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Distribution of cerebral blood flow in the dominant hemisphere during motor ideation and motor performance.

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Distribution of Cerebral Blood Flow in
the Dominant Hemisphere During Motor
Ideation and Motor Performance
David H. Ingvar, MI), and Lars Philipson, MSci
Distribution of activity in the dominant (left) hemisphere was studied with a multidetector instrument during
diagnostic measurements of regional cerebral blood flow in 6 patients, 4 of them neurologically normal. Computercalculated charts, in color, of the flow/activity distribution-“cerebral ideograms”-were obtained in three situations: at rest, during motor ideation (attempts to conceive of rhythmic clenching movements of the right hand), and
during actual movements of the right hand. Motor ideation changed the normal “hyperfrontal” resting flow
distribution, and an increase of the hemisphere mean flow was recorded. T h e increase was especially marked in
frontal and temporal structures. This pattern differed from the one during actual hand movements, when a rolandic
flow increase was seen. T h e result suggests that centers for motor ideation have a different cerebral location than
those which control the actual hand movement.
Ingvar DH, Philipson L: Distribution of cerebral blood flow in the dominant hemisphere during motor
ideation and motor performance. A n n Neurol 2:230-237, 1977
Neurophysiological investigations of volition have
mainly used two methods. First, microelectrode
studies of single neurons in the cerebral cortex and in
motor pathways in monkeys have shown unit discharge patterns that correlate with peripheral motor
events of intentional character [ 5 , 6, 321. Second,
evoked potential studies, especially of the contingent
negative variation response and the so-called readiness motor potential, have demonstrated characteristic features, not only during voluntary movements,
but also preceding them [ l , 3, 25, 34, 351.
I n general, however, only fragmentary knowledge
exists about the behavior of larger aggregates of brain
neurons, and still less is known about the behavior
of whole cortical fields during and preceding voluntary motor activity. This appears t o be d u e mainly t o
lack of adequate methods. Microtechniques are unsuitable for such studies. Furthermore, changes in
evoked potentials are difficult to relate to distinct
brain regions, as are electroencephalographic alterations during voluntary movemcnts [2, 221.
In the present investigation we used xenon 133 to
measure regional cerebral blood flow (rCBF) with a
multidetector device 1261 in order to analyze the
events that accompany motor ideation (i.e., attempts
to conceive of a movement without carrying it out;
and t o compare this situation with the rolandic flow
changes induced by actual hand movements 1291. We
have recently confirmed Olesen’s [29] original obserFrom rhc Departinelit of Clinical Ncurophysiology, University
Hospital, Lund, Sweden.
Accepted for publication Apr 5 , 1977
230
vation of this rolandic flow increase in o u r laboratory
and further analyzed its distribution [12, 131.
In this paper we also present a new technique of
displaying two-dimensional color diagrams of the
mean flow distribution in a group of subjects w h o
underwent rCBF measurements. W e have termed
such graphic displays “cerebral ideograms” [4, 131.
Materials and Methods
Patient Material
Six patients were studied. Four of them were neurologically
normal, right-handed, male psychiatric patients without a
history o f organic brain disorder, head injury, epilepsy, or
similar abnormalities. None was taking any medication of
importance. The clinical diagnoses were chronic schizophrenia (in an inactive state) in 2 patients (22 and 30 years
old) [7]and suspected presenile dementia in the other 2
(45 and 48 years old) [lo]. The 2 older patients showed
slight psychometric defects. The Table summarizes basic
data concerning these 4 patients.
The measurements of rCBF were made for diagnostic
purposes with the patients’ informed consent. Elsewhere we
have dealt i n detail with the selection ofpsychiatric patients
for cerebral blood flow measurements as well as with the
important ethical questions that must be considered 17, 101.
rCBF measurements by the intraarterial technique carry
almost no risk i n patients without evidence of gross inrracranial disease [ 151. During diagnostic rCBF procedures in
our laboratory, various forms of activation are routinely
carried out, including voluntary hand movements. The
Address reprint requests to Dr I n g a r , Department of Clinical
Neurophysiology, Univrrsity Hospital, S-22 1 85 Lund. Sweden.
present study required an extra xenon injection during
motor ideation, which added n o further risk to the patient.
Two additional patients (male 2 I , female 25 years) were
studied by an identical procedure to that used for the 4
psychiatric patients. They were not included in the main
analysis since they suffered from therapy-resistant focal cortical epilepsy and showed moderate EEG slowing as well as
focal paroxysmal disturbances in the left temporal region.
rCBF measurements were done in these 2 patients in an
attempt to identify a possible hyperemic region in the cortex
corresponding to the epileptogenic focus. As shown by
Hougaard et a1 (see [13J), rCBF studies in focal cortical
epilepsy can be valuable in identifying the extent and intensity of the cortical focus.
In the present context the 2 epileptics as well as the 4
psychiatric patients all can be considered as having a normal
mental state at the time of the examination. A good contact
was obtained, and cooperation was highly satisfactory in all
cases.
Measurement Proredu re
The rCBF was measured simultaneously with 32 detectors
in accordance with a previously described technique [26,
3 11. Briefly, 2 to 4 ml of saline in which 3 to 5 mCi of ‘“:’Xe
had been dissolved was injected into the internal carotid
artery via a thin polyethylene catheter on the left side. The
uptake and subsequent clearance of the isotope were recorded by the detectors placed at the side of the patient’s
head. By means of a small computer, flow values were
calculated from each region. From the first minutes of
clearance an “initial flow” value (finit) was calculated. The
10-minute flow value (fl0)was obtained by the height over
area method. Flow in the gray and white matter (f, and f,,,)
were obtained by biexponential analysis of the clearance
curves. The relative weight of the gray matter (g F)was
also obtained by exponential analysis. In the following discussion only rCBF values determined by flow in the gray
matter (finit, fs, and flo) are considered.
The cerebral ideograms are based on finitvalues. It has
been shown that this indicator of rCBF is the most reliable
one to use for studies of rCBF changes related to mentation
[121.
Datu Processing
In the present study we used a new type of display technique, in color, developed by one of us (L.P.), as an im-
provement over previously used manual techniques to display rCBF distribution in groups of patients [13, 161. A
common feature o f the present and previous techniques is
that they take the hemisphere mean finit flow at rest as a
reference. We did these studies using a unique hard-copy
color display system with ink jets, including its software
system, available at Lund University Computing Center [ 1 1,
23,24, 331.
In calculating mean flow distribution in our 6 patients,
three stages can be identified:
1. A smoothingprorerlur.Relative flow values are entered
onto a matrix that contains several hundred positions having
a fixed relation to a standard contour o f t h e hemisphere (Fig
I). Since the position of the detectors varies from case to
case, the values from a series of patients are distributed
throughout the matrix. If two or more values fall in the same
position, a mean value is entered. T h e matrix is used as an
input for the smoothing procedure, in which each element is
equalized to a weighted sum of the values in the immediate
vicinity. In this way, empty elements in the input matrix are
given values so that the output matrix is completely filled.
2. Color coding. This is based upon isarithm technique of a
type used for topographic maps, in which each level has its
own color. The isarithms are calculated with much greater
spatial accuracy than the matrix elements by using twodimensional interpolation. By means of the special color jet
software, the data necessary to control the ink jet plotter are
then edited and stored on magnetic tape. The hemisphere
contour, color scale, and headlines are also included.
3. Color plotting. U p to this, point the procedure is performed by a Univac I108 computer and requites about 1
minute of central processing unit time. The actual plotting
is then made off-line by a special plotter using three electronically controlled ink jets containing yellow, red, and
blue ink, respectively. The spatial resolution with this
technique is 0.2 mm, and the whole plot takes about 60
seconds using the data on the magnetic tape.
Meaurement Procedure
All 6 patients were examined by a uniform procedure. Prior
to the rCBF study the measuring technique was explained to
the patient in general terms, and in the introductory phase a
highly reassuring attitude was attempted so that good
psychological rapport was obtained. In order to avoid
Ingvar and Philipson: Cerebral Blood Flow during Motor Ideation and Performance
231
F ig 1 Matrixforcerebralideogra~zsused in thefirst step ojiomputer calculationsforplotting the color diagrams shown
in Figure 2. Relative f l o . ~ itdues
,
(in perrentage of m e m
~5’ourouliin t h e indizmidual heniisphereJ)from .tinglestudies
in different patients art7 introduced in positiovs
i-ori-espondingto the centers of /he dcjelector fields and
related t o dn acerage iontour of the left hemisphere. The
wxt step ii the aitual smoothing procedure, u.hm the
diffrrenies between neighboring elements of the matrix are
ionsiderahlj reduced and empt? elements jlled out uiith
appropriate v a h u (see text)
I
habituation effects, however, the various phases in the
procedure were not described in detail.
At first, a resting mea~zrrementwas made (situation A in the
Table). This was carried out about 10 to 20 minutes following the carotid artery puncture, when the immediate effects
of the catheter insertion had worn off. Complete silence was
attempted in the laboratory, and the patient had a pad placed
over his eyes. He was not aware of the moment of the
isotope injection, and during the whole clearance period he
was neither spoken to nor touched intentionally [121.
During the second measurement, “hand moz’ement.r conreizsed” (situation B), the patient was briefly instructed to
concentrate on imagining a slow, rhythmic clenching
movement of the right hand. The movement was demonstrated verbally and visibly to him for 10 to 1 5 seconds,
during which the eye pad was removed. A brief attempt was
then made to let the patient imagine the movement. This
was followed by a 10-to 30-second rest. Then afew renewed
verbal suggestions were given to the patient to imagine that
he was clenching his right fist with a slow rhythm. During
this period, a second isotope injection was made without the
patient being aware of the exact moment of the injection.
During the actual flow measurement, however, verbal reminders of the type “open-clench, open-clench” were given
by the examiner in a soft’voice five or six rimes during the
first few minutes of the clearance period, which lasted 15
minutes total. All patients confirmed with a small nod or a
soft “yes” that they were able to imagine thc movement
demonstrated to them. The hand under study (right) was
observed continuously by the examiner during this phase,
but in no case could any movements be discerned. Three of
the patients rcportcd afterward that it had been difficult to
imagine the hand movement.
Finally, a third flow measurement was carried out during
rhythmic nzoiwnents v/&e right hand (situation C ) [29], the
232
Annals of Neurology
Vol 2
No 3
patient being asked to squeeze a small rubber balloon
rhythmically.
I n 2 of the 4 neurologir-ally normal patients afinalrontrol
measurement was obtained, during general conversation
and during a reasoning test, respectively.
During all rCBF measurements the systolic blood pressure was checked, and arterial blood samples for measurement of Paco, were taken immediately following the
isotope injection and 3 minutes later. There were no complications from the rCBF measurements [ 151.
Results
Mean Hemisphere rCB F Measurements
The Table gives blood gas, blood pressure, and mean
hemisphere rCBF values in the 4 neurologically normal patients. The P C Odid
~ not change. As expected,
however, there was a slight (8 mm Hg) increase in
mean systolic blood pressure during the actual hand
movements [29].
The rCBF values at rest were normal [28].
There was a moderate increase in the mean gray matter blood flow (reflected in the finit,f,, and fl0values)
during ideation and motor activity (situations B and
September 1977
Cj, while f, and g $6 remained essentially unchanged.
This confirms that mental events mainly involve
functional changes within the gray matter [ 12, 3 11.
Regional Findings
The main results of the study are shownin Figure 2. At
rest (Fig 2A) a normal hemisphere finit ( 5 5 m1/100
gmimin) prevailed for the whole group. A normal flow
distribution of the hyperfrontal type was also seen,
with the highest flow values frontally 112, 13, 181. By
the scale at the right side of the figure, flow in many
regions in the premotor and frontal areas was 30 t o
35% above the hemisphere mean, and several postcentral regions, especially in temporal parts but also in
parietal and occipital regions, showed a correspondingly lower flow.
When the subjects attempted to conceive of a
rhythmic right hand movement (Fig 2B), aided by
verbal suggestions as described, a general flow increase amounting to about 7% occurred without any
alterations in PaCOz o r blood pressure. The increase
was most marked in premotor and frontal regions,
including the supraorbital parts. There was also an
increase of flow in postcentral-parietal areas as well as
in the sylvian and temporal regions, where flow, relative to the mean, increased from about minus 30 to
355X to plus 30 to 35%: in several regions.
When the patients moved their right hand rhythmically (Fig 2C), the rCBF pattern changed markedly
and the typical rolandic increase emerged. The peak
was localized at the vertex, where flow augmentations
of more than 50% were recorded (cf. Olesen [29]).
There was also a flow increase in postcentral and
parietal regions as well as a “ridge” of high flows
approximately following the rolandic fissure down the
side of the hemisphere. The flow recorded over frontal as well as in temporal regions was generally lower
in this phase than during motor ideation.
The three cerebral ideograms of Figure 2 show
white regions occipitally, an area not covered by the
detectors and thus not measured.
Figure 3 shows the rCBF changes in 1 of the neurologically normal psychiatric patients, a 49-year-old
man. Both flow distribution in relation to the hemisphere mean flow at rest and absolute flow distributions in situations B and C are shown in regional
distribution charts during rest, motor ideation, and
actual hand movements. Detector-detector comparison shows distinctly that motor ideation produced the
most marked relative flow increase in the temporal
region, where it amounted to 60 to 70% at several
points measured. The figure reemphasizes that the
flow increase in frontal and temporal regions was less
during actual hand movements than during motor
ideation.
In one of the two final control measurements, during conversation, a general flow increase of about
17% was recorded. In the other case the mean flow
hardly changed during a reasoning test. The pattern
observed during motor ideation was not seen in either
case.
The results in the 2 patients with focal cortical
epilepsy coincided fully with the findings in the 4
neurologically normal patients: there was a clear-cut
difference in rCBF values during rest, motor ideation,
and the actual motor act (Fig 4).
Discussion
The rCBF technique, including its use in clinical
studies, has been discussed elsewhere [26, 271. The
color display system, here used for the first time in a
clinical study, appears to have attractive properties for
the presentation of cerebral changes accompanying
motor and mental efforts. In the display system significant flow peaks in individual patients may be
smoothed out more or less completely; this risk is
greater when the number of patients is small. Adaptation of t h e data sets to a standard matrix within a
standard brain contour may also cause artifacts. However, such factors have apparently played a limited
role, since it was possible to confirm with the aid of the
system not only the normal hyperfrontal flow distribution at rest [12, 231, but also the hand movement
pattern [291.
The main finding of the present study is the observation that the pattern of rCBF (the cerebral ideogram) accompanying an attempt to conceive of a hand
movement differs from that of an actual hand movement. The conceptualization of a given movement
(motor ideation) induced high flow in the whole frontal lobe, including its supraorbital parts. It also involved parietal and temporal regions. In contrast, the
actual hand movement produced an increase mainly in
the rolandic area.
The normal hyperfrontal resting rCBF pattern has
been firmly established in large series of normal brains
studied in different laboratories. It can also be recorded with the detector battery looking at the brain
from the vertex, and hence it cannot be explained as
an artifact caused by detector geometry. The dominant hemisphere at rest shows a higher flow (activity)
in frontal regions anterior to a line following the anterior part of the sylvian fissure and up the rolandic
fissure, and correspondingly lower flows in regions
posterior to this line. This pattern has been interpreted to show that anterior, “efferent” brain structures responsible for the programming of behavior in
its widest sense are more active at rest than are postcentral regions, in which sensory (“afferent,” “gnostic”) as well as mnestic functions are localized [28]. In
accordance with this view, resting consciousness implies a low degree of anticipatory programming of
behavior, or a “simulation” of behavior [ 12, 131. This
view is supported by the finding that an increased
Ingvar and Philipson: Cerebral Blood Flow during Motor Ideation and Performance 233
A
B
C
F i g 2. Cerebral ideograms obtained from 4 neurologii-ally
normalsubjects at rest (A), during motor ideation (B). and
during actual movements of the right hand (C).To the
leJt the mean values for Pco2 ikPai and systolic blood
prejjsi.kve (mnz Hgi are giwn, as well as the mean
hemisphere Joui t1alue.r for the whole grvup ginit,
in
mll100 gnzlmin).To the right. the color scale (alsoproduced bj
the color displap system) is seen, Each step corresponds t o a
relatiue flou ualue as indicated. Note that yellow (middle of
the scale) correspondJ to the referenre mean Jou, at rest.
234
Annals of Neurology
Vol 2
No 3 September 1977
At rest (A) the normal hyperfronialJou, distribution is
seen. with high f l v u ~ sin prevnotor and frontal regions
and very l o w Jous tevnporalLy. During “hand
movements conceived” (B)$without actual
motmz-ents, mean JYGW u/aJ augmented by about I T 7:.The
most marked rise i n Jozu was seen in the frontal region, and
jou: was also incveesed over sylvian and temporal straitam.
During “hand movements performed” (C) a
clear-cut Jou!peak was recorded ouer the syloian region,
u6ile f l o z ~ vin the frontal and temporal structures u’as
lower than i n B.
a
HAND MOVEMENTS
PERFORMED
CONCEIVED
Rel. to
hemisphere f
.
o
i o olsolO ”
REST
R
D
A
0
0
*.b
, O.
10 2 0 30 40
50%
BP 120
m m Hg
F
F i g .3. rCBF measurenrerrts in a 49-year-old man with
suspeitedpresenile denzentia (Patient 4 i n the Table).This
patient had no neurologiialdefcii and normalpsychonirlrii
Yesu Its.
The diagram are redrawn from aitual plots obtained
dircL-t[yfrom the computer. In A. the j o u ! distribution is
shown in relation t o the hemisphere mean f l o w at rest. Small
XT indisate detestor fields withfEOws wirhin 2 10% of the
mean.
At the right ofthefigure, the upper Y O U ofdiagrams shoics
j o u ’ dirtribution during motor ideation IB) andactual
hand moisements (C}.using the actual mean j o z c . (65
and 60 mlll 00 gmlmini as referenies.
D and E shnu j o u distribution i n the same two
situations, using the re.rting hemisphere mean j o w (54
mllI()(j gmlmin) as reference. Values obtained in this
manner were used for the calculation which gave the
cerebral ideograms shown in Figure 2.
In F a n d G , a regionalcomparison bas been madefor each
detei-torjeld: i.e., tach regionaljou-a alue u.as compared zcith
j o z i ’ at rest in the same position. This type ofplot shows more
slear4y the rery marked temporal and frontal j o u :
augmentations during motor ideation and, in contrast. the
marked rolandii flou increase during the actual
performance of hand movements.
DCOZ
5 5
*Pa
130
5 6
G
level of awareness (consciousness) induced by touch
or slight pain does not in principle alter the hyperfrontal distribution, but only its general level [171.
Willful conceptualization of a hand movement
would, it seems, require an increased amount of behavioral programming, with a rise in frontal flow as a
result (Fig2B). The “valley”-i.e., the region with low
flow seen over the rolandic area at the same time
during motor ideation-might be related to inhibitory
phenomena in regions preparing themselves for the
actual performance of the movement conceived [91.
Jacquy et a1 [20] have recently confirmed the present
results in principle, using a modified rheoencephalographic method that yields regional values which correlate highly with blood flow in the gray matter. During imagined hand movements in an experimental
situation very similar to the present one, Jacquy et a1
[21] showed distinct increases of their index over
values in precentral regions.
Motor ideation also activated sylvian and temporal
structures pertaining to those brought into play by
speech [12, 181. It is inviting to speculate whether
motor ideation (without movements) implies that the
subject “reminds” himself by inner verbal commands
about the movement he is thinking of. The important
increase of flow in temporal structures during motor
ideation suggests further that memory engrams located in this region [301 must be mobilized in order
for a subject to formulate an inner concept of a
movement.
It might be argued that we did not have any control
over the actual mental events going on in the subjects
Ingvar and Philipson: Cerebral Blood Flow during Motor Ideation and Performance 235
REST
f
PCO,
BP
45
130
49
130
A
HAND MOVEMENTS CONCEIVED
/--
B
-
HAND MOVEMENTS PERFORMED
4. rCBF nieasuremrnts in a 2j-yeur-old iiiovian
with focal cortical epilepsy. The jtndy u.a.r made i n an
ilzterictal phuje. The patzewl u z i f i d y furid and
rooperuted cxcellent(y. Her mean hemisphere rCAP at
40 mlllOO grnlmin) uws subnormal (comparewith
t’alueji n the Table). but there u w n o focaf hypereniia in the
tenzporul region, where moderate parox.y.irmaf E E G changes
had been recorded.
(A)~hou1.rtheJou distrihutiori at rut in relation t o the
hemisphevemeanjou~of40 mlll0Ogmln~in.Thetwo lower
diagrams are based upon detector-detector comparisons id
Fig 3F,Gi, ( B ) shouis the froiztul and tempor-alJRoz.o
increuse during motor ideation. The inrreuse in meun
f l o w was nioderute (4-3nil/lO0 gmlmin). (Ci shows the
localized rolandicjofl:increase during hand moiiements.
The mean ,flou’ i~’u.r41 nilllOO gvilmin.
Fig
In recent years our laboratory has advanced evidence using the rCBF technique that concept formation, ideation, abstract thinking, and resting conscious
mentation d o not activate rolandic regions as much
as they d o frontal areas [12, 13, 18, 311. This
view generally agrees with several electrophysiological studies which have shown that precentral and prerolandic neuronal events may precede the performance of a motor act [ I , 3, 25, 34, 351.
The present study supports the notion that the formation of abstract concepts-ideation-is
now accessible for direct quantitative studies. Previously we
demonstrated that patients who have organic dementia, with a reduced resting cerebral blood flow, show
less increase in frontal flow during psychological testing than normal subjects [ 10, 141. This is of interest in
the present context since a main feature of the
psychological defect in organic dementia is a diminished capacity to form concepts, to ideate.
Chronic schizophrenia should also be mentioned. Deteriorated patients with this disorder have a “hypufrontal” rCBF pattern at rest, i.e., relatively low flows
in frontal structures. We have concluded that this may
imply an abnormally low degree of resting ideation [7,
81. During attempts to activate severely deteriorated
chronic schizophrenics by means of psychological
tests, the blood flow in the frontal lobe was found to
increase less than in normal subjects [8]. This indicates that measurements of the rCBF distribution at
rest and during various forms of mental activation,
including motor ideation, might be useful in studies of
the cerebral pathophysiology of mental disorders.
Supported by the Swedish Medical Research Council (Project
B76-14X-00084-12A) and by the Wallenberg and Thuring Foundations, Stockholm.
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Ingvar and Philipson: Cerebral Blood Flow during Motor Ideation and Performance 237
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