Analysis of time and space invariance of BOLD responses in the rat visual system

Cerebral Cortex

Volumn 23, Issue 1, 2013, Pages 210-222

  Bailey, Christopher J ^a,b,c,d   Sanganahalli, Basavaraju G ^a,b,e   Herman, Peter ^a,b,e   Blumenfeld, Hal ^b,e   Gjedde, Albert ^c,d   Hyder, Fahmeed ^a,b,e,f  

^a Magnetic Resonance Research Center (MRRC)   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c AARHUS UNIVERSITY   (Denmark)

^d AARHUS UNIVERSITY HOSPITAL   (Denmark)

^e Department of Diagnostic Radiology ^*  (United States)

^f Yale University   (United States)

Author keywords

calibrated fMRI; local field potential; multiunit activity; neuroenergetics; neurometabolic coupling; transfer function

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BLOOD OXYGENATION; BLOOD OXYGENATION LEVEL DEPENDENT; BRAIN BLOOD FLOW; COLOR VISION; FUNCTIONAL MAGNETIC RESONANCE IMAGING; NONHUMAN; PRIORITY JOURNAL; RAT; SPACE; STRIATE CORTEX; SUPERIOR COLLICULUS; TIME; VISUAL STIMULATION; VISUAL SYSTEM;

ANIMALS; BLOOD FLOW VELOCITY; BRAIN MAPPING; CEREBROVASCULAR CIRCULATION; MAGNETIC RESONANCE IMAGING; MALE; OXYGEN; PHOTIC STIMULATION; RATS; RATS, LONG-EVANS; VISUAL PERCEPTION;

EID: 84870851785     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhs008     Document Type: Article

References (78)

1. Berwick J, Johnston D, Jones M, Martindale J, Martin C, Kennerley AJ, Redgrave P, Mayhew JE. 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.
2. Binns KE. 1999. The synaptic pharmacology underlying sensory processing in the superior colliculus. Prog Neurobiol. 59:129-159.
3. Birn RM, Saad ZS, Bandettini PA. 2001. Spatial heterogeneity of the nonlinear dynamics in the FMRI BOLD response. Neuroimage. 14:817-826.
4. Borowsky IW, Collins RC. 1989. Metabolic anatomy of brain: a comparison of regional capillary density, glucose metabolism, and enzyme activities. J Comp Neurol. 288:401-413.
5. Boynton GM, Engel SA, Glover GH, Heeger DJ. 1996. Linear systems analysis of functional magnetic resonance imaging in human V1. J Neurosci. 16:4207-4221.
6. Carlson T, Hogendoorn H, Fonteijn H, Verstraten FA. 2011. Spatial coding and invariance in object-selective cortex. Cortex. 47:14-22.
7. Castro-Alamancos MA. 2004. Dynamics of sensory thalamocortical synaptic networks during information processing states. Prog Neurobiol. 74:213-247.
8. Dräger UC, Olsen JF. 1980. Origins of crossed and uncrossed retinal projections in pigmented and albino mice. J Comp Neurol. 191:383-412.
9. Engel SA, Glover GH, Wandell BA. 1997. Retinotopic organization in human visual cortex and the spatial precision of functional MRI. Cereb Cortex. 7:181-192.
10. Englot DJ, Mishra AM, Mansuripur PK, Herman P, Hyder F, Blumenfeld H. 2008. Remote effects of focal hippocampal seizures on the rat neocortex. J Neurosci. 28:9066-9081.
11. Frackowiak RSJ. 2004. Human brain function. Amsterdam: Elsevier Academic Press.
12. Frahm J, Haase A, Matthaei D. 1986. Rapid three-dimensional MR imaging using the FLASH technique. J Comput Assist Tomogr. 10:363-368.
13. Friston KJ. 1998. Imaging neuroscience: principles or maps? Proc Natl Acad Sci USA. 95:796-802.
14. Friston KJ, Josephs O, Rees G, Turner R. 1998. Nonlinear event-related responses in fMRI. Magn Reson Med. 39:41-52.
15. Gias C, Hewson-Stoate N, Jones M, Johnston D, Mayhew JE, Coffey PJ. 2005. Retinotopy within rat primary visual cortex using optical imaging. Neuroimage. 24:200-206.
16. Girman SV, Lund RD. 2007. Most superficial sublamina of rat superior colliculus: neuronal response properties and correlates with perceptual figure-ground segregation. J Neurophysiol. 98:161-177.
17. Girman SV, Sauvé Y, Lund RD. 1999. Receptive field properties of single neurons in rat primary visual cortex. J Neurophysiol. 82:301-311.
18. Goense JBM, Logothetis NK. 2008. Neurophysiology of the BOLD fMRI signal in awake monkeys. Curr Biol. 18:631-640.
19. Gutschalk A, Hamalainen MS, Melcher JR. 2010. BOLD responses in human auditory cortex are more closely related to transient MEG responses than sustained ones. J Neurophysiol. 103:2015-2026.
20. Harms MP, Melcher JR. 2003. Detection and quantification of a wide range of fMRI temporal responses using a physiologically-motivated basis set. Hum Brain Mapp. 20:168-183.
21. Hennig J, Nauerth A, Friedburg H. 1986. RARE imaging: a fast imaging method for clinical MR. Magn Reson Med. 3:823-833.
22. Herman P, Sanganahalli BG, Blumenfeld H, Hyder F. 2009. Cerebral oxygen demand for short-lived and steady-state events. J Neurochem. 109(Suppl 1):73-79.
23. Hespanha JP. 2009. Linear systems theory. Princeton (NJ): Princeton University Press.
24. Hirano Y, Stefanovic B, Silva AC. 2011. Spatiotemporal evolution of the functional magnetic resonance imaging response to ultrashort stimuli. J Neurosci. 31:1440-1447.
25. Huettel SA, Song AW, McCarthy G. 2004. Functional magnetic resonance imaging. Sunderland (MA): Sinauer Associates, Inc.
26. Huttunen JK, Gröhn O, Penttonen M. 2008. Coupling between simultaneously recorded BOLD response and neuronal activity in the rat somatosensory cortex. Neuroimage. 39:775-785.
27. Huttunen JK, Niskanen J-P, Lehto LJ, Airaksinen AM, Niskanen EI, Penttonen M, Gröhn O. 2011. Evoked local field potentials can explain temporal variation in blood oxygenation level-dependent responses in rat somatosensory cortex. NMR Biomed. 24:209-215.
28. Hyder F, Kida I, Behar KL, Kennan RP, Maciejewski PK, Rothman DL. 2001. Quantitative functional imaging of the brain: towards mapping neuronal activity by BOLD fMRI. NMR Biomed. 14:413-431.
29. Hyder F, Rothman DL, Blamire AM. 1995. Image reconstruction of sequentially sampled echo-planar data. Magn Reson Imaging. 13:97-103.
30. Hyder F, Sanganahalli BG, Herman P, Coman D, Maandag NJG, Behar KL, Blumenfeld H, Rothman DL. 2010. Neurovascular and neurometabolic couplings in dynamic calibrated fMRI: transient oxidative neuroenergetics for block-design and event-related paradigms. Front Neuroenergetics. 2.
31. Iadecola C. 2004. Neurovascular regulation in the normal brain and in Alzheimer's disease. Nat Rev Neurosci. 5:347-360.
32. Iadecola C, Nakai M, Mraovitch S, Ruggiero DA, Tucker LW, Reis DJ. 1983. Global increase in cerebral metabolism and blood flow produced by focal electrical stimulation of dorsal medullary reticular formation in rat. Brain Res. 272:101-114.
33. Jacobs GH, Fenwick JA, Williams GA. 2001. Cone-based vision of rats for ultraviolet and visible lights. J Exp Biol. 204:2439-2446.
34. Janz C, Heinrich SP, Kornmayer J, Bach M, Hennig J. 2001. Coupling of neural activity and BOLD fMRI response: new insights by combination of fMRI and VEP experiments in transition from single events to continuous stimulation. Magn Reson Med. 46:482-486.
35. Kannurpatti SS, Biswal BB. 2006. Spatial extent of CBF response during whisker stimulation using trial averaged laser Doppler imaging. Brain Res. 1089:135-142.
36. Kim D-S, Ronen I, Olman C, Kim S-G, Ugurbil K, Toth LJ. 2004. Spatial relationship between neuronal activity and BOLD functional MRI. Neuroimage. 21:876-885.
37. Klein B, Kuschinsky W, Schrock H, Vetterlein F. 1986. Interdependency of local capillary density, blood flow, and metabolism in rat brains. Am J Physiol. 251:H1333-H1340.
38. La Garza BHD, Muir ER, Li G, Shih Y-YI, Duong TQ. 2011. Blood oxygenation level-dependent (BOLD) functional MRI of visual stimulation in the rat retina at 11.7 T. NMR Biomed. 24:183-193.
39. Lau C, Zhou IY, Cheung MM, Chan KC, Wu EX. 2011. BOLD temporal dynamics of rat superior colliculus and lateral geniculate nucleus following short duration visual stimulation. PLoS One. 6:e18914.
40. Liu Z, He B. 2008. fMRI-EEG integrated cortical source imaging by use of time-variant spatial constraints. Neuroimage. 39:1198-1214.
41. Liu Z, 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.
42. Liu Z, Zhang N, Chen W, He B. 2009. Mapping the bilateral visual integration by EEG and fMRI. Neuroimage. 46:989-997.
43. Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A. 2001. Neurophysiological investigation of the basis of the fMRI signal. Nature. 412:150-157.
44. Lund RD, Land PW, Boles J. 1980. Normal and abnormal uncrossed retinotectal pathways in rats: an HRP study in adults. J Comp Neurol. 189:711-720.
45. Lund RD, Lund JS, Wise RP. 1974. The organization of the retinal projection to the dorsal lateral geniculate nucleus in pigmented and albino rats. J Comp Neurol. 158:383-403.
46. Maandag NJG, Coman D, Sanganahalli BG, Herman P, Smith AJ, Blumenfeld H, Shulman RG, Hyder F. 2007. Energetics of neuronal signaling and fMRI activity. Proc Natl Acad Sci USA. 104:20546-20551.
47. Madsen M. 1992. A simplified formulation of the gamma variate function. Phys Med Biol. 37:1597-1600.
48. Maeda M, Duelli R, Schrock H, Kuschinsky W. 1998. Autoradiographic determination of local cerebral blood flow and local cerebral glucose utilization during chemical stimulation of the nucleus tractus solitarii of anesthetized rats. J Auton Nerv Syst. 69:132-140.
49. Maggi CA, Meli A. 1986. Suitability of urethane anesthesia for physiopharmacological investigations in various systems. Part 1: general considerations. Experientia. 42:109-114.
50. Martin C, Martindale J, Berwick J, Mayhew J. 2006. Investigating neuralhemodynamic coupling and the hemodynamic response function in the awake rat. Neuroimage. 32:33-48.
51. Matsuura T, Kanno I. 2001. Quantitative and temporal relationship between local cerebral blood flow and neuronal activation induced by somatosensory stimulation in rats. Neurosci Res. 40:281-290.
52. Nemoto M, Sheth S, Guiou M, Pouratian N, Chen JW, Toga AW. 2004. Functional signal-and paradigm-dependent linear relationships between synaptic activity and hemodynamic responses in rat somatosensory cortex. J Neurosci. 24:3850-3861.
53. Niell CM, Stryker MP. 2008. Highly selective receptive fields in mouse visual cortex. J Neurosci. 28:7520-7536.
54. Ogawa S, Lee TM, Kay AR, Tank DW. 1990. Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc Natl Acad Sci USA. 87:9868-9872.
55. Ohki K, Chung S, Ch'ng YH, Kara P, Reid RC. 2005. Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex. Nature. 433:597-603.
56. Ostwald D, Porcaro C, Bagshaw AP. 2010. An information theoretic approach to EEG-fMRI integration of visually evoked responses. Neuroimage. 49:498-516.
57. Pawela CP, Hudetz AG, Ward BD, Schulte ML, Li R, Kao DS, Mauck MC, Cho YR, Neitz J, Hyde JS. 2008. Modeling of region-specific fMRI BOLD neurovascular response functions in rat brain reveals residual differences that correlate with the differences in regional evoked potentials. Neuroimage. 41:525-534.
58. Paxinos G, Watson C. 1998. The rat brain in stereotaxic coordinates. San Diego (CA): Academic Press.
59. Prusky GT, Harker KT, Douglas RM, Whishaw IQ. 2002. Variation in visual acuity within pigmented, and between pigmented and albino rat strains. Behav Brain Res. 136:339-348.
60. Sanganahalli BG, Herman P, Blumenfeld H, Hyder F. 2009a. fMRI and electrophysiological studies with a-chloralose and domitor anesthesia. J Cereb Blood Flow Metab. 29:S616
61. Sanganahalli BG, Herman P, Blumenfeld H, Hyder F. 2010. BOLD impulse response functions and baseline-dependent response adaptation. Proc Int Soc Magn Reson Med. 18:184.
62. Sanganahalli BG, Bailey CJ, Herman P, Hyder F. 2009. Tactile and nontactile sensory paradigms for fMRI and neurophysiologic studies in rodents. Methods Mol Biol. 489:213-242.
63. Sanganahalli BG, Herman P, Blumenfeld H, Hyder F. 2009b. Oxidative neuroenergetics in event-related paradigms. J Neurosci. 29:1707-1718.
64. Sanganahalli BG, Herman P, Hyder F. 2008. Frequency-dependent tactile responses in rat brain measured by functional MRI. NMR Biomed. 21:410-416.
65. Sceniak MP, Maciver MB. 2006. Cellular actions of urethane on rat visual cortical neurons in vitro. J Neurophysiol. 95:3865-3874.
66. Sefton AJ, Dreher B, Harvey A. 2004. Visual system. In: Paxinos G, editor. The rat nervous system. Amsterdam: Elsevier Academic Press. p. 1083-1165.
67. Sherman SM. 2005. Thalamic relays and cortical functioning. Prog Brain Res. 149:107-126.
68. Sheth SA, Nemoto M, Guiou M, Walker M, Pouratian N, Toga AW. 2004. Linear and nonlinear relationships between neuronal activity, oxygen metabolism, and hemodynamic responses. Neuron. 42:347-355.
69. Smith AJ, Blumenfeld H, Behar KL, Rothman DL, Shulman RG, Hyder F. 2002. Cerebral energetics and spiking frequency: the neurophysiological basis of fMRI. Proc Natl Acad Sci USA. 99:10765-10770.
70. Stark E, Abeles M. 2007. Predicting movement from multiunit activity. J Neurosci. 27:8387-8394.
71. Ueki M, Linn F, Hossmann KA. 1988. Functional activation of cerebral blood flow and metabolism before and after global ischemia of rat brain. J Cereb Blood Flow Metab. 8:486-494.
72. Ueki M, Mies G, Hossmann KA. 1992. Effect of alpha-chloralose, halothane, pentobarbital and nitrous oxide anesthesia on metabolic coupling in somatosensory cortex of rat. Acta Anaesthesiol Scand. 36:318-322.
73. Ureshi M, Matsuura T, Kanno I. 2004. Stimulus frequency dependence of the linear relationship between local cerebral blood flow and field potential evoked by activation of rat somatosensory cortex. Neurosci Res. 48:147-153.
74. van Camp N, Verhoye M, de Zeeuw CI, van der Linden A. 2006. Light stimulus frequency dependence of activity in the rat visual system as studied with high-resolution BOLD fMRI. J Neurophysiol. 95:3164-3170.
75. van der Linden A, van Camp N, Ramos-Cabrer P, Hoehn M. 2007. Current status of functional MRI on small animals: application to physiology, pathophysiology, and cognition. NMR Biomed. 20:522-545.
76. Vazquez AL, Noll DC. 1998. Nonlinear aspects of the BOLD response in functional MRI. Neuroimage. 7:108-118.
77. Yang X, Renken R, Hyder F, Siddeek M, Greer CA, Shepherd GM, Shulman RG. 1998. Dynamic mapping at the laminar level of odorelicited responses in rat olfactory bulb by functional MRI. Proc Natl Acad Sci USA. 95:7715-7720.
78. Zhang N, Liu Z, He B, Chen W. 2008. Noninvasive study of neurovascular coupling during graded neuronal suppression. J Cereb Blood Flow Metab. 28:280-290.