Dieter

R. Enzmann,

Brain with Brain was

MD

#{149} Norbert

motion

during

the cardiac

prospectively

cycle

(diencephalon,

cerebellar

brain

stem,

shortly after carotid systole, with concurrent cephalic motion of the major cerebral lobes and posterior cerebellar hemisphere. Peak brain displacement was in the range of 0.1-0.5 mm for all the structures

sils,

tonsils)

except

the

cerebellar

ton-

which

had greater displacement (0.4 mm ± 0.16 [mean ± standard error of mean]). Caudal motion of the central structures did not occur simultaneously but progressed in a caudal-to-rostral and posterior-toanterior sequence, being seen first in the cerebellar tonsils and then later in the diencephalon (hypothalamus). Caudal motion of the low brain stem and cerebellar tonsil was simultaneous with caudal motion of cerebrospinal

fluid

in the

cervical

noid space. Oscillatory aqueduct was delayed brain stem motion.

T

terms:

Brain

stem,

pulse nities

and

cerebrospinal

logic

cardiac

cycle

correlated with cal symptomatology brain itself was effort to explain ability to study

been

reach

methods. during

studied

the

and

a possible link to clini(1). Motion of the hypothesized in an CSF motion (2,3). The brain motion with MR

imaging techniques was first shown by Feinberg and Mark, who demonstrated caudal motion of the dien-

cephalon and brain stern during cardiac systole (4). A variety of MR imaging techniques have been used to study brain motion; all of them offered improved quanlitation of brain motion (4,5). The development of cine

fluid,

From the Department of Radiology, Rm 5-072, Stanford University School of Medicine, 300 Pasteur Dr. Stanford, CA 94305-5105. Received April 3, 1992; revision requested May 29; revision received June 26; accepted July 6. Ad-

to D.R.E.

RSNA, 1992 See also the article by Poncelet et al (pp 651) and editorial by Feinberg (pp 630-632) this issue. e

645in

trigger.

between period, pendent

data

Be-

relationship

the sequences and the cardiac the entire cycle is sampled indeof variations in heart rate. The

collected

within

each cardiac

cycle

and with each velocity sensitivity are interpolated into 16 frames in the cardiac cycle. If the number of interpolated lime frames is much larger than the number of repetitions of a particular sequence type within

each

cycle,

adjacent

time-frame

images will be correlated. The method is perhaps best described as retrospectively sorted cine with real-time selection of spatial phase encoding. The strength of the velocity sensitivity is operator-selected and parameterized by means of the encoding velocity the velocity that produces a phase shift of 180#{176} between the acquisitions. Stronger encoding (smaller Venc) produces improved pre-

cision

for measuring

motions.

In the

images.

MR

imaging

(6-8)

during

the

cardiac

has

to charthe carits rela-

cycle.

present

slow

tion

contrast

further improved our ability actenze brain motion during diac cycle and demonstrate

MATERIALS

AND

This

study

prospective a 1.5-T

imager

cine

was

(Signa;

Milwaukee)

contrast

METHODS

by

MR pulse

this sequence, two quisitions interrogating

performed

GE using

Medical a phase-

sequence

(7). In

gradient-echo the same

cine acsection

but with different sensitivity to velocity in a selected direction are interleaved. As a result of the differential velocity sensitiv-

1992; 185:653-660

to the

tionship to CSF flow (9,10). This study was designed to measure brain mo-

phase

flow in the compared with

MR.

subsequent

of this asynchronous

a low V,,. of 2 cm/sec was selected so as to be sensitive to the slow velocity of brain motion. From the data, two images are produced for each point in the cardiac cycle. Images proportional to the magnitude of the transverse magnetization in each pixel (magnitude images) have the same appearance as conventional gradient-echo

Systems,

requests

has

physiothe

cause

shift

I

reprint

(CSF)

outside

of previous investigatory Motion of the spinal cord

ity,

dress

fluid

characteristics

subarach-

Brain, MR, 13.1214, 15.1214 146.1214 #{149} Cerebrospinal flow dynamics, 16.91 #{149}Hypothalamus, 144.1214 #{149} Magnetic resonance (MR), cine study . Spinal cord, MR, 341.1214

Radiology

initiated

of motion-sensi-

tive magnetic resonance (MR) sequences has offered opportuto study aspects of brain motion

with

Index

Imaging’

development

HE

in 10

healthy volunteers by using a phasecontrast cine magnetic resonance (MR) pulse sequence. The major cerebral lobes, diencephalon, brain stem, cerebellum, cerebellar tonsils, and spinal cord were studied. The overall pattern of brain motion showed caudal motion of the central and

ScD

Motion: Measurement Phase-Contrast MR

measured

structures

J. Pelc,

moving

spins

phase

proportional

lected

direction.

acquire

an

incremental

to velocity

in the Se-

Pulse sequence repetitions are executed continuously and at a constant rate so as to maintain an MR steady state. Sequence repetitions initiated within the same cardiac cycle employ the same spatial phaseencoding gradient and alternating velocity sensitivity. The phase-encoding amplitude is updated

and

this

at detection

new

value

of a cardiac

is used

trigger,

for sequences

study,

Images in each

proportional pixel

due

to the to the

phase

differential

velocity encoding (velocity images) are proportional to velocity in the ± V,,,. range. Any motions not synchronous with the cardiac cycle produce blurring and artifacts,

as in conventional

interleaved

MR

acquisition

two velocity

imaging.

of data

sensitivities

The

with

the

minimizes

mis-

registration errors due to other motions (eg, respiration). Interleaving, however,

yields

a temporal

mately

twice

For this study,

resolution

the

sequence

the technical

approxirepetition

time.

parameters

were repetition time, 54 msec (single section), yielding temporal resolution of 108 msec; echo time, 9-17 msec; matrix, 128 x 256; section thickness, 5 mm; two signals averaged; field of view (FOV), 12-24 cm.

Abbreviations: CSF = cerebrospinal FOV = field of view, RO! = region venc

=

encoding

fluid,

of interest,

velocity.

653

b.

a.

C.

Figure 1. (a) Sagittal magnitude image (50/ 16.5; FOV, 24 cm) shows the ROIs for the frontal and posterior cerebellar regions.

a,) Coronal 24 cm)

and

magnitude

shows

the

ROIs

diencephalon

magnitude

occipital 17; FOV,

men brain

lobe

FOV,

(c) Axial 16 cm)

per-

to the aqueduct shows ROIs for brain stem (pons), aqueduct, and

magnum stem

shows (medulla)

magnitude

at the

upper

FOV,

parietal

(50/17;

lobe. (d) Axial 16 cm) obtained

(e) Axial cm)

(50/16.5;

the

(hypothalamus).

image

pendicular the upper

image for

C-2

level

cervical

magnitude image just above the

the ROIs and image shows

(50/ fora-

for the low

cerebellar tonsil. (50/17; FOV, 16 the ROI for the

cord.

e.

d.

The acquired

raw data

were

interpolated

with

to produce 16 frames equally spaced in the cardiac cycle. Imaging was performed at several anatomic sites: 1. Coronal imaging (FOV, 24 cm) through the hypothalamus. This showed the diencephalon and parietal lobes. 2. Sagittal imaging (FOV, 24 cm) in the midline. This showed the frontal lobes, diencephalon, mesencephalon, pons, me-

dulla,

upper

cervical

cord,

sils, and cerebellar vermis. CSF flow in the aqueduct, and subarachnoid space. 3. Oblique

axial

imaging

cerebellar

ton-

It also fourth

showed ventricle,

(FOV,

16 cm)

5. Axial imaging

(FOV,

16 cm) at the C-2

to C-3 level for cord motion and CSF motion in the subarachnoid space. For all of these images, motion encoding was in the superior-inferior direction. These measurements were performed in 10 healthy volunteers, six men aged 26-36 years and four women aged 23-34 years.

In four subjects

additional

coronal

images

were obtained with right-left motion encoding. In three other subjects additional sagittal images were obtained with anterior-posterior encoding. Peripheral gating

654

#{149} Radiology

relative in this

timing study.

on

measurements The cardiac

defined by means pulse, and the percentage

cycle relative

a finger

in all cases. Peripheral gatto be acceptable for the

fore,

envisioned was, there-

cycle

of the peripheral of the cardiac

to the onset

was defined

by

means of the finger pulse. This places the onset of carotid systole approximately 62% through the cycle. Phase-contrast cine MR imaging pro-

duces

images

function rors

through the mesencephalon and aqueduct at the incisura. This showed mesencephalon motion in addition to CSF flow in the aqueduct and incisura. 4. Axial imaging (FOV, 16 cm) at the level of the cerebellar tonsils and medulla.

a photoplethysmograph

was employed ing was judged

that represent

of time

(baseline)

the

effects

rents,

as a

Additive

er-

may

be

present

because

of gradient-induced

but with

must

velocity

in the cycle.

be

eddy

the technique,

similar

these

in neighboring

velocity

errors

regions

and constant over the motion baseline for each brain region was estimated by measuring

of the apparent

of

cur-

cycle. A investigated the average

cle. The tegrated placement) cycle cardiac

movement profile.

We

of the found

brain the

and not displacement

graphs

(Figs

2-4)

easier

than

velocity

note that “velocity” velocity slightly locity)

represents

(low

signal

systole

in the

above

For this investigation, the

brain

culated

structure

from

Displacement as the product after baseline of one of the

regions

(Fig 1).

displacement

in millimeters

the measured

rewere

velocity

of was

cal-

data.

for one frame is calculated of velocity measurement subtraction and the duration 16 frames of the cardiac cy-

5-8),

(Fig 2). (high signal and

intenblack

represents

degree

of “whiteness”

is directly

proportional to yewith a V. of 2 cm,

example,

black refers

white

is 2 cm/sec

is -2 to the

cm/sec. onset

(ie, high signal of interest. were

motion

ye-

intensity)

brightest

ROIs

to

images are and since the

displacement are offset displacement after peak will be a difference between

The For

its velocity

to understand

caudal

“blackness”

graphed, physical

It is important

and images images, white

sity)

zero velocity. performed

graphs.

and (peak there

darkest

was

the phase-contrast images (Figs

the graphs On the

the

is indis-

of the

in the

locity.

With this as a baseline, (ROl) measurements

frame (total

eral trigger. Displacement since our interest was

motion.

in that structure

in each brain motion the beginning

as a function of time throughout the cycle, as defined from the periph-

throughout the cycle. Since vascular structures were excluded and since there is no net brain motion, this average represents gion-of-interest

displacement to yield from

intensity) 0.4-1

.0 cm2

cranial and

and

the

The term CSF of caudal motion in the CSF space for

brain

motion

measurements (Fig 1). Hypothalamic and parietal lobe measurements were made on coronal images. Brain stem, occipital, and

cerebellar on axial cerebellum

tonsil images.

measurements Frontal lobe

measurements

and

were

were made posterior made

December

on

1992

50

50

% of

cardiac

cycle

% of cardiac

2.

cycle

3.

Figures

2, 3.

(2) Graph

shows

the

relationship

between

velocity

changes

and

physical

displacement

for

the

hypothalamus

in all 10 healthy

volunteers. The left y axis is displacement (in millimeters), and the right y axis is velocity (in millimeters per second). The change in velocity precedes the change in displacement by approximately 12% of the cardiac cycle. (3) Graph shows mean brain displacement (in millimeters) as a function of time in the cardiac cycle (percentage of cardiac cycle). Downward deflection of the curve represents caudal motion; upward deflection is cephalic motion. These curves are of the mean physical displacement in all 10 healthy volunteers, while the accompanying images (Figs 5-8,

11) show

velocity

in the

same

individual

throughout.

Displacement

is relative;

zero

represents

the

location

of brain

structures

at the

onset

of the cardiac cycle as defined by means of the peripheral trigger. Shown are the curves for the cerebellar tonsils (TONSILS), medulla (BSTEMLO), mesencephalon (BSTEM-HI), and posterior cerebellum (Post-CBL). These curves show downward displacement (descending curve) of the brain stem (BSTEM-HI and BSTEM-LO), with concomitant upward displacement (ascending curve) of the posterior cerebellum during carotid systole,

which

(69%)

occurs

before

62%

does

of the

cardiac

(75%)

cycle

(vertical

dashed

line).

The

cerebellar

-.-.-.---

-0---

tonsils

exhibit

downward

displacement

(see Figs 5, 9).

liters) displaced that frame. The

through the ROl during sum of this quantity over in which it is positive is an esti-

HYPOTH FRONTAL PARIETAL OCCIPITAL

-#{149}-

E E

at approximately (BSTEM-HI)

the midbrain

all frames mate of the volume (milliliters) displaced in one direction through the ROl. A similar sum formed.

value

over The

negative values can be perlesser of the two in absolute

represents

the net volume

that is

displaced in a reciprocating or oscillatory fashion through the ROI over one cycle (in milliliters per cycle, or milliliters per minute if multiplied by the heart rate). CAUDAL

25

0

50

75

% of cardiac

In the aqueduct, both the oscillatory flow volume and average (net) CSF flow rates were measured. The area of mea-

100

cycle

surement ranged from 7.8 to 13.6 mm2 and was composed of at least 10 pixels. The

Figure 4. Graph shows the mean brain displacement (in millimeters) in the supratentorial space including the hypothalamus (HYPOTH) and each of the major cerebral lobes (frontal, panetal,

flow measurement contains

and occipital) as a function of time in the cardiac cycle (percentage of cardiac cycle). The hypothalamus shows a pattern of brain molion similar to that of the mesencephalon (BSTEM-H1 in Fig 3), with the onset of caudal displacement at 75% of the cardiac cycle. The major phalic

cerebral direction

lobes show concurrent during systole.

opposite

motion

in the

both

mesencephalic

mian

cluded

the 16 points

in the cardiac

cycle.

The ex-

ception is Figure 9, which shows the displacement in one individual to match the images in Figure 8. Measurements for aqueductal CSF flow

and tissue

displacement

were

obtained

through the incisura. For each pixel and each of the 16 time frames, the product of

the velocity is an

in the pixel

estimate

(milliliters

Volume

of the

per

volume

minute)

flow

through

flow rate as a function

through CSF spaces sum of the volume

Volume

and the pixel area

185

rate

the

pixel.

of time

was measured as the flow rates through the

#{149} Number

3

pixels

within

frame.

The sections

a defined

ROI

were

they were perpendicular and the C2-3 subarachnoid minimized partial volume

pixel size for these

so that

to the aqueduct space; this artifact. The

measurements

and

Blood from

and

and brain

this

of

cistern,

peri-

superior

ver-

tissue

sometimes

vessels

the incisura to motion

were

(ie, the mesthe superior always ex-

ROI.

RESULTS

for each

angulated

cistern,

cistern)

encephalon

ce-

due

CSF (interpeduncular

vermis).

sagittal images. Cord motion was measured on axial images. The graphs of brain displacement represent the mean displacement in all 10 volunteers for each of

through

components

was

0.62 x 1.25 mm. The average flow rate was determined by averaging the volume flow

rate throughout the cycle and was expressed in milliliters per minute, or in milliliters per cycle if divided by the heart rate. The accuracy of average volume flow rate measurements has been validated in vitro and in vivo (10-12). For a given ROI and for any frame, the product of volume flow rate (milliliters per minute) and the time interval between cine frames (minutes) is the volume (milli-

The overall pattern of brain motion showed caudal motion (high signal intensity) of the central structures, the diencephalon, and brain stem, with concurrent cephalic motion (low signal intensity) of the more peripheral regions, the major cerebral lobes, and posterior cerebellar hemisphere. The following structures had caudal displacement: the diencephalon (hypothalamus) (Figs 3, 5, 7), brain stem (medulla, pons, and mesencephalon) (Figs 4-6), and the cerebellar tonsils (Figs 4-6). The caudal velocity changes depicted in the phase-conRadiology

#{149} 655

a. Figure healthy trations

5. Series of 16 phase-contrast volunteer shows the systolic in this article were obtained

individuals. proportional

before

High signal intensity to the velocity. CSF

b. (A-P) throughout the cardiac cycle (defined by means of the finger pulse) of a structures. Velocity range was -2 to +2 cm/sec. All of the phase-contrast illus31), so the timing differences are true differences and not variations between

sagittal images (50/16.5) caudal motion of midline in the same person (aged

(white) systole

is caudal (ie, caudal

motion, motion

and low signal intensity (black) of CSF in the cervical subarachnoid

is cephalic space)

motion, with the signal is depicted in images

intensity and

M-P

CSF systole,

being

A-E. Just (ie, low signal

the cerebellar tonsil shows downward velocity (arrow in L), while CSF is still flowing in a cephalic direction frame (M), greater downward velocity is seen in the tonsil as well as in the medulla and pons. The CSF in the prepontine cistern is still flowing in a cephalic direction (arrow in M). In the next frame (N), brain stem and CSF motion is now consonant. Caudal displacement of the midline structures progresses from the tonsil to the medulla and pons, to the mesencephalon, and finally to the diencephalon (L-P and A) (see Fig 8). In these images the systolic cephalic motion of the occipital-parietal region is also evident by its low intensity on images M-P. The inhomogeneous intensity in the cervical subarachnoid space is caused by velocity aliasing because of the very low V,. This healthy intensity).

In the

next

individual shows bidirectional phalic flow posterior to the

trast

images

ment

preceded

changes

6%-12%

one cine

the

shown

of the

in the cervical subarachnoid This is a normal variation.

displace-

graphs

cycle,

of the

that

2). For example, showed the onset

caudal

at 62%

whereas

displacement

at 75%

(Figs

caudal

is,

of the was

the of

cycle,

brain

detected

placement

just

of the

major

preceded

2). The

coronal

left motion surable by using

brain our

motion in this flow-encoding

was

stem and multaneous

diencephalon but occurred

to-rostral cerebellar

sequence tonsils

all the cerebellar greater

above

of 0.1-0.15

structures

tonsils, displacement

which

except

mm

for

the

exhibited (0.40 ± 0.16

mm) during the cardiac cycle (Figs 5, 6; Table 1). In the infratentorial space, the posterior cerebellar hemisphere balanced the caudal motion of the brain stem by moving in the opposite direction, that is, cephalad (Fig 4, Table 2). In the supratentorial space the 656

#{149} Radiology

systole,

lobes

with

showed

The

range

of CSF

cerebral

images

encoding

and then accompanied CSF systole for subarachnoid CSF. The onset of CSF systole in the subarachnoid space differed for varying anatomic localions but matched local brain motion (vide infra). Peak brain displacement in the

end

downward motion of the diencephalon (hypothalamus) was balanced by an opposite, cephalic motion of the frontal, parietal, and occipital lobes during systole (Figs 3, 5). Mean dis-

ble

is defined as caudal then the accompanymotion

at the

of all healthy volunteers was less than 0.1 mm during the cardiac cycle (Ta-

2, 3).

If CSF systole motion of CSF, ing

by

16-image

hypothalamus

motion

space

with

caudal

flow

anterior

to the

cord

and

ce-

(B-E).

in the

cardiac

or two frames data set (Fig

flow cord

right-

no meadirection range.

spinal

mm/sec cord

The

± 2.0)

(5.7

caudal

and mm/sec

motion

upper

cervical

± 2.8).

of the brain

(Figs moved

nor velocity component showed a similar cephalic progression up the brain

peak velocities of brain structures were in the 1.1-1.5-mm/sec range except for those in the cerebellar tonsil

(4.7

timing of caudal displacement is illustrated in a healthy volunteer in Figure 8, and the displacement is graphed in Figure 9. The tonsil (and cord) may reverse direction before the brain stem and CSF. The brain stern exhibited some anterior motion that was measured with anterior-posterior motion flow encoding (Fig 8). The ante-

was not siin a caudal8, 9). The caudally first,

tole,

while

CSF

are

lion,

the

phalic

tonsil

rior

lower

brain

stem

just

cord

rnotion

was

the brain still

stem

moving

cord

direction

and

cervical

in a caudal

begins

moving

(Figs

8, 10).

direc-

in a ceThis

mo-

lion also occurs to a lesser degree in the cerebellar tonsil (Figs 8, 9). This opposing

pre-

ceded the reversal and caudal flow CSF (ie, CSF systole). This sequential

cervical

also evaluated in this study. In early CSF systole the cervical cord moves caudally in synchrony with the brain stem (Fig 8). The onset of caudal motion coincides with adjacent caudal CSF motion. Slightly later in CSF sys-

followed by caudal motion of the lower brain stem, then the upper brain stem, and finally the diencephalon (Figs 8, 9). Caudal motion of the and

stern.

Upper

of

type

ullary

motion

causes

some

and

a “flexion”

displacement of movement

junction

(Fig

poste-

at the cervicomed7 [A-D]). During December

1992

b.

a. 6.

Figure cm/sec.

Axial

Note

b). Motion space

the

images high

(50/17.3) signal

intensity

of these structures

is complex

because

show

the motion (ie, caudal

occupies

of velocity

of the medulla motion

of the

only a short portion aliasing

due

to the

very

and

cerebellar

medulla

and

of the cardiac low

during

to detect

the cardiac cycle. Velocity range was -2 to +2 [M in bJ) prior to the onset of CSF systole (N in The signal intensities in the premedullary subarachnoid

tonsils

cycle (M-O).

V,n#{231}used

a.

tonsils

cerebellar

brain

motion.

b.

Figure 7. Coronal images (50/16.5) depict brain motion (velocity) in the diencephalon during the cardiac cycle with a velocity range of -2 to +2 cm/sec. The caudal motion of the diencephalon is seen as high signal intensity in images M-P (b). At the onset of caudal motion of the diencephalon, suprasellar and third ventricular CSF shows cephalic motion (M). In the next frame suprasellar CSF has reversed to caudal flow (curved arrow in N), while CSF in the third ventricle is still in a cephalic direction, that is, of low signal intensity (straight arrow in N). Cephalic motion (low signal intensity) of the diencephalon is noted in late diastole (K-P and A-G).

late

systole,

can

be moving

anteriorly

the

is moving

while and

therefore, cord

posteriorly

Volume

185

(Figs #{149} Number

the

brain and

stem caudad

cephalad

7, 8). 3

Caudal

motion

of the

lower

stem and tonsils just preceded sal of cervical CSF flow in the le-to-systole transition. Caudal

brain reverdiastoflow

in

the cervical subarachnoid space appeared to be directly temporally related to caudal brain stem motion. The diastole-to-systole transition of Radiology

657

#{149}

a.

b.

Figure 8. nor-posterior

Comparison direction

of sagittal images (50/16.5) (E-H in b) in the transition and in the anterior-posterior

tion for images A-D systole. The progression

of caudal

of the brain stem in the superior-inferior direction (A-D in a) and in the anterange was -2 to +2 cm/sec. Flow encoding is in the superior-inferior direcdirection in images E-H during the same part of the cardiac cycle displayed here, the onset of is from the tonsil to the mesencephalon and diencephalon (A-D). Simultaneous with this is a small (low signal intensity) in the brain stem (E-H), which shows a similar progression from the medulla to

motion

shows systole.

motion Velocity

component of anteriorly directed motion the mesencephalon. Cord motion is first caudal and then cephalic during CSF systole Simultaneous with this is posterior motion of the cord (high signal intensity in F-H ment at the cervical medullary junction during CSF systole.

cardiac

% of

pattern

space

of motion

(low

signal

suggests

% of cardiac

intensity

a flexion

type

in B-D). of move-

cycle

10.

Figures

9, 10. 8. Caudal

Figure

(10)

This

cycle

9.

pons, pons

in the subarachnoid ).

(9) Graph

mesencephalon, and mesencephalon Mean

±

standard

dal displacement sal in the

shows

displacement

and

of the

at the onset

suprasellar, perirnesencephalic

first

hypothalamus late in systole

error

subarachnoid

displacement occurs

of midline in the

cerebellar

structures tonsil

(hypothal) (diencephalon). (94% of cycle). The tonsil

mean

of cord

of subarachnoid

displacement

space

as a function (69%

of cardiac

The returns and

and

tonsil and medulla to a zero displacement

(millimeters)

CSF systole

of the cardiac cycle),

in all healthy

cephalic

cycle

is followed actually move

position

persons

displacement

in the same

this

during

at the end

healthy

individual

depicted

in

by displacement in the medulla, in directions opposite those of the

at the beginning the

cardiac

of CSF systole

cycle.

of the cardiac The

preceding

cord

cycle.

shows

cau-

CSF flow

rever-

space.

interpeduncular, CSF

and related

was

to

diencephalic brain motion and was, therefore, slightly delayed in relation to spinal CSF flow. It was not uncommon to have a short period of bidirectional flow in the prepontine and suprasellar cistern. Because of the earlier caudal-anterior brain stem,

flow

could be briefly, dal and cephalic. intensity

tion

was

motion anterior

of the low to the pons

simultaneously This mixed not

of the brain

the mesencephalon tently earlier than

aliasing.

stem

stem

motion

Caudal

at the

was

at that initially

companied by cephalic motion in the aqueduct (Fig 11). This discrepancy was noted in the

658

Radiology

#{149}

mo-

level

of

was also consisthe onset of caudal

CSF flow in the aqueduct level (Figs 9, 11). Therefore, brain

causignal

same

caudal acof CSF same third

ventricle with (Fig 7). This group

a mean mean)

diencephalic of healthy

measured

subjects

had

(± standard error of the oscillatory CSF flow volume

through the aqueduct mm ± 0.34. The mean

error

motion

of the

mean) through

of 1.72 rnL/ (± standard

net CSF flow the aqueduct

as was

0.34 rn/mm ± .09, which was 22% ± 4 of the total oscillatory flow volume. Total brain tissue and CSF volume displacement through the incisura was 16.8 rnL/min ± 2.3. The aqueductal oscillatory CSF volume flow represented a mean (± SEM) of 12% ± 3 of this total incisura volume displacement. December

1992

locity of the brain stern cord were greater than major cerebral lobes. As Feinberg and Mark (4), in

the

magnitude

velocity)

of

of these

and spinal those of the noted by the difference

displacement

(or

structures

may

explained by the conservation mentum of these structures. A somewhat surprising

be of mo-

finding

was

the earlier caudal motion of the cerebellar tonsils and low brain stern cornpared with that of the high brain stem (rnesencephalon) and diencephalon (hypothalamus).

brain

This

motion

in the

provides

an

CSF

into

flow

most caudal tonsils, not has a greater

early

suggests

force

the

that

posterior

fossa

for

spinal

structure, only moves physical

directing

canal.

The

the cerebellar first but also displacement

than does the mesencephalon or diencephalon. The cephalic progression of caudal brain motion probably reflects the cephalic movement of the systolic

pressure

and

blood

volume

wave. The downward motion of the central brain structures occurs shortly after cardiac systole. Feinberg and Mark showed this to be approximately 270 msec after the R wave (4). In our own investigations of CSF flow in which difference

a measured was used

arteriovenous as a surrogate

for

brain brain with

expansion, caudal motion of the stern appeared simultaneous the rapidly increasing arteriove-

nous

blood

flow

approximately diac

cycle

difference

70% as defined

that

through with

occurs

the

car-

a periph-

eral

trigger (10). This timing is very to that defined by Feinberg and Mark in that this arteriovenous differclose

ence Figure volunteer.

11.

Two Shown

in the bottom

four

sets of four in the

top

images

consecutive

axial

four

(A-D)

(E-H),

images

the transition

images is the

from

(50/17.3) transition

diastole

obtained in the same healthy from systole to diastole, and

to systole.

Velocity

range

was

-2

to +2 cm/sec. These images show the out-of-phase nature of aqueductal CSF flow, subarachnoid space CSF flow, and brain stem motion (mesencephalon). In the transition from diastole to systole (F-H) downward motion of the mesencephalon and superior vermis is initially accompanied by persistent cephalic flow (very low signal intensity) of CSF in the aqueduct (F). CSF flow in the perimesencephalic cistern is mixed but predominantly cephalic initially (E), and then becomes more homogeneously caudal (F-H). Some of the persistent very low signal intensity represents veins with cephalic flow. In the transition from systole to diastole (A-D) persistent high signal intensity in the aqueduct indicated aqueductal caudal flow when the brain stem showed some cephalic motion, that is, low intensity (C). At this time, cephalic CSF flow (very low signal intensity) is present in the perimesencephalic cistern, while flow in the aqueduct is caudal (C).

DISCUSSION The observed overall pattern of brain motion is caudal motion of the deep central structures shortly after cardiac systole with concurrent, balancing cephalic motion of the more peripheral regions of the brain. In the posterior fossa, this caudal motion Volume

185

#{149} Number

3

was

exhibited

by

the

brain

stern

coincides

with

carotid

systole,

the early peak of which occurs approximately 200 rnsec after the R wave. Caudal motion of the upper

and

cerebellar tonsils while concurrent cephalic motion was seen in the posterior cerebellar hemispheres and vermis. In the supratentorial space the caudal motion was seen in the diencephalon, whereas cephalic motion was seen in the frontal, parietal, and occipital lobes. Displacement and ye-

brain

stem

preceded

the

maximum

CSF noid

velocity in the space (4,10,13).

cervical Axial

subarachand sagittal

views duct stern

of the mesencephalon show clearly that caudal motion precedes systolic

and aquebrain CSF

flow reversal in the aqueduct. Brain motion appears to be the driving force for CSF pulsation. The earlier motion and caudal displacement of posterior fossa structures (ie, cerebellar tonsils and brain stem) account for the earlier systolic caudal

flow of cervical CSF CSF in the aqueduct.

compared CSF flow

with in the

basal cisterns (suprasellar, interpeduncular, and perimesencephalic) seemed to be governed by diencephalic motion. Since diencephalic

caudal motion is delayed with tonsil motion, caudal

compared CSF flow

Radiology

#{149} 659

in the terns with neous seen systole.

prepontine and suprasellar ciswas also delayed compared spinal CSF systolic flow. Simultabidirectional flow could be in these areas in the transition to While causing the downward

velocity

of CSF,

the

cephalic

progres-

sion of both caudal and anterior brain stem velocity may cause a cephalic component to CSF flow that may be related to the ultimate slow bulk flow of CSF toward the convexities. Therefore, a type of upward “milking” aclion is caused by this cephalic progression of downward brain stem motion. The out-of-phase nature of brain stem motion and aqueductal flow relates to the site of motion causing the CSF flow. In the aqueduct, CSF flow is governed not by local brain motion but rather by cerebral hemisphere motion and its effect on the lateral

these two spaces accounts for the difference in the phase of oscillation in these CSF spaces. Motion of the upper cervical cord and cerebellar tonsils at the craniocervical junction exhibits some added complexity. Both of these structures in late systole can show reversal of motion (ie, cephalic) while CSF and/ or the upper brain stem are still moving caudad. The pattern is similar to that reported in healthy persons by Levy et al although they did not use a cine pulse sequence (1). Our measured peak systolic cord velocity was somewhat lower, 5.8 mm/sec ± 3.2 compared with 12.4 mm/sec (1). The

5.

cervicomedullary

9.

junction,

therefore,

cerebral hemisphere volume changes that are delayed in time compared with those of the posterior fossa (13). As an example, this delay is reflected in the time delay of the systolic pulse wave between the basilar artery and

undergoes some shear stress, since the brain stem and cord can be moving in opposite directions. This investigation used a very low motion-encoding velocity range of 2 cm/sec (compared with vascular applications), which improves the signal-to-noise ratio of the flow images. The measured CSF volume flow rates for aqueductal flow and movement of CSF and tissue through the incisura are not substantially different from those observed in another group of healthy subjects studied with a higher

the

velocity-encoding

ventricles.

CSF

the

foramen

are

similar

middle

at least

flow

characteristics

of Monro and

cerebral

12%

by

cardiac

means

aqueduct reflect

artery,

of the

determined

and

presumably

at

which

is

cycle

of blood

in the

Monro) in time

third

ventricle

(foramen

and aqueduct. The difference of arrival of the pulse wave

Radiology

#{149}

6.

1.

2.

Levy

7.

8.

10.

Di Chiro

G, McCullough

DC,

of

in

du Boulay GH, O’Connell J, Curie J, Bostick T, Verity P. Further investigation on pulsatile movements in the cerebrospinal fluid pathways. Acta Radiol Diagn 1972; 13:496-523. Feinberg DA, Mark AS. Human brain molion and cerebrospinal fluid circulation demonstrated with MR velocity imaging. Radiology 1987; 163:793-799.

Naylor

HD,

Riederer

SJ.

Society 1991.

Rapid

ResoAJ, MR im-

GL, Firmin

DN,

Longmore

DB.

Blood flow imaging by cine magnetic resonance. J Comput Assist Tomogr 1986; 10: 715-722. Enzmann DR. Pelc NJ. CSF in normal and syringomyelia patients using phase contrast cine MR (abstr). In: Book of abstracts: Society of Magnetic Resonance in Medicine 1989. Berkeley, Calif: Society of Magnetic Resonance in Medicine, 1989; 11. Pelc LR, Pelc NJ, Rayhill SC, et al. Arterial and venous blood flow: noninvasive quantitation with MR imaging. Radiology 1992; Rubin DL, Herfkens RJ, Pelc NJ, Jeffrey Measurement of portal blood flow in

abstracts: Medicine Magnetic 12.

14.

262.

3.

of abstracts:

aging of blood flow with a phase-sensitive, limited-flip-angle, gradient recalled pulse sequence: preliminary experience. Radiology 1990; 176:255-262. Pelc NJ, Herfkens RJ, Shimakawa A, Enzmann DR. Phase contrast cine magnetic resonance imaging. Magn Reson Q 1991; 7:229-254.

chronic dicting

et

al. Fixed spinal cord: diagnosis with MR imaging. Radiology 1988; 169:773-778. du Boulay GH. Pulsatile movements in the CSF pathways. BrJ Radiol 1966; 39:255-

In: Book

185:809-812.

11.

13. LM,

(abstr).

of Magnetic Resonance in Medicine Berkeley, Calif: Society of Magnetic nance in Medicine, 1991; 44. Spritzer CE, Pelc NJ, Lee JN, Evans Sostman

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4.

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phy

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CSF

rifle

1992