776
Regional Cerebral Blood Flow in Stroke:
Hemispheric Effects of Cognitive Activity
Ruben C. Gur, PhD, Raquel E. Gur, MD, PhD, Frank L. Silver, MD,
Walter D. Obrist, PhD, Brett E. Skolnick, PhD, Michael Kushner, MD,
Howard I. Hurtig, MD, and Martin Reivich, MD
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Regional cerebral blood flow (rCBF) was measured with the xenon-133 inhalation technique in 15
patients with unilateral cerebral infarction and 12 matched controls. Measurements were performed
during a standard resting baseline condition and during the performance of standardized verbal
analogies and spatial line orientation tasks. Resting and activated CBF were lower in patients than in
controls, and there were differences in the hemispheric pattern of activated CBF. Control subjects
replicated earlier findings of asymmetric increase in CBF for the cognitive tasks, whereas patients
showed abnormalities in lateralIzed CBF changes consistent with side of infarction. These findings
underscore the utility of cognitive challenges in the study of rCBF in stroke. This can lead to an
experimental paradigm in clinical studies of the relation between behavioral deficits and regional
brain dysfunction and may also improve the utility of CBF measurements in clinical settings. (Stroke
1987;18:776-780)
T
he xenon-133 inhalation technique provides a
noninvasive method for determining regional
cerebral blood flow (rCBF). 12 It has been applied extensively in the study of the effects of stroke.
Previous reports have documented overall reduction in
rCBF, but data on the effects of unilateral cerebral
infarction (CI) on hemispheric rCBF have been inconsistent. *-5 The measurement of hemispheric rCBF
changes during cognitive activity in relation to the side
of anatomic lesions may help us understand the behavioral consequences of stroke and its effects on physiologic changes in regional brain function.
Most studies of rCBF in CI performed thus far are of
limited value for addressing this relation because the
rCBF measurements were obtained during resting conditions. The exceptions are the studies of Meyer et al6
and Knopman et al.7 Meyer et al studied rCBF in 14
patients with left hemispheric infarctions and aphasia,
6 with severe infarctions and poor recovery from aphasia and 8 with mild-to-moderate infarctions and good
recovery. They used multimodal stimulation and for
the first group reported bilaterally reduced hemispheric CBF during stimulation, with reduction in left hemispheric rCBF in Broca's and Wernicke's areas. In the
mild group there was bilateral increase in CBF, with
right hemisphere blood flow greater than left. The data
From the Cerebrovascular Research Center. Departments of
Neurology (R.C.G., R.E.G., F.L.S., W.D.O., B.E.S., M.K.,
H.I.H., M.R.) and Psychiatry (R.C.G., R.E.G.), University of
Pennsylvania and The Graduate Hospital, Philadelphia, Pennsylvania.
Supported by National Institutes of Health Grant NS 19039,
National Institute of Mental Health Grant MH 30456, and The
Spencer Foundation. F.L.S. was supported by the Ontario Heart
Foundation.
Address for reprints: Dr. Ruben C. Gur. Brain Behavior Laboratory, 205 Piersol Building, University of Pennsylvania, Philadelphia, PA 19104.
Received November 17, 1986; accepted February 16, 1987.
were interpreted as supporting the transfer of language
functions to the right hemisphere in association with
recovery. Knopman et al measured rCBF in 21 aphasic
patients with left hemispheric ischemic infarction at
resting baseline and during an auditory verbal comprehension task. They reported increased right hemispheric CBF associated with recovery from aphasia,
supporting the hypothesis that such recovery coincides
with increased right hemispheric involvement in language comprehension. The behavioral deficits in CI
presumably reflect failure of brain regions to be activated in response to task demands. These findings
encourage a more systematic examination of the relation between hemispheric changes in CBF and cognitive activity.
There is evidence that cognitive tasks produce systematic changes in hemispheric rCBF. 8 "" Gur et al' 2
reported that, in normal subjects, performance of a
verbal analogies task produced a greater increase in
left-hemispheric CBF, whereas right-hemispheric
CBF increased more for a spatial task requiring judgment of line orientation. We report the results of applying the same tasks to a sample of patients with unilateral CI.
Subjects and Methods
Subjects
Fifteen patients were selected from consecutive admissions and outpatient visits at the neurology services
of the Hospital of the University of Pennsylvania and
The Graduate Hospital. A laterality questionnaire13
was administered to exclude left-handed patients.
Only patients with a completed CI as evidenced by a
clear unilateral deficit that lasted > 24 hours were
admitted to the protocol. A computed tomography
(CT) scan was performed on admission to the hospital.
In addition, an echocardiogram and Doppler studies of
the carotid arteries were used to exclude major vascu-
Cur et al
Activated rCBF in Stroke
777
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lar disease and diagnoses other than ischemic, nonhemorrhagic CI. All patients were neurologically stable at the time of study, and their deficit was
sufficiently mild to permit participation. All were
treated with aspirin, and 4 patients, studied within 3
days after infarction, received no other medications.
The 11 other patients were treated with antihypertensive medication.
On the basis of the clincial data, patients were assigned to one of two groups: left-hemispheric cerebral
infarction (LCI) (n = 8) and right-hemispheric cerebral infarction (RCI) (n = 7). Diagnostic assignment
was performed independently by two neurologists with
complete agreement. Pertinent characteristics of the
sample are summarized in Table 1.
The controls (C) (n = 12) were right-handed, identically screened, and were balanced with patients for
sex ratio (male: female, LCI 5:3; RCI 5:2; C 5:7) and
age (mean ± SD, LCI 63.6 ± 8.9; RCI 51.9 ± 9.3; C
56.1 ± 11.8 years) [F(2,24) = 2.48, not significant].
The 3 groups did not differ in hemoglobin levels (LCI
14.0 ± 1.6; RCI 14.7 ± 1.3; C 14.4 ± 1.6 mg/100
ml) [F(2,24) < 1], systolic (LCI 133.3 ± 18.8; RCI
137.0 ± 19.4; C 132.5 ± 10.0 mm Hg) [F(2,24) < 1]
and diastolic blood pressure (LCI 81.6 ± 15.4; RCI
85.0 ± 6.5; C 81.6 ± 6.6) [F(2,24) < 1]. The 2
patient groups did not differ in time since ictus (LCI
38.1 ± 55.7; RCI 43.3 ± 72.3 days) (r13 < 1).
Procedures
The purpose and procedures were explained to the
subjects in detail, and informed consent was obtained.
Table 1.
A complete history was obtained and neurologic examination performed immediately before the rCBF
study.
Three rCBF determinations (during resting baseline
and verbal analogies and spatial line orientation tests)
were made on each subject in a single session. The
measurements were separated by at least 15 minutes to
assure that background activity was at acceptable levels ( < 10% of peak counts). The verbal analogies were
adapted from the Scholastic Aptitude Test14 with the 4
response pairs presented underneath the test analogy
pair. The spatial task was an adaptation of the Benton
Line Orientation Test. 1316 Subjects were shown pairs
of lines that varied in length and orientation and were
asked to indicate, on an array presented below the
stimulus field, the lines corresponding to the stimulus.
Five practice trials were provided for each task, and
subjects proceeded at their own pace. Tasks were initiated 5 minutes before inhalation of xenon-133 and
continued throughout the 15 minutes of uptake and
clearance measurement, for a total of 20 minutes.
Order of conditions was randomized across subjects
in a Latin square design. Ambient noise and lighting
were kept to the minimum required for operation of the
laboratory. Subjects had their eyes open in all conditions, and their ears were not occluded. Subjects were
in a supine position, and test stimuli were projected on
an overhead screen. Response modes in the 2 tasks
were equated by having subjects indicate their response with a flashlight held in both hands. Patients
with hemiparesis could still hold the flashlight with
both hands.
Patient Characteristics
Patient/Age/Sex
Left hemispheric
Interval from ictus,
days
Neurologic deficit at
time of study
CT scan findings
infarction
8
2
10
8
1/66/M
2/71/F
3/79/M
4/63/F
None
L parietal infarct
R arm weakness
Negative
R hemiparesis
Negative
R hemiparesis, R homonomous
L parietal, L occipital infarct
hemianopia
5/60/F
6/64/F
7/56/M
8/50/M
Right hemispheric
1/53/M
2/60/M
3/55/M
4/40/M
5/64/F
6/41/M
7/50/F
150
2
100
25
R hemiparesis
L frontal infarct
Anomic aphasia
Negative
Broca's aphasia
L frontal infarct
R hemiparesis
L internal capsule
19
10
201
59
2
9
3
None
R frontal infarct
L leg weakness
Negative
L hemiparesis
R frontal infarct
L hemiparesis
R frontal infarct
L hemiparesis
Negative
L hemiplegia
Negative
L hemiparesis
Negative
infarction
The patients with no neurologic deficit at the time of study had hemiparesis that cleared; CT scans were obtained within
48 hours of admission. L, left; R, right; CT, computed tomography.
778
Stroke
LOCATION OF DETETT0R5
FIGURE 1. Schematic probe configuration, intended to cover
the middle cerebral artery distribution.
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CBF was determined by the xenon-133 inhalation
technique. u Trace amounts of l33Xe (5-7 mCi/1) in air
were inhaled through a face mask for approximately 60
seconds. The uptake and clearance of the isotope from
the brain were monitored by 16 collimated sodium
iodide crystal detectors placed over the scalp (Figure
1). rCBF was computed from the clearance rates, as
described by Obrist and Wilkinson.17 The clearance
curves were analyzed for 14 minutes after inhalation.
The 14-minute analyses were preferred over shorter
intervals because they increase the stability of the computed parameters. l8 The integrity of the rCBF measurements was evaluated for absence of artifacts, good
count rates and curve fits, and adequate estimation of
end-tidal carbon dioxide levels. There were no differences in carbon dioxide levels measured with a capnograph in mm Hg between LCI patients (mean ± SD,
resting 35.6 ± 2.6; verbal 35.2 ± 2.3; spatial 34.9 ±
5.4), RCI patients (resting 36.4 ± 3.6; verbal 35.7 ±
3.4; spatial 35.6 ± 3.2), and controls (resting 36.4 ±
3.4; verbal 36.1 ± 3.1; spatial 35.8 ± 3.2) [all
F(2,24) < 1]. The rCBF values for the 2 activation
measurements in each subject were corrected to the
resting baseline carbon dioxide level.19-20 The correction factor was 3%/mm Hg change in Pco 2 . The statistical analyses were also performed on the uncorrected
data, and the effects reported here persisted.
Results
The dependent variable was IS of Obrist and Wilkinson,16 which is an index of flow defined as the tangent
at time zero for an equivalent bolus injection. IS is
more sensitive than Risberg's ISI21 to blood flow in the
fast-clearing, gray matter compartment. IS was preferred over the traditional measure of gray matter flow,
F l , because it is more stable in pathologic conditions.18 Analyses were also performed forFl andCBF15, the mean flow of the fast and slow compartments, with similar results.17 We report findings in
which diagnostic grouping (patients vs. controls) was
significant.
Table 2 presents the hemispheric means for each
measure across groups and conditions. The results
were analyzed with an analysis of variance (ANOVA)
procedure22 using diagnosis as a grouping factor (LCI,
RCI, C) and task (resting, verbal, spatial) and hemisphere (left, right) as within-group factors. There was
a significant effect of task [F(2,48) = 14.62, p <
0.0001 ], indicating higher CBF during cognitive activ-
Vol 18, No 4, July-August 1987
ity compared with resting. A task X hemisphere interaction [F(2,48) = 3.28, p = 0.046] indicated that
across all groups there was a relatively greater increase
in the left hemisphere CBF for the verbal task and a
greater right hemisphere increase for the spatial task.
This effect, however, was different in the patient and
control groups as indicated by the hypothesized
higher-order task X hemisphere X diagnosis interaction [F(4,48) = 3.03, p = 0.026]. This interaction is
illustrated in Figure 2.
To evaluate which specific differences are significantly responsible for the higher-order interaction, the
three-way interaction was decomposed using the
simple-effects procedure of Davidson and Toporek22
for univariate contrasts. The controls duplicated the
pattern seen in our studies with younger normal subjects, 1223 with higher left hemispheric CBF for the verbal relative to higher right hemispheric CBF for the
spatial task (p - 0.011). This pattern was not significant for either group of patients. LCI patients showed
no overall activation for the verbal task and only a
marginally significant overall increase for the spatial
task (p = 0.051, one-tailed). There were no significant effects of task on hemispheric CBF asymmetries.
By contrast, RCI patients snowed significant overall
activation for both the verbal (p = 0.016) and spatial
tasks (/? = 0.030). Furthermore, they had greater left
than right hemispheric activation for both the verbal (p
= 0.031) and spatial tasks (p = 0.017).
Additional univariate analyses were performed to
compare patients (LCI and RCI combined) with controls for each task condition. For resting baseline, patients had significantly lower flows than controls (p =
0.031). When each subgroup of patients was compared
with controls, there was a marginally significant reduction in overall CBF for LCI (p = 0.07, one-tailed)
and a significant reduction for RCI (p = 0.033, onetailed). For the verbal task, patients had lower overall
flows than controls (p = 0.028). Subgroup comparisons showed that the LCI group had lower CBF than
controls (p = 0.043), whereas the RCI group did not
differ from controls. For the spatial task as well, patients had lower flows (p = 0.009), and each group
separately had lower CBF (LCI, p = 0.026; RCI, p =
0.048). Thus, RCI patients were most clearly differentiated from controls during the spatial task, whereas
LCI patients were differentiated from controls during
both tasks.
To evaluate task performance, the proportion of correct responses for the verbal and spatial tasks administered during the rCBF session were calculated. Standard (z-score) transformations of those proportions
were the dependent measure in a diagnosis x task
ANOVA. There was a significant effect of diagnosis
[^(2,24) = 5.25, p = 0.014], indicating that controls
performed better than patients. No other effects or
interactions were significant. The task x diagnosis
interaction was not significant, probably because of
the mild impairment of these subjects and the small
sample size considering the power of the statistical tests.
Gur et al
Activated rCBF in Stroke
779
Table 2.
IS, Fl, and CBF-15 in Controls and Patients With Left and Right Cerebral Infarct
Group
Controls
IS
Fl
CBF-15
LCI
IS
Fl
CBF-15
RC1
IS
Fl
CBF-15
Spatial task
Verbal task
Resting
RH
LH
RH
LH
RH
LH
55.53 + 8.22
58.47 ±3.43
37.85±7.O5
55.58±8. 51
58.45 + 3. 28
38.06±7.08
59.35 ±6.66
62.64±2.64
62 .43 ±8.64
39.79 ±6.02
58.67 + 6.62
63.05 + 2.59
39.69±6.36
65 .6O±5.54
41 .02 + 7.54
50.37 + 4.46
53.84±5.71
35.12±3.22
50.76±4. 04
54.54 ±4.63
35.44±3. 30
52.02±6.72
55.91 ±4.35
36.14±4.35
52.13 + 6.35
56.89±3.97
36.37 + 3.86
53 .10±4.85
59 .26 ±6.74
37 .55±5.19
53.70 + 5.34
59.81 ±6.30
37.9O±5.79
46.53 ±11.73
52.62± 12.55
34.29±5.63
47.10 + 9. 40
52.56±9. 94
34.07 + 5. 33
52.53± 12.59
59.93± 13.34
36.63 ±4.17
51.06+11.25
58.44±12.18
36.12 + 4.16
51 .83± 15.64
59 .38+ 14.38
36 .59 ±8.07
5O.O5± 13.01
57.35± 10.77
63.26±8.69
66.23±5.50
41.47 + 8.09
35.74±7.57
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IS, initial slope of impulse equivalent clearance curve; Fl, fast-flow compartment (ml/100 g/min); CBF-15, mean flow of fast and slow
compartments (ml/100 g/min); LH, left hemisphere; RH, right hemisphere; CI, cerebral infarct. Values are mean ± SD.
Discussion
The results for controls are consistent with our previous studies with normal subjects12-23 and with reports
from other laboratories indicating increased CBF
during cognitive activity, with laterality of changes
congruent with hemispheric specialization of function.7"" Also consistent with these earlier studies,
these effects are small and superimposed on a bilateral
increase in CBF. The reliable hemispheric effects were
attributed to the consistency of asymmetry rather than
the magnitude.7"9
In contrast to controls, patients with hemispheric
infarcts demonstrated abnormalities in the laterality of
CBF increase. RCI patients showed greater disturbance in right hemispheric activation for the spatial
task, whereas LCI patients showed greater left hemispheric impairment of activation for the verbal task.
The results for LCI are consistent with the data of
Meyer et al6 on a similar group of patients with mild-
o
Controls
Left hemiiphare
Right hamtaphare
R
Lsft
carabral infarct
Right
carabral infarc
R
V
S
FIGURE 2. Hemispheric cerebral blood flow for resting (R),
verbal (V) and spatial (S) conditions in patients and matched
controls.
to-moderate infarcts. The comparison with the RCI
group suggested further evidence that hemispheric infarction disturbs the normal pattern of lateralized cerebral activation in accordance with task demands. This
supports the notion that behavioral deficits associated
with CI may reflect failure of brain regions to become
active in response to cognitive challenges.
The side of a stroke also affected the magnitude of
asymmetry of hemispheric CBF increase produced by
cognitive activation (Figure 2). RCI patients had a
normal activation pattern for the verbal task (increased
left hemispheric activation) and relative bilateral reduction in overall activation for the spatial task. LCI
patients showed reduced activation for both tasks. In
view of the lack of an hypothesis that the side of a
lesion is related to the degree of cortical activation
impairment during cognition, replication of this study
is indicated.
The effects obtained may be metabolic or hemodynamic. Specifically, the reduced augmentation of CBF
during cognition can be a primary defect of tissue
metabolism associated with ischemic neuronal damage. It could also be attributed to a hemodynamically
compromised cerebral circulation unable to respond to
the increased metabolic demands of cognitive activation. In the intact brain neural activity, cerebral metabolism and blood flow are tightly coupled.24-25 CI is
associated with neuronal loss and concomitant decrease in metabolism and blood flow.26-27 Abnormalities in blood flow changes during cognitive activation
may reflect failure of brain regions to become metabolically activated. On the other hand, it is possible
that vascular disease impairs the capacity for an appropriate increase in perfusion during cognitive activity.
This question can be addressed by assessing the relation between individual patterns of CBF changes in
patients who differ in the degree of clinical impairment, the amount of neural loss, and the extent of
vascular disease. The question can also be answered by
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780
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future positron emission tomography studies in which
glucose and oxygen metabolism are compared with
CBF in the same individuals.
The hemispheric asymmetries of changes in CBF
have been attributed to the effects of cognitive activity.
This seems justified because the stimulation and response modalities were equal for the verbal and spatial
tasks with respect to sensorimotor and attentional components, and only patients who could manipulate the
flashlight and perform the cognitive tasks were studied. However, the sensorimotor and attentional components merit more specific investigation to identify
their contribution to CBF changes in normal and pathologic conditions.
The results of the present investigation should be
regarded as preliminary in view of the small and heterogeneous sample. However, they suggest a potential
use of the cognitive activation paradigm in a systematic study of brain-behavior relations. In this initial step,
only hemispheric effects were examined. Future research can use tasks aimed at activating more specific
regions and relate behavioral deficits to abnormalities
in blood flow changes for appropriate brain regions.
Larger and more homogeneous populations will be
needed for such studies, and follow-up data will be
necessary to establish the relation between activation
patterns and recovery.7 The potential of cognitive challenge procedures for improving the clinical utility of
the 133Xe technique also merits further investigation to
determine whether these group effects are helpful in
identifying cerebral disease in individual patients. It
also remains to be seen whether abnormalities in rCBF
changes during cognitive activity predict recovery, as
suggested by Knopman et al,7 and whether the pattern
of abnormality may assist in identification of patients
who are at higher risk for further ischemic events.
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KEY WORDS • rCBF • xenon-133 inhalation technique •
cognitive activation • unilateral cerebral infarct • verbal and
spatial tasks
Regional cerebral blood flow in stroke: hemispheric effects of cognitive activity.
R C Gur, R E Gur, F L Silver, W D Obrist, B E Skolnick, M Kushner, H I Hurtig and M Reivich
Stroke. 1987;18:776-780
doi: 10.1161/01.STR.18.4.776
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