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An Introduction to Functional MRI
Bruce Pike
McConnell Brain Imaging Centre
Montreal Neurological Institute McGill University
B. Pike, MNI 2
Outline • MRI review (4 slide crash course) • fMRI overview
– basic premise – experimental design and analysis
• BOLD fMRI physiology – biophysical basis – CBF, CBV, and CMRO2
• fMRI Experiment Designs – block, event, phase, resting state
• BOLD fMRI issues – spatial specificity – field strength – Noise – EPI artifacts
B. Pike, MNI 3
NMR
B0
external field B0
M M
x
y
z
B0
f = (42 x B0) MHz
Felix Bloch (1905-1983)
Edward Purcell (1912-1997)
1952 1952
B. Pike, MNI 4
Excitation and Relaxation excitation
M
x’
y’
z
RFTx
B0
relaxation
x
y
z
B0
T1 T2 (spin echo) T2* (gradient echo)
RFRx
B. Pike, MNI 5
MRI Scanner
Head Coil B1 [µT] x
y
Main Magnet B0 [T] z
Gradient coils Gx, Gy, Gz [mT/m]
main magnet (T) gradient coils (mT/m)
RF coils (µT)
Gradient amps RF amp Receiver
Computer
Display
• gradients vary the field strength with position • gradients encode location (i.e. produce image) • gradients make all the noise • EPI - echo planar imaging is a way to image fast
B. Pike, MNI 6
MRI Review
• based on the NMR phenomenon • static magnetic field and radio waves • image primarily water distribution • can select contrast weighting based on water
content (PD) and relaxation mechanisms (T1, T2, T2*)
Paul Lauterbur (1929-2007)
T1W T2W T2* W EPI PDW
2003
B. Pike, MNI 7
Functional MRI (fMRI) • indirect detection of neuronal activity
• BOLD: Blood Oxygenation Level Dependent – magnetic properties of hemoglobin
• deoxyhemoglobin is like a contrast agent
• dynamically monitor changes in [dHb] changes and correlate with tasks or stimuli
9
4
t value
Seiji Ogawa (1934 -)
B. Pike, MNI 8
Basic Premise of BOLD fMRI: Neurovascular Coupling
Buckner et al., 2002
neural activity
linearly transforms: spatial & temporal blur
BOLD fMRI signal
Hemodynamic Response Function (HRF)
B. Pike, MNI 9
neuronal activity
tissue energy demand
Glucose, O2 consumption
blood flow and volume
local dHb content of blood
local dHb-induced magnetic field disturbance
BOLD fMRI signal
neurovascular coupling
fMRI relevant physiological correlates
Activation Physiology & fMRI
B. Pike, MNI 10
Hemoglobin, Oxygenation, and MR Relaxation
Oxyhemoglobin χ ~ -0.3
B0
longer T2, T2*
↑ BOLD upon activation
Deoxyhemoglobin χ ~ 1.6
shorter T2,T2*
↓ BOLD at rest
oxyRBC deoxyRBC
Linus Pauling (1901-1994)
!
1954 1962
B. Pike, MNI 11
BOLD Contrast: deoxy-Hb Effects
• Hb compartmentalized in RBCs
• H20 motion – diffusion
• IV: D ~ 2 µm2/ms • EV: D ~ 1 µm2/ms
– exchange • IV: fast across erythrocytic membrane: τex < ~5ms • EV: slow across capillary wall: τex > ~500ms
• effects on MR signal – IV: T2 and T2* shortening – EV: T2 and T2* shortening
B. Pike, MNI 12
Total Steady-state BOLD Signal
• a weighted sum of extravascular (EV) and intravascular (IV) signals components
• relative contributions determined by the voxel architecture
BOLD = xtissue BOLDEV + xblood BOLDIV
Harrison 2002 50 µm
B. Pike, MNI 13
BOLD and Neuronal Activation
• metabolic response – ↑ Glc consumption – ↑ O2 consumption : ↑ dHb : ↓ BOLD
• steady-state hemodynamic response – ↑↑ cerebral blood flow (CBF) : ↓ dHb : ↑ BOLD – ↑ cerebral blood volume (CBV) : ↑ dHb : ↓ BOLD
x CMRO2 CBV CBF
∴ BOLD ∝
B. Pike, MNI 14
BOLD: Activation Physiology
O2!
MRI voxel at rest
O2!
MRI voxel upon activation
B. Pike, MNI 15
fMRI Experiment: Block Design
stimulus off
on
image acquisition
time
-2
2
6
14
10
t - value
correlation
0
time
voxel response
0 20 40 60 80 100 120 140 160 180
-1.5
0
3
4.5
Time [s]
ΔSi
gnal
[%]
1.5 predicted response
B. Pike, MNI 16
fMRI Experiment: Event-Related Design
-2
2
6
14
10
t - value
time
ROI
stimulus off
on
image acquisition
time
time
0 5 10 15 20 25 99 100 101 102 103 104 105
ΔSi
gnal
[%]
Time [s]
Average Time Course
stim
ulus
B. Pike, MNI 17
fMRI Experiment: Phase-Encoded Design
eccentricity
0! 50! 100! 150! 200! 250! 300! 350!810!
820!
830!
840!
850!
860!
870!
880!
890!
Time (s)!
Sign
al!
Time FFT
magnitude phase
• periodically varying stimulus – e.g. eccentricity and polar angle visual stimulation
• Fourier transform time series of images – activated regions show magnitude response at stimulus frequency – phase of response shows position within stimulus field
B. Pike, MNI 18
fMRI mapping of Primary Visual Cortex: Polar Angle
Resting State fMRI
B. Pike, MNI 19 Van den Heuvel, 2010
Independent Component Analysis (ICA)
image acquisition
B. Pike, MNI 20
BOLD fMRI Issues • Is the BOLD response magnitude linear?
– does 2 x BOLD signal mean 2 x neuronal activity?
• Is the BOLD response uniform? – does the relationship between activity and BOLD signal vary across
the brain or with stimulus?
• What do negative BOLD responses mean?
• Is BOLD a valid marker of neuronal activity in pathology?
• What is the spatial accuracy of the BOLD response?
B. Pike, MNI 21
Event-Related Design and Linearity
Birn et al, NeuroImage 2001
measured measured
linear linear
B. Pike, MNI 22
BOLD Signal Model is Nonlinear Deoxyhemoglobin Dilution Model
0 Δ CBF/CBF0!
M
ΔB
OLD
/BO
LD0!
CMRO2+!
CMRO2-!
0
Davis et al., 1998 Hoge et al., 1999.
B. Pike, MNI 23
Flow-Metabolism Coupling: V1 & M1
Hoge et al., PNAS 96: 9403-8, 1999. Hoge et al., MRM 42:849-63,1999.
N=12"
0
5
10
15
20
25
CM
RO
2 (%
incr
ease
)
0 10 20 30 40 50
CBF (% increase)
Slope = 0.51
Atkinson et al., Neuroimage,11:5 Sup 2, 2000.
0 10 20 30 40 50 60 70 0
5
10
15
20
25
30
35
Slope = 0.38 CM
RO
2 (%
incr
ease
) CBF (% increase)
N=30"Primary Visual Cortex Primary Motor Cortex
B. Pike, MNI 24
Negative BOLD Responses • ‘blood stealing’ vs neuronal inhibition
• various conditions are associated with inhibition and produce negative BOLD – partial visual field stimulation – unilateral fine motor tasks
• mirror movement suppression, manual dexterity
• paradigm – right hand pinch grip – low force (within 4-7% of MVC) – phasic (1Hz)
B. Pike, MNI 25
BOLD and CBF Responses
N = 8
2 3
6 5
0 1
4
- +
2 3
6 5
0 1
4
+ -
BOLD
L N = 1
CBF
L
0 20 40 60 80 100 120 -1
-0.5
0
0.5
1
1.5
ΔB
OLD
[%]
Time [s]
120 -40!
0 20 40 60 80 100
ΔC
BF
[%]
Time [s]
-30!-20!-10!
0!10!20!30!40!50!60!
contralateral ipsilateral
Stefanovic et al., NeuroImage 2004
B. Pike, MNI 26
Activation and Deactivation CMRO2 - CBF Coupling
-40! -20! 0! 20! 40! 60! 80! 100!-40!
-30!
-20!
-10!
0!
10!
20!
30!
40!
50!
60!
ΔC
MR
O2 [
%]!
ΔCBF [%]!• maximal motor cortex BOLD: M ~ 7.2 ± 1.0 % • consistent coupling: ΔCMRO2 / ΔCBF ~ 0.44 ± 0.04
Stefanovic et al., NeuroImage 2004
N = 8
B. Pike, MNI 27
BOLD Spatial Specificity: Draining Veins
• factors – vascular architecture – spatial extent of neural activity
• rough calculations* based on mean vascular geometry
– distance of draining vessel showing full ΔY Aact ~ 100mm2 ⇒ dfull ~ 4.2mm Aact ~ 100mm2 ⇒ d0.25 ~ 25mm
*Turner, NeuroImage 2002
B. Pike, MNI 28
BOLD Spatial Specificity: GE vs SE
Vessel Radius [µm]
ΔR
2* [s
-1]
GE EV (TE = 40ms)
Vessel Radius [µm]
ΔR
2 [s-1
]
SE EV (TE = 100ms)
Buxton, 2002
B. Pike, MNI 29
Diffusion Effects on BOLD
field offset averaging by diffusion
Capillary Venule
dynamic narrowing
static dephasing
B. Pike, MNI 30
BOLD fMRI as a Function of B0
• greater susceptibility (BOLD) effect • greater extravascular ΔT2* / T2* • shorter optimal TE • ~ 2/3 of BOLD is IV @ 1.5 T • ~ 1/2 of BOLD is IV @ 3 T • ~ 1/4 of BOLD is IV @ 7 T
• improved activation localization and sensitivity
B. Pike, MNI 31
SNR Gains in fMRI at High B0: BOLD Signal Power Spectrum
Buxton, 2002
Frequency (Hz)
Pow
er
B. Pike, MNI 32 Triantafyllou, 2005
Practical fMRI SNR Gains
tSNR = fMRI times series SNR SNR0 = single image SNR
Phantom Human
B. Pike, MNI 33
EPI - Echo Planar Imaging
• fast imaging technique – typically acquire image in a single shot (~20-50ms) – trade off SNR and resolution for speed
• GE-EPI is most common BOLD sequence – geometric distortion in areas of magnetic field non-
uniformity – signal loss in areas of magnetic field non-uniformity – EPI acquisition details affect distortion and signal loss
B. Pike, MNI 34
fMRI GE-EPI Bandwidth
410 µs (2.4 kHz)
660 µs (1.5 kHz)
1250 µs (0.8 kHz)
decreasing EPI readout times (increasing bandwidth)
GE-EPI 4x4x4mm voxels 64x64 matrix TE = 40 ms
B. Pike, MNI 35
fMRI GE-EPI Echo Time
decreasing TE (decreasing BOLD sensitivity)
GE-EPI 4x4x4mm voxels 64x64 matrix 410 µs (2.4 kHz BW)
TE = 60 ms
TE = 40 ms
TE = 20 ms
B. Pike, MNI 36
8 mm
6 mm
4 mm
decreasing slice thickness
fMRI GE-EPI Slice Thickness
GE-EPI 4x4 mm voxels 64x64 matrix 410 µs (2.4 kHz BW)
B. Pike, MNI 37
Conclusion • fMRI detects physiological correlates of neuronal
activation
• BOLD – BOLD ∝ [dHb]
• [dHb] = f(CBF, CBV, CMRO2 and vascular anatomy) – valid marker of neuronal activity under normal physiological
conditions • V1, M1, activation, deactivation
– more complex for pathological states (e.g. stroke) – spatial specificity
• IV & EV components • improves with SE & field strength
– SNR increases with field strength • physiological noise limits
– EPI artifacts • acquisitions require optimization
Rick Hoge
Bojana Stefanovic Jan Warnking Jeff Atkinson
Karin Rylander Karma Advani Claire Cohalan Eva Alonso-Ortiz
Ilana Leppert Mike Ferreira Keith Worsley
Jean Chen Clarisse Mark
Eva Ortiz
CIHR NSERC FRSQ CFI
Acknowledgements
END
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