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Published online before print November 21, 2002, 10.1148/radiol.2261020141
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(Radiology 2003;226:188-194.)
© RSNA, 2002

Neuroradiology

Correlation of Functional MR Imaging Activation Data with Simple Reaction Times1

Kader Karli Oguz, MD, Nina Mikelashvili Browner, MD, Vince D. Calhoun, PhD, Colin Wu, PhD, Michael A. Kraut, MD and David M. Yousem, MD

1 From the Russell H. Morgan Department of Radiology and Radiological Sciences, Divisions of Neuroradiology (K.K.O., N.M.B., M.A.K., D.M.Y.) and Psychiatric Neuro-Imaging (V.D.C.), Johns Hopkins Hospital, 600 N Wolfe St, Phipps B-112, Baltimore, MD 21287; and Office of Biostatistics Research, National Heart, Lung, and Blood Institute (C.W.). Received February 22, 2002; revision requested May 15; revision received June 24; accepted July 31. Supported by RPN 99-01-21-03. K.K.O. supported in part by TUBITAK (Scientific and Technical Research Council of Turkey). Address correspondence to D.M.Y. (e-mail: yousem@rad.jhu.edu).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To determine the relationship between subject reaction times (RTs) and activation volume in the brain during visuomotor functional magnetic resonance (MR) imaging.

MATERIALS AND METHODS: Twenty-four subjects performed a simple RT task during single-event functional MR imaging, and RTs were recorded. The six subjects with the fastest RTs were designated the fast RT group, and the six subjects with the slowest RTs were designated the slow RT group. The data were processed with noncorrected height threshold (P < .001) for individual comparisons and corrected height threshold (P < .05) for group comparisons (t tests). The activation volumes in both occipital lobes, the left sensorimotor cortex, and the supplemental motor cortices were compared for the two groups.

RESULTS: The mean RT ± SD was 342 msec ± 20.15 for the fast RT group and 475 msec ± 36.17 for the slow RT group (P < .0001). More voxels of activation were seen in the fast RT group than in the slow RT group in the occipital lobes, left sensorimotor cortices, and supplemental motor cortices on individual and group maps. This difference was statistically significant in the left sensorimotor (P = .03) and left visual (P = .05) cortices. In the right visual cortex, a trend toward more activation in the fast RT group was noted (P = .15). There was a negative correlation between RTs and activation volume in the left sensorimotor cortex (P = .048).

CONCLUSION: There was a greater activation volume in motor and visual cortices in the fast RT group than in the slow RT group.

© RSNA, 2002

Index terms: Brain, cortex • Brain, function, 133.12144 • Brain, MR, 10.121412, 10.12144 • Magnetic resonance (MR), functional imaging, 10.121412, 10.12144


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
A reaction time (RT) is the time between the onset of a stimulus and the motor response to it. In a simple RT test, the time from stimulus onset to time of stimulus detection (perceptual latency) is measured, as well as the motor time, which is the time it takes to perform the motor task (1). There is wide variability in simple RTs between individuals. Factors that may influence RTs include the type, intensity, and background of the stimulus and subject age, sex, educational level, socioeconomic status, affective state, attentional and arousal state, caffeine use, exercise level, cardiovascular status and risk factors, blood alcohol level, and general health (1–6). Auditory stimulus RTs are generally shorter than are visual RTs, and RTs tend to increase with subject age for a variety of stimuli (4,6–13). The prolongation of RTs can account for the propensity of motor vehicle accidents, slips, and falls in the elderly and infirm, since their RTs to emergency situations tend to be slower (2,12).

The delays that occur in visuomotor RTs may be due to delays in detecting the stimulus (eg, visual acuity), transporting the information about the stimulus to the brain for central processing (eg, transport of data from retina to occipital lobes), processing the data within the brain (eg, visual, association, supplemental motor, and motor cortices), sending a message to the peripheral reactors (eg, transport through the brain to the spine and neuromuscular unit), or performing the peripheral function (eg, electromyographic stimulation and motor times) (14). The intensity of the stimulus may affect the RTs in some subsets of subjects, but Botwinick and Storandt (6) believe that the slowing of RTs is rarely accounted for by an inability to perceive the stimulus.

Functional magnetic resonance (MR) imaging can be used to interrogate the central processing aspect of the visuomotor RT task. The volume of brain activated by a given stimulus and the degree and timing of activation can be evaluated by using single-event paradigms. We hypothesized that subjects with faster RTs would show a greater number of activated voxels at visuomotor functional MR imaging. Our hypothesis was based on a theory that activation of a larger volume of the brain reflects a more robust vascular response to a stimulus, which would positively affect RTs. Thus, the purpose of our study was to determine the relationship between subject RTs and the activation volume of the brain during visuomotor functional MR imaging.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Subjects
All subjects were recruited from healthy volunteer registries from the Parkinson’s Disease Research Center, Baltimore, Md; a neuroradiology patient database; or advertisements in the printed media. After we obtained informed consent, as recommended by our hospital institutional review board, 24 healthy subjects underwent single-event visuomotor functional MR imaging in which the subject RTs were measured.

All participants were right handed and healthy (ie, none were taking medication or had a chronic illness). Neuropsychologic tests were performed before each individual underwent functional MR imaging, and all subjects scored within normal range of intelligence quotients with no evidence of depression. Visual acuity was tested by visualizing an 8-inch (20.3-cm) colored object at 12 inches (30.5 cm) for stimulus presentation, and all subjects passed this test.

Participants were selected on the basis of their RTs in the MR imager. "Fast" and "slow" RT groups were assigned with six subjects in each group (we chose the fastest and slowest six subjects to increase the difference between the RTs in the two groups). The fast RT group included four women and two men, and the slow group included three women and three men. Subject age ranged from 38 to 72 years (mean age, 57.5 years) in the fast RT group and from 31 to 85 years (mean age, 59.5 years) in the slow RT group. We wished to reduce the effects of age in this study; fortunately, the ages of the subjects selected for the two groups negated the influence of age.

MR Imaging
Functional MR imaging was performed with a 1.5-T imager (Gyroscan ACS-NT Powertrak 6000; Philips Medical Systems, Best, the Netherlands) equipped with 2.3 G/cm gradients and echo-planar capability. A standard head coil with foam padding was used to limit head motion. For the functional MR imaging protocol, we used a gradient-echo blood oxygen level–dependent, or BOLD, technique, with 1,000/39 (repetition time msec/echo time msec), 90° flip angle, 24-cm field of view, and 360 time points in a 6-minute sequence. Sections were acquired with a 5-mm thickness and an intersection spacing of 1 mm with a matrix of 128 x 128. Twelve sections angled parallel to the intercomissural line that included both primary visual and sensorimotor cortices were obtained.

At the echo time of 39 msec, there is not enough time to sample the 128 x 128 k-space data matrix fully, so a 128 x 128 matrix size requires partial acquisition of the k-space data. Hence, the actual spatial resolution exceeds the 1.875 x 1.875-mm pixel size within the section.

The single-event paradigm, developed with E-prime (Psychology Software Tools, Pittsburgh, Penn) programming software, consisted of a round multicolored visual cue that appeared on the screen for 0.5 seconds either at 20- or 30-second intervals randomly throughout the study. The subjects were asked to tap a finger-press button with their right index finger as soon as they saw the visual cue. RTs were measured from the button box.

Data Processing and Recording
Functional data processing was performed with Ultra workstations (Sun Microsystems, Santa Clara, Calif) by using Statistical Parametric Mapping 99 software (Wellcome Department of Cognitive Neurology, London, England) implemented in MATLAB software (Mathworks, Sherbon, Mass) (15–23). Realignment for motion correction, normalization, and deformation to a standard atlas (Montreal Neurologic Institute template), smoothing at 5-mm section thickness, and data analysis performed by using a noncorrected height threshold at a P value of .001 were performed with the mapping software for individual subjects. We placed no limits on cluster sizes.

Group maps were also generated by using the smoothed normalized data sets with corrected height threshold at a P value of .05. Use of corrected height thresholds is a more rigorous test because it accounts for the multiple comparisons made in the large number of voxels studied in the brain (analogous to Bonferroni correction). Therefore, when the corrected height threshold is applied, one reduces the P value to less than .05; the analogous uncorrected value would be less than 4 x 10-7. Because of the increase in power by using six individuals for the group maps, such a strict P value can be used.

The mapping printout with x, y, and z axis coordinates was used to localize activation and determine activation volumes in left and right visual, sensorimotor, and supplemental motor cortices, as defined in the Montreal Neurologic Institute template and the Talairach and Tournoux atlas (24). Because both sides of the central sulcus region are often activated with motor tasks, the voxel sizes used (smoothed to 5 x 5 x 5 mm) make it difficult to separate adjacent cortices. We used normalized data, which required warping of a subject’s brain data into Montreal Neurologic Institute template space, and smoothing was used to 5 mm. We chose to assess the sensorimotor cortex rather than try to isolate the motor cortex.

The cluster sizes for the voxels (k values in the mapping program) that exhibited statistically significant signal intensity changes were recorded within each region of interest. Two authors (K.K.O., N.M.B.) working together compared coordinates from the Montreal Neurologic Institute and Talairach and Tournoux (24) templates with defined regions of the brain in the atlas (24). When there were multiple areas of activation in a region of interest, these were added together. The individual maps were also constructed by using a second model, which adjusted for the RTs for two subjects from each group to determine if there was any effect of RT on activation in the left sensorimotor cortex. Finally, subtraction images of the activation in the fast RT group versus that in the slow RT group were generated to demonstrate the difference in activation between groups by using a corrected height threshold at a P value of .05 and a noncorrected height threshold at a P value of .001.

The regions of interest were defined on the basis of the Montreal Neurologic Institute template of a globally normalized brain. This deformation protocol was used to correct for anatomic differences between subjects, since the data from all subjects were normalized to Montreal Neurologic Institute template space. To identify the location of these voxels, x, y, and z axis coordinates are used in the template to plot activation onto specific gyri after conversion to spatial coordinates, as defined by the analogous templates from Talairach and Tournoux (24). The Montreal Neurologic Institute templates were used to uniformly display the individual functional MR imaging maps, as well as the group maps for activation localization. Thus, a deformation protocol was used to correct for anatomic differences between subjects, since the data from all subjects were globally normalized.

Statistical Analysis
RTs and functional MR imaging data for each cortex described above were analyzed by means of one-way analysis of variance and the Welch modified two-sample t test. Spearman correlations between RTs and activation volumes were performed. Age was also assessed for effect.

All patients underwent screening T2-weighted 4,000/102 MR imaging as part of their evaluation to assess for masses and the presence and degree of white matter lesions. Only subjects with minor white matter abnormalities and no mass lesions were included in the analysis. All images were reviewed by a trained neuroradiologist (D.M.Y., who earned the certificate of added qualification in neuroradiology and had 12 years of experience), who affirmed the absence of clinically important pathologic findings in the brain. Besides punctate nonconfluent periventricular white matter hyperintensity in few patients, the T2-weighted images showed normal findings.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 
The mean RTs of the subjects in the fast RT group (342.35 msec ± 20.15) were significantly shorter than those in the slow RT group (475.36 msec ± 36.17) (analysis of variance, P < .0001). When the two groups were analyzed for age, there was no statistically significant difference (fast RT group: mean age, 57.5 years ± 11.32; slow RT group: mean age, 59.5 years ± 17.80; analysis of variance, P = .82) (Tables 1, 2).


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  		TABLE 1. RTs in the Fast RT Group

 

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  		TABLE 2. RTs in the Slow RT Group

 
With the exception of one subject in the slow RT group, all subjects in both groups showed suprathreshold activation in both visual cortices and in the left sensorimotor cortex on individual maps when the uncorrected P value was set at .001 (Table 3; Figs 1, 2). The exceptional subject showed activation only in the right visual cortex and had the least activation volume in this region among the subjects. Three subjects in each group showed activation in the left supplemental motor cortex, and of those, one subject in the slow RT group showed bilateral activation in the supplemental motor cortices (Table 3).


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  		TABLE 3. Number of Voxels per Brain Region

 


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  		Figure 1. Transverse activation map in a subject with fast RTs shows activation in the visual (arrowheads; activation in the left cortex greater than that in the right) and sensorimotor cortices (images presented in radiologic convention, where right side of image is left side of brain). The left sensorimotor cortex activation (straight arrows) is greater than that of the right (curved arrow). No supplemental motor cortex activation is seen.

 


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  		Figure 2. Transverse activation map in a subject with slow RTs. Less activation is seen in the visual and motor cortices than that in the subject with fast RTs in Figure 1.

 
Results of statistical analysis of the task-related signal intensity changes are summarized in Table 4. Because there was wide variation in cluster sizes of activation between subjects, we used natural-based logarithmic scales of the values for statistical analysis. For this reason, "1" values in Table 4 reflect zero voxels activated. There was a significant increase in the activation volumes in the left sensorimotor cortex (Welch modified t test, P = .03) in the fast RT group. While there was a significantly greater activation volume in the left visual cortex in the fast RT group, results of statistical analysis only showed trends toward more activation in the fast RT group for the right visual cortex (Welch modified t test, P = .05 for the left visual cortex and P = .15 for the right visual cortex). No correlation was seen for the left supplemental motor cortex (Welch modified t test, P = .41). None of the subjects, except for one in the slow RT group, showed suprathreshold activation in the right supplemental motor cortex (Table 3). Activation volumes showed no substantive changes when the mapping analysis was performed to correct for the RTs obtained in two subjects in each group.


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  		TABLE 4. Differences in Activation Volumes between Fast and Slow RT Groups

 
In the group maps constructed with the more strict corrected height threshold compensation (P < .05) corresponding to an uncorrected P value of 4 x 10-7, a greater number of voxels was activated in all regions of interest in the fast RT group compared with that in the slow RT group (Table 5, Fig 3). A random effects model could not be used because of the small sample size. The subtraction image of the activation in the fast RT group versus that in the slow RT group showed a substantial graphic difference in both visual and motor cortices (Fig 4).


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  		TABLE 5. Number of Voxels per Brain Region

 


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  		Figure 3a. Transverse activation group maps of subjects with (a) fast and (b) slow RTs. Subjects with fast RTs show more activation in the visual (arrowheads) and sensorimotor (arrows) cortices than do subjects with slow RTs. Even the intensity of the activation is greater in the subjects with fast RTs (red and orange areas show greater statistical correlation than do yellow and green areas).

 


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  		Figure 3b. Transverse activation group maps of subjects with (a) fast and (b) slow RTs. Subjects with fast RTs show more activation in the visual (arrowheads) and sensorimotor (arrows) cortices than do subjects with slow RTs. Even the intensity of the activation is greater in the subjects with fast RTs (red and orange areas show greater statistical correlation than do yellow and green areas).

 


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  		Figure 4. Transverse subtraction map of activation in the fast RT group versus that in the slow RT group shows the difference in activation volumes in the left visual and sensorimotor cortices. Interestingly, the difference in right sensorimotor cortex activation between the two groups becomes more striking. It is well known that unilateral motor cortex activation often involves both sensorimotor cortices; therefore, the right-sided differences may be discovered by comparing the group maps in Figures 3 and 4.

 
Significant correlation was found between RT and the activation volume in the left sensorimotor cortex when Spearman correlation was performed ({rho} = -0.59; P = .048). The volumes of activation in other regions showed less correlation with RTs ({rho} = -0.42 and P = .15 for the left visual cortex; {rho} = -0.35 and P = .24 for the right visual cortex).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
REFERENCES
 
Since slowing of motor functions has an undeniable effect on quality of life as people get older, it is important to understand the underlying pathophysiology of this phenomenon. In the past 4 decades, results of many behavioral studies on RTs have shown that RT increases with age (7–11). Mean RTs and intra- and intersubject variability in RTs increase with age, and most researchers believe that it is the psychomotor component of the RT that shows the greatest deterioration (26). This might suggest that one would find the greatest differences in brain activation between slow and fast RT groups in the motor processing areas of the brain. Although results of some studies (25,27–30) have shown the effects of age on brain function since the introduction of functional MR imaging, few investigators have examined the change in brain activation volume with respect to RT.

In the present study, we compared groups of healthy adults with different RTs measured during functional MR imaging while correcting for age. We sought to reduce any effects of anticipation or accommodation by using a single-event paradigm with a long but variable interstimulus delay. We believe this conforms most closely to reactions to stimuli outside the imager and in the working environment. We chose a visuomotor RT task in our study because of its simplicity and well-described place in the literature. Also, this task is well understood, and the functional MR imaging findings can be compared with results of behavioral studies performed previously (7–11).

The fast RT group activated a greater volume of the brain at all sites than did the slow RT group on both individual and group maps (Figs 1–3). The activation in the left sensorimotor and left visual cortices was significantly higher in the fast RT group and showed a trend toward being higher in the right occipital lobe. The variability in the activation volumes in both groups was greater in the fast RT group. This finding also reflects the possible variability in the population that should be considered in every functional MR imaging study. Sample fluctuation could contribute to the correlation between RT and activation volume in the left sensorimotor cortex. For this reason, we chose to use logarithmic scales of the values, which are less sensitive to the wide SDs in the activation volumes. The small sample size leads to larger variances in the groups when outliers exist, and this can affect results of statistical analysis.

In the RT paradigm of D’Esposito et al (27), it was shown that five older subjects with no suprathreshold activation had slower mean RTs than those of younger subjects with suprathreshold activation. They found that the number of suprathreshold voxels in older subjects was four times less than that in younger subjects. These results raise the question as to whether an age or performance effect was seen (or both). This question is what generated the hypotheses that led to the present study.

It has been shown previously that there is an age-related diminution in activation volumes and amplitudes of signal in the motor cortex (28). Performance data are scarcer in the literature. In one odor-stimulated functional MR imaging study, Yousem et al (25) demonstrated that decrease in performance in odor identification and detection corresponds with decreases in the activation volume of olfactory eloquent areas. Older subjects with hyposmia either showed no activation of the olfactory eloquent cortex or showed decreased activation volumes compared with those in younger subjects (25). Since others (28) have noted an age-related decline in absolute and relative signal amplitude during blood oxygen level–dependent functional MR imaging motor tasks, we were careful to consider age effects in analyzing our data. The effects of age and RT probably intersect with respect to activation volumes.

The sex of the subjects could be another effect that influences the activation maps, as shown by results of previous positron emission tomographic (PET) and functional MR imaging studies (31–37). Although findings are not consistent, women display higher regional cerebral glucose metabolism and regional and global cerebral blood flow than those of men at rest and at stimulation in many PET studies (31–36). On the basis of the fact that women perform better than men in standardized odor identification and detection tests, Yousem et al (37) studied the effect of sex on odor-stimulated functional MR imaging. They demonstrated that the number of voxels activated in olfactory eloquent areas by women exceeded that of men by up to eight times. This report was another example of findings at functional MR imaging mirroring physiologic differences between men and women. With behavioral studies, some investigators (4,8,38,40) found that men were faster than women in different types of experimental tasks, while Noble et al (39) reported that RTs in women were slightly shorter than those of men in the 71–87-year age group. With four women and two men in the fast RT group and equal numbers of men and women in the slow RT group, we believe that the effects of sex were less likely to influence the results in the present study.

Although the positive association of RT with intelligence mentioned by Mathey (41) is another potential factor that could affect RTs, no participant scored below the normal values of intelligence quotients during neuropsychologic evaluation in our study. Moreover, we believe that the intelligence levels of the subjects are less likely to affect RT in the visuomotor task our subjects performed because of its simplicity.

Blood oxygen level-dependent functional MR imaging depends on local changes in blood flow and oxyhemoglobin and deoxyhemoglobin concentrations in the microvasculature, mediated by neurovascular coupling. A decrease in vascular supply, neuronal loss, changes in histologic structure of the microvasculature, and disturbance in neurovascular coupling may all result in diminution of change in signal amplitude and extension. Hence, we cannot separate the effects of these factors from each other. However, since recent experimental evidence (42) shows that the blood oxygen level-dependent response reflects synaptic and postsynaptic phenomena to a greater degree than those of action potentials, our data suggest that the greater signal intensity changes that accompany faster RTs are at least in part due to activation of a greater number of synapses within the sensorimotor cortex. Presumably, these have to occur in phase to result in generation of action potentials at the output neurons of the primary motor cortex. Whether this synaptic activation reflects input from nonprimary motor cortices or the thalamus or perhaps indirectly reflects input from visual cortices will ultimately require electrophysiologic investigation in nonhuman primates, coupled with elucidation of the relevant anatomic connections between the cortices and subcortices.

The present study has several limitations. It would have been beneficial to have more subjects in each group so that a random effects model could be generated to generalize the findings to whole populations. If the spread of subject ages was narrower and the ages and sexes were more closely matched, the results would have more validity. We could have used a higher resolution matrix, thinner sections, or surface coils to more readily depict individual gyri, but often this means extending the length of the study, and fatigue effects may enter the equation. We cannot explain why the activation volume in the left visual cortex was greater than that in the right on the group maps, other than to suggest that results of one study (43) indicated that mental image generation localizes more to the left side of the brain than to the right.

We did not explore use of both the right and left fingers in our study—we assumed that right-handed subjects with right index finger responses would be a simpler analysis. We must also explain why the subtraction image showed a greater difference between the fast and slow RT groups in the right sensorimotor cortex than in the left. While activation is known to be a bilateral process, the activation volume in the slow RT subjects must be less in the right sensorimotor cortex than in the left. Perhaps in the subjects with faster RTs, more supplemental motor cortices are activated to react more quickly.

In the present study, we did not use regression analysis to show effects of RT on activation. The study design was not meant to demonstrate correlations of RTs with activation, in part because we had such a large cluster of 12 individuals in our pool of 24 subjects who had tightly clustered intermediate RTs. The design was meant to compare and contrast two divergent study populations—slow versus fast RT groups—as in a case-cohort design.

In conclusion, since diminution in the activation volume may accompany an increase in RT, as defined on functional MR imaging activation maps, the performance of a subject given a RT task should be considered when interpreting functional MR imaging findings. This must be a variable that is accounted for in any RT study analysis in which the activation volumes between subjects are evaluated.


   FOOTNOTES
 
Abbreviation: RT = reaction time

Author contributions: Guarantor of integrity of entire study, D.M.Y.; study concepts, D.M.Y., M.A.K., V.D.C.; study design, D.M.Y., M.A.K.; literature research, N.M.B., K.K.O.; clinical studies, N.M.B., K.K.O.; data acquisition, N.M.B., K.K.O., D.M.Y., V.D.C., M.A.K.; data analysis/interpretation, N.M.B., K.K.O., V.D.C., C.W.; statistical analysis, C.W., V.D.C.; manuscript preparation, D.M.Y., N.M.B., K.K.O.; manuscript definition of intellectual content, D.M.Y., N.M.B., K.K.O., V.D.C.; manuscript editing, revision/review, and final version approval, all authors.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 

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