Neural and hemodynamic responses elicited by forelimb- and photo-stimulation in channelrhodopsin-2 mice: Insights into the hemodynamic point spread function

Cerebral Cortex

Volumn 24, Issue 11, 2014, Pages 2908-2919

  Vazquez, Alberto L ^a,b   Fukuda, Mitsuhiro ^a   Crowley, Justin C ^c   Kim, Seong Gi ^a,b  

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

^b University of Pittsburgh   (United States)

^c CARNEGIE MELLON UNIVERSITY   (United States)

Author keywords

fMRI; hemodynamics; laminar activity; optogenetics; point spread function

Indexed keywords

CHANNELRHODOPSIN 2; RHODOPSIN; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; CHANNELRHODOPSIN 2, MOUSE; PHOTOPROTEIN; YELLOW FLUORESCENT PROTEIN, BACTERIA;

ANIMAL EXPERIMENT; ARTICLE; BRAIN ELECTROPHYSIOLOGY; BRAIN FUNCTION; CONTROLLED STUDY; ELECTRODE; FORELIMB; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HEMODYNAMICS; LASER DOPPLER FLOWMETRY; MOUSE; NONHUMAN; OPTOGENETICS; PHOTOSTIMULATION; POINT SPREAD FUNCTION; SOMATOSENSORY STIMULATION; TRANSGENIC MOUSE; ANIMAL; BRAIN CIRCULATION; C57BL MOUSE; CYTOLOGY; ELECTROSTIMULATION; EVOKED RESPONSE; GENETICS; INNERVATION; METABOLISM; NERVE CELL; PHYSIOLOGY; SENSORY NERVE; SOMATOSENSORY CORTEX; TIME FACTOR; VASCULARIZATION;

AFFERENT PATHWAYS; ANIMALS; BACTERIAL PROTEINS; CEREBROVASCULAR CIRCULATION; ELECTRIC STIMULATION; EVOKED POTENTIALS; FORELIMB; HEMODYNAMICS; LASER-DOPPLER FLOWMETRY; LUMINESCENT PROTEINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURONS; PHOTIC STIMULATION; RHODOPSIN; SOMATOSENSORY CORTEX; TIME FACTORS;

EID: 84910674912     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bht147     Document Type: Article

References (40)

1. Altamura C, Dell'Acqua ML, Moessner R, Murphy DL, Lesch KP, Persico AM. 2007. Altered neocortical cell density and layer thickness in serotonin transporter knockout mice: A quantitation study. Cereb Cortex. 17:1394-1401.
2. Arenkiel B, Peca J, Davison I, Feliciano C, Deisseroth K, Augustine G, Ehlers M, Feng G. 2007. In vivo light-induced activation of neural circuitry in transgenic mice expressing channelrhodopsin-2. Neuron. 54:205-218.
3. Armstrong-James M, Fox K, Das-Gupta A. 1992. Flow of excitation within rat barrel cortex on striking a single vibrissa. J Neurophysiol. 68:1345-1358.
4. Ayling OGS, Harrison TC, Boyd JD, Goroshkov A, Murphy TH. 2009. Automated light-based mapping of motor cortex by photoactivation of channelrhodopsin-2 transgenic mice. Nat Methods. 6:219-224.
5. Berwick J, Johnston D, Jones M, Martindale J, Martin C, Kennerley AJ, Redgrave P, Mayhew JEW. 2008. Fine detail of neurovascular coupling revealed by spatiotemporal analysis of the hemodynamic response to single whisker stimulation in rat barrel cortex. J Neurophysiol. 99:787-798.
6. Boynton GM, Engel SA, Glover GH, Heeger DJ. 1996. Linear systems analysis of functional magnetic resonance imaging in human V1. J Neurosci. 16:4207-4222.
7. Buxton R, Wong E, Frank L. 1998. Dynamics of blood flow and oxygenation changes during brain activation: The balloon model. Magn Reson Med. 39:855-864.
8. Cheng K, Waggoner RA, Tanaka K. 2001. Human ocular dominance columns as revealed by high-field functional magnetic resonance imaging. Neuron. 32:359-374.
9. Davis T, Kwong K, Weisskoff R, Rosen B. 1998. Calibrated functional MRI: Mapping the dynamics of oxidative metabolism. Proc Natl Acad Sci USA. 95:1834-1839.
10. de Kock CPJ, Bruno RM, Spors H, Sakmann B. 2007. Layer-And cell-Type-specific suprathreshold stimulus representation in rat primary somatosensory cortex. J Physiol (Lond). 581:139-154.
11. Desai M, Kahn I, Knoblich U, Bernstein J, Atallah H, Yang A, Kopell N, Buckner RL, Graybiel AM, Moore CI et al. 2011. Mapping brain networks in awake mice using combined optical neural control and fMRI. J Neurophysiol. 105:1393-1405.
12. Duong T, Kim D, Ugurbil K, Kim S. 2001. Localized cerebral blood flow response at submillimeter columnar resolution. Proc Natl Acad Sci USA. 98:10904-10909.
13. Engel S. 1997. Retinotopic organization in human visual cortex and the spatial precision of functional MRI. Cereb Cortex. 7:181-192.
14. Fukuda M, Rajagopalan U, Homma R, Matsumoto M, Nishizaki M, Tanifuji M. 2005. Localization of activity-dependent changes in blood volume to submillimeter-scale functional domains in cat visual cortex. Cereb Cortex. 15:823-833.
15. Fukuda M, Moon C, Wang P, Kim SG. 2006. Mapping iso-orientation columns by contrast agent-enhanced functional magnetic resonance imaging: Reproducibility, specificity, and evaluation by optical imaging of intrinsic signal. J Neurosci. 26:11821-11832.
16. Hansen KA, David SV, Gallant JL. 2004. Parametric reverse correlation reveals spatial linearity of retinotopic human V1 BOLD response. Neuroimage. 23:233-241.
17. Kahn I, Desai M, Knoblich U, Bernstein J, Henninger M, Graybiel AM, Boyden ES, Buckner RL, Moore CI. 2011. Characterization of the functional MRI response temporal linearity via optical control of neocortical pyramidal neurons. J Neurosci. 31:15086-15091.
18. Kim S, Rostrup E, Larsson H, Ogawa S, Paulson O. 1999. Determination of relative CMRO2 from CBF and BOLD changes: Significant increase of oxygen consumption rate during visual stimulation. Magn Reson Med. 41:1152-1161.
19. Kim SG, Ogawa S. 2012. Biophysical and physiological origins of blood oxygenation level-dependent fMRI signals. J Cereb Blood Flow Metab. 32:1188-1206.
20. Logothetis N, Pauls J, Augath M, Trinath T, Oeltermann A. 2001. Neurophysiological investigation of the basis of the fMRI signal. Nature. 412:150-157.
21. Malonek D, Grinvald A. 1996. Interactions between electrical activity and cortical microcirculation revealed by imaging spectroscopy: Implications for functional brain mapping. Science. 272:551-554.
22. Martindale J, Berwick J, Martin C, Kong Y, Zheng Y, Mayhew J. 2005. Long duration stimuli and nonlinearities in the neural-haemodynamic coupling. J Cereb Blood Flow Metab. 25:651-661.
23. Menon RS, Goodyear BG. 1999. Submillimeter functional localization in human striate cortex using BOLD contrast at 4 Tesla: Implications for the vascular point-spread function. Magn Reson Med. 41:230-235.
24. Moon C, Fukuda M, Park S, Kim S. 2007. Neural interpretation of blood oxygenation level-dependent fMRI maps at submillimeter columnar resolution. J Neurosci. 27:6892-6902.
25. Oberlaender M, de Kock CPJ, Bruno RM, Ramirez A, Meyer HS, Dercksen VJ, Helmstaedter M, Sakmann B. 2012. Cell type-specific threedimensional structure of thalamocortical circuits in a column of rat vibrissal cortex. Cereb Cortex. 22:2375-2391.
26. Ogawa S, Lee TM, Stepnoski R, Chen W, Zhu XH, Ugurbil K. 2000. An approach to probe some neural systems interaction by functional MRI at neural time scale down to milliseconds. Proc Natl Acad Sci USA. 97:11026-11031.
27. Ogawa S, Menon R, Tank D, Kim S, Merkle H, Ellermann J, Ugurbil K. 1993. Functional brain mapping by blood oxygenation leveldependent contrast magnetic resonance imaging. A comparison of signal characteristics with a biophysical model. Biophys J. 64:803-812.
28. Rios C, Zhang N, Yang L, Chen W, He B. 2010. Linear and nonlinear relationships between visual stimuli, EEG and BOLD fMRI signals. Neuroimage. 50:1054-1066.
29. Sanganahalli BG, Herman P, Blumenfeld H, Hyder F. 2009. Oxidative neuroenergetics in event-related paradigms. J Neurosci. 29:1707-1718.
30. Scott NA, Murphy TH. 2012. Hemodynamic responses evoked by neuronal stimulation via channelrhodopsin-2 can be independent of intracortical glutamatergic synaptic transmission. PLoS ONE. 7: E29859.
31. Shmuel A, Yacoub E, Chaimow D, Logothetis NK, Ugurbil K. 2007. Spatio-Temporal point-spread function of fMRI signal in human gray matter at 7 Tesla. Neuroimage. 35:539-552.
32. Silva AC, Lee SP, Yang G, Iadecola C, Kim SG. 1999. Simultaneous blood oxygenation level-dependent and cerebral blood flow functional magnetic resonance imaging during forepaw stimulation in the rat. J Cereb Blood Flow Metab. 19:871-879.
33. Tian P, Teng IC, May LD, Kurz R, Lu K, Scadeng M, Hillman EMC, De Crespigny AJ, D'Arceuil HE, Mandeville JB et al. 2010. Cortical depth-specific microvascular dilation underlies laminar differences in blood oxygenation level-dependent functional MRI signal. Proc Natl Acad Sci USA. 107:15246-15251.
34. Vazquez AL, Fukuda M, Tasker ML, Masamoto K, Kim S-G. 2010. Changes in cerebral arterial, tissue and venous oxygenation with evoked neural stimulation: Implications for hemoglobin-based functional neuroimaging. J Cereb Blood Flow Metab. 30: 428-439.
35. Vazquez AL, Noll D. 1998. Nonlinear aspects of the BOLD response in functional MRI. Neuroimage. 7:108-118.
36. Wang H, Peca J, Matsuzaki M, Matsuzaki K, Noguchi J, Qiu L, Wang D, Zhang F, Boyden E, Deisseroth K et al. 2007. High-speed mapping of synaptic connectivity using photostimulation in Channelrhodopsin-2 transgenic mice. Proc Natl Acad Sci USA. 104:8143-8148.
37. Weber B, Burger C, Wyss M, Schulthess von G, Scheffold F, Buck A. 2004. Optical imaging of the spatiotemporal dynamics of cerebral blood flow and oxidative metabolism in the rat barrel cortex. Eur J Neurosci. 20:2664-2670.
38. Yacoub E, Harel N, Ugurbil K. 2008. High-field fMRI unveils orientation columns in humans. Proc Natl Acad Sci USA. 105:10607-10612.
39. Yang X, Hyder F, Shulman R. 1996. Activation of single whisker barrel in rat brain localized by functional magnetic resonance imaging. Proc Natl Acad Sci USA. 93:475-478.
40. Zhao F, Wang P, Hendrich K, Kim S. 2005. Spatial specificity of cerebral blood volume-weighted fMRI responses at columnar resolution. Neuroimage. 27:416-424.