changes in odor perception. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:13543-13548.
45. Martin C., Grenier D., Thevenet M., Vigouroux M., Bertrand B., Janier M., Ravel N., Litaudon P. fMRI visualization of transient activations in the rat olfactory bulb using short odor stimulations. Neuroimage 2007, 36:1288-1293.
46. Martin C.J., Kennerley A.J., Berwick J., Port M., Mayhew J.E. Functional MRI in conscious rats using a chronically implanted surface coil. J. Magn. Reson. Imaging 2013, 38(3):739-744.
47. Mishra A.M., Ellens D.J., Schridde U., Motelow J.E., Purcaro M.J., DeSalvo M.N., Enev M., Sanganahalli B.G., Hyder F., Blumenfeld H. Where fMRI and electrophysiology agree to disagree: corticothalamic and striatal activity patterns in the WAG/Rij rat. J. Neurosci. 2011, 31:15053-15064.
48. Mori K., Takahashi Y.K., Igarashi K.M., Yamaguchi M. Maps of odorant molecular features in the Mammalian olfactory bulb. Physiol. Rev. 2006, 86:409-433.
49. Mullinger K.J., Mayhew S.D., Bagshaw A.P., Bowtell R., Francis S.T. Poststimulus undershoots in cerebral blood flow and BOLD fMRI responses are modulated by poststimulus neuronal activity. Proc. Natl. Acad. Sci. U. S. A. 2013, 110(33):13636-13641.
50. 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.
51. Neville K.R., Haberly L.B. Beta and gamma oscillations in the olfactory system of the urethane-anesthetized rat. J. Neurophysiol. 2003, 90:3921-3930.
52. Panagiotaropoulos T.I., Deco G., Kapoor V., Logothetis N.K. Neuronal discharges and gamma oscillations explicitly reflect visual consciousness in the lateral prefrontal cortex. Neuron 2012, 74:924-935.
53. 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.
54. Rasch M., Logothetis N.K., Kreiman G. From neurons to circuits: linear estimation of local field potentials. J. Neurosci. 2009, 29:13785-13796.
55. Restrepo D., Doucette W., Whitesell J.D., McTavish T.S., Salcedo E. From the top down: flexible reading of a fragmented odor map. Trends Neurosci. 2009, 32:525-531.
56. Rojas-Libano D., Kay L.M. Olfactory system gamma oscillations: the physiological dissection of a cognitive neural system. Cogn. Neurodyn. 2008, 2:179-194.
57. Sanganahalli B.G., Herman P., Behar K.L., Blumenfeld H., Rothman D.L., Hyder F. Functional MRI and neural responses in a rat model of Alzheimer's disease. Neuroimage 2013, 79:404-411.
58. 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.
59. 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.
60. Schoppa N.E., Urban N.N. Dendritic processing within olfactory bulb circuits. Trends Neurosci. 2003, 26:501-506.
61. Shepherd G.M., Charpak S. The olfactory glomerulus: a model for neuro-glio-vascular biology. Neuron 2008, 58:827-829.
62. Shipley M.T., Ennis M. Functional organization of olfactory system. J. Neurobiol. 1996, 30:123-176.
63. Shmuel A., Augath M., Oeltermann A., Logothetis N.K. Negative functional MRI response correlates with decreases in neuronal activity in monkey visual area V1. Nat. Neurosci. 2006, 9:569-577.
64. Sloan H.L., Austin V.C., Blamire A.M., Schnupp J.W., Lowe A.S., Allers K.A., Matthews P.M., Sibson N.R. Regional differences in neurovascular coupling in rat brain as determined by fMRI and electrophysiology. Neuroimage 2010, 53:399-411.
65. Takahashi Y.K., Kurosaki M., Hirono S., Mori K. Topographic representation of odorant molecular features in the rat olfactory bulb. J. Neurophysiol. 2004, 92:2413-2427.
66. Viswanathan A., Freeman R.D. Neurometabolic coupling in cerebral cortex reflects synaptic more than spiking activity. Nat. Neurosci. 2007, 10:1308-1312.
67. Wang L., Saalmann Y.B., Pinsk M.A., Arcaro M.J., Kastner S. Electrophysiological low-frequency coherence and cross-frequency coupling contribute to BOLD connectivity. Neuron 2012, 76:1010-1020.
68. Willhite D.C., Nguyen K.T., Masurkar A.V., Greer C.A., Shepherd G.M., Chen W.R. Viral tracing identifies distributed columnar organization in the olfactory bulb. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:12592-12597.
69. Wilson R.I., Mainen Z.F. Early events in olfactory processing. Annu. Rev. Neurosci. 2006, 29:163-201.
70. 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.
71. 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.
72. Xu F., Schaefer M., Kida I., Schafer J., Liu N., Rothman D.L., Hyder F., Restrepo D., Shepherd G.M. Simultaneous activation of mouse main and accessory olfactory bulbs by odors or pheromones. J. Comp. Neurol. 2005, 489:491-500.
73. 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.
74. Yen C.C., Fukuda M., Kim S.G. BOLD responses to different temporal frequency stimuli in the lateral geniculate nucleus and visual cortex: insights into the neural basis of fMRI. Neuroimage 2011, 58:82-90.
75. Young C.K., Brown A.R., Robinson J.H., Tuor U.I., Dunn J.F., Bland B.H., Teskey G.C. Functional MRI response and correlated electrophysiological changes during posterior hypothalamic nucleus deep brain stimulation. Neuroimage 2011, 56:35-44.