Original Article
Cerebral Glucose Metabolism in Adults with Hyperactivity of Childhood Onset
N Engl J Med 1990; 323:1361-1366November 15, 1990
- Abstract
- Abstract
Background and Methods.
The cause of childhood hyperactivity (attention deficit–hyperactivity disorder) is unknown. We investigated the hypothesis that cerebral glucose metabolism might differ between normal adults (controls) and adults with histories of hyperactivity in childhood who continued to have symptoms. Each patient was also the biologic parent of a hyperactive child. None of the adults had ever been treated with stimulant medication. To measure cerebral glucose metabolism, we administered 148 to 185 MBq (4 to 5 mCi) of [18F]fluoro-2-deoxy-D-glucose intravenously to 50 normal adults and 25 hyperactive adults while they performed an auditory-attention task. Images were obtained for 30 minutes with a Scanditronix positron-emission tomograph with a resolution of 5 to 6 mm. Whole-brain and regional rates of glucose metabolism were measured with computer assistance by two trained research assistants, working independently, who were blinded to the subjects' status (control or hyperactive).
Results.
Conclusions.
Glucose metabolism, both global and regional, was reduced in adults who had been hyperactive since childhood. The largest reductions were in the premotor cortex and the superior prefrontal cortex — areas earlier shown to be involved in the control of attention and motor activity. (N Engl J Med 1990; 323:1361–6.)
Media in This Article
Figure 1
Schematic Representation of the Regions Sampled.Figure 2
Regions of the Brain That Had Significantly Decreased Absolute Rates of Glucose Metabolism in Hyperactive Adults (N = 25) as Compared with Controls (N = 50).Article Activity
- Article
HYPERACTIVITY is a disorder of unknown cause that affects 2 to 4 percent of school-age children.1 , 2 Despite extensive efforts, researchers have been unable to demonstrate consistent neurobiologic differences between hyperactive children and normal controls.3 , 4 Therefore, the validity of hyperactivity as a syndrome remains controversial,5 as does its treatment with stimulant medication.6 Using positron-emission tomography (PET) of the brain with use of [18F]fluoro-2-deoxy-D-glucose, a technique that permits the measurement of regional glucose metabolism, we studied this disorder in hyperactive adults. Adults were chosen as subjects because of ethical concerns about exposing children to a radioactive tracer. A pilot study7 found evidence suggestive of depressed global cerebral glucose metabolism and possible frontal hypometabolism in the brains of hyperactive adults. In this study we have confirmed the findings of abnormal regional and global glucose metabolism in the brains of adults with hyperactivity.
The symptoms of hyperactivity (recently renamed attention deficit–hyperactivity disorder)8 are motor restlessness, attentional difficulties, distractibility, and impulsiveness. The disorder is probably inherited in certain families, as reported by Biederman et al.,9 and symptoms persist into adulthood in 40 to 60 percent of persons with childhood hyperactivity.10 , 11 Neurochemical studies of patients with this disorder document a large number of possible abnormalities, but no consistent finding has emerged to implicate a specific neurotransmitter, modulator, or neuroanatomical substrate.3 , 4
Earlier neuroanatomical imaging studies12 of patients with attention deficit disorder with hyperactivity either have found no abnormality or have included large numbers of subjects with substance-abuse disorder,13 making it difficult to determine whether the findings were secondary to chronic drug use or part of the syndrome. In addition, in the studies by Lou et al. of cerebral blood-flow abnormalities in attention deficit disorder with hyperactivity,14 , 15 there was a large discrepancy in age between the patients and controls, and the study included subjects with developmental dysphasia and mental retardation.
To improve on these earlier studies, we examined cerebral glucose metabolism rather than blood flow and used a scanner with considerably higher resolution. In addition, the patients in our study had not been treated with stimulants and had no history of substance abuse. We decided to study hyperactive adults who were the biologic parents of children given a diagnosis of attention deficit disorder with hyperactivity because familial hyperactivity might increase the likelihood of identifying a biologic determinant of the disorder. As children, these parents were themselves hyperactive. Biederman et al.16 reported that 28.6 percent of the biologic parents of hyperactive children also had a history of hyperactivity. The parents in our study continued to have symptoms as adults and, with three exceptions, were living with their hyperactive children.
Methods
This study was approved by the Human Subjects Protection Committee of the National Institute of Mental Health, and informed consent was obtained from all the subjects.
Sample
Fifty healthy normal adults (28 men and 22 women; mean age [±SD], 36.3±11.7 years) participated in the study as controls and were assessed in a semistructured psychiatric interview by a staff psychiatrist. Forty-five of the controls were right-handed, and five were left-handed. The presence of a serious medical or psychiatric problem in the subject or of psychiatric disorder in a first-degree relative led to exclusion from the study. The 25 patients (18 men and 7 women; mean age, 37.4±6.9 years) were included if, in semi-structured interviews, they reported a definite childhood history of attention deficit disorder with hyperactivity that met the criteria of the Diagnostic and Statistical Manual of Mental Disorders (third edition, not revised), met the Utah criteria for attention deficit disorder in adulthood,17 were the biologic parents of children given a diagnosis of attention deficit disorder with hyperactivity, and had no history of other major psychiatric disorders, including alcohol or substance-abuse disorders or conduct disorder. All the patients continued to have considerable difficulty with both restlessness and inattentiveness as adults. Twenty were right-handed, and five were left-handed. The characteristics of the patients and controls are shown in Table 1Table 1
Characteristics of Patients and Controls.*. Specific developmental disorders (i.e., difficulty with reading or arithmetic) were evaluated in all but one patient but were not grounds for exclusion.The presence of other psychiatric disorders and their severity were assessed with use of the Schedule for Affective Disorders and Schizophrenia (lifetime version),18 modified to detect personality disorders. A modified version of the Abbreviated Conners' Rating Scale (the Parents Rating Scale17), which measures the severity of symptoms of hyperactivity, was completed retrospectively by the parents of the hyperactive adults, by the adults with hyperactivity, and independently by their spouses. The Global Assessment Scale19 was also completed by one of us who is a psychiatrist. Within two months of the PET scan, all the patients and 15 of the normal control group completed a short form of the Wechsler Adult Intelligence Scale, Revised (WAIS-R), which yields an IQ that correlates highly (r = 0.96) with that derived from the full test.20
Finally, our assessment included the collection of socioeconomic data, including estimated social class, details of previous and current alcohol use, and information on any problems with the law. Both patients and controls had taken no medications for a minimum of three weeks before the PET scan. None of the patients had been treated at any time with stimulant medication.
Positron-Emission Tomography
A computerized auditory-attention task was performed by all the patients and controls during the PET scan. The task was chosen because our earlier work21 had localized its effects on cortical metabolism. Moreover, the task was used to control for extraneous environmental stimulation as well as internal mental activity. In this task (an auditory continuous-performance test), the subjects were asked to press a hand-held response button to indicate the lowest-intensity tone (target, 67 dB) of three tones 1 second in duration presented in random order (all at 500 Hz) with intervals of 2 seconds between the tones.22 With their eyes covered, the subjects began the auditory-attention task several minutes before the injection of 148 to 185 MBq (4 to 5 mCi) of [18F]fluoro-2-deoxy-D-glucose and completed the task 35 minutes after the injection. Standard instructions and test procedures were used for the task, including training before the scan to ensure the subjects' adequate understanding of the test. The auditory-attention task was computer-generated, so that the identical task was presented to both patients and controls. Tracer-input curves were calculated on the basis of blood samples drawn from a radial-artery catheter. In the course of the PET scan, 28 images ("slices") were obtained for each subject, starting 5 mm above the plane parallel to the canthomeatal line. The interval between slices was approximately 3.5 mm, and the scans were obtained with a Scanditronix scanner with 5-to-6-mm full-width half-maximum in plane resolution. Correction for attenuation was made with a transmission scan. A custom-fitted plastic head holder immobilized the subject's head. Immediately after the completion of the PET-scan procedure, all subjects were asked to rate their anxiety level during the attention task and scanning on a Spielberger scale.
Raw pixel values were converted to metabolic rates for glucose.23 , 24 For the determination of regional rates of glucose metabolism, 60 regions of interest were measured in five standard planes by two trained research assistants, working independently, who were unaware of the identity and diagnosis of the persons they were evaluating. The results, as determined by the two research assistants, were essentially identical, with an average correlation coefficient for 60 regions of r = 0.95 within the groups of controls and patients. Therefore, only one set of values is presented. Data on test—retest variability on positron-emission tomography for individual subjects is unavailable because we were concerned about the ethics of exposing research subjects to additional radiation.
The global rates of glucose metabolism reported here are estimates of the average value for glucose metabolism obtained for all the gray matter—rich areas of the cortex we examined. Regional glucose-metabolism rates are averages of the normalized data on glucose metabolism obtained for the region of interest. Normalization was performed by dividing a subject's absolute glucose-metabolism rate for the region of interest by his or her global glucose-metabolism rate (region/global). This procedure is similar in principle to the reference-ratio or "landscape" method.25 It is designed to minimize the effect of individual variations in global glucose metabolism on regional metabolism. All PET scans (in controls and patients) were obtained during a 36-month period.
Statistical Analysis
We used unpaired Student's t-tests (uncorrected for the number of comparisons) for comparisons between controls and patients. Despite data from a pilot study7 that provided an a priori hypothesis, two-tailed t-tests were used to evaluate conservatively the large number of regions examined (n = 60).
Results
Sample
As Table 1 shows, the patients were generally from the upper middle class and had had minimal problems with alcohol or the law. They were well matched with the normal controls with respect to age, IQ, socioeconomic status, and education, although the control group included more women than the patient group (44 percent vs. 28 percent). On average, the patients were rated higher than 98 percent of normal persons with respect to their symptom-deviance score on the Parents Rating Scale.17 The average rating on the Global Assessment Scale indicated that patients were "mildly impaired in multiple settings." Their mean full-scale IQ (from the WAIS-R) was slightly above average. On average, achievement scores were commensurate with educational level, although six patients had clear histories of learning problems, with documented disabilities (five in reading and one in arithmetic).
Glucose Metabolism
As assessed by PET scanning, global cerebral glucose metabolism was 8.1 percent lower in the hyperactive patients than in the controls (9.05± 1.20 mg per minute per 100 g vs. 9.85±1.68 mg per minute per 100 g; two-tailed P = 0.034).
Absolute regional glucose-metabolism rates differed significantly between the two groups (P<0.05, 70 to 73 df, by two-tailed t-test) for 30 of the 60 specific brain regions we studied (Fig. 1Figure 1
Schematic Representation of the Regions Sampled. and 2Figure 2Regions of the Brain That Had Significantly Decreased Absolute Rates of Glucose Metabolism in Hyperactive Adults (N = 25) as Compared with Controls (N = 50).). In all 30, including both cortical and subcortical regions, metabolism in the patients was depressed.When the values for the individual regions of interest were normalized (divided by the global glucose values, as described in Methods), four regions, primarily in the premotor and somatosensory cortex, had significantly lower metabolism in the patients than in the controls (Fig. 3Figure 3
Regions of the Brain That Had Significantly Decreased Normalized Rates of Glucose Metabolism in Hyperactive Adults (N = 25) as Compared with Controls (N = 50). and 4Figure 4
Representative Transverse Images (Left, Normal Control; Right, Patient with Attention-Deficit Disorder with Hyperactivity) through Plane A, Approximately 94 mm above the Canthomeatal Line.). Because these four regions were tightly clustered in one area of the brain, correlations among the values for the four were examined in the controls. The Pearson correlation coefficients ranged from —0.27 to 0.33 (mean, 0.17). Only two regions were significantly correlated at the 0.05 level, and this correlation explained less than 10 percent of the variance.Total brain size, as measured by pixel counts, did not differ significantly between the hyperactive patients and the controls.
Results of Continuous-Performance Testing
Our analysis of the patients' performance on the auditory-discrimination task during the PET scan did not identify significant differences between the groups in the number of errors of commission or omission or in the proportion of correct identifications. The controls correctly identified a mean (±SD) of 166.2±46.5 tones of a possible 210, whereas the hyperactive patients identified 167.9±34.0. The controls made 16.2±33.0 errors of commission, whereas the patients made 9.2± 14.0. The subjective ratings of anxiety level during the test and scan did not differ between the groups.
Effects of Sex
Global glucose metabolism was 1.9 percent higher in the brains of the women with hyperactivity than in those of the men with hyperactivity (9.24±1.13 mg per minute per 100 g vs. 9.07±1.21 mg per minute per 100 g; P not significant). The metabolic data were analyzed both for men only (18 patients vs. 28 controls) and for women only (7 patients vs. 22 controls). The results for men only were similar to those for all the subjects considered together. Among the men, global cerebral glucose metabolism was 6.0 percent lower in the hyperactive patients than in the controls (9.14±1.29 mg per minute per 100 g vs. 9.72±1.32 mg per minute per 100 g), but the difference was not significant. When global cerebral glucose metabolism was compared in the 7 hyperactive women and the 22 normal women, it was found to be 12.7 percent lower in the hyperactive women (9.02±1.29 mg per minute per 100 g vs. 10.33±2.07 mg per minute per 100 g), but the difference was not significant.
We used two-way analysis of variance to examine the interaction of sex and diagnosis; no significant effect was found (F = 0.52, P>0.47). Therefore, the 12.7 percent reduction in glucose metabolism in women with hyperactivity, as compared with normal women, was not significantly different from the 6.0 percent reduction in men with hyperactivity.
Learning Disabilities
When the six subjects with current disabilities in reading and arithmetic, documented by test scores, were excluded from the data analysis, all the previously significant differences in regional and global cerebral glucose metabolism retained statistical significance. No significant differences were found in global cerebral glucose metabolism between patients with hyperactivity who had current learning deficits and those who did not.
Discussion
Despite the limitations of previous blood-flow14 , 15 and CT12 , 13 studies, our data are, in general, consistent with the results of earlier work, including our own pilot PET study7 of a separate sample of patients with hyperactivity. In that study, in which we used an older scanner (ECAT II), we found both a significant global decrease in cerebral glucose metabolism and a trend toward a reduction in metabolism in the anterior frontal region. It is unlikely that these findings were the results of differences in brain size or degree of atrophy, since the total size of the brain (measured by pixel counts) was not significantly different between the patient and control groups. Finally, although our statistical approach did not correct for the large number of t-tests, the number of regions found to be significantly different from normal in the patients with hyperactivity (30 of 60 in absolute metabolic rate) argues convincingly against a Type I error. The finding that 4 of 60 regions had significantly depressed normalized metabolic rates could be explained by chance alone and thus requires replication.
The adult patients with hyperactivity whom we studied had symptoms but were less severely impaired than earlier follow-up studies of similar patients10 , 11 would suggest, especially in terms of substance abuse and problems with the law. This difference is most likely due to our eligibility criteria and to the selection bias inherent in studying parents from intact families of currently identified hyperactive children. Nonetheless, we detected significant defects in cerebral glucose metabolism. Studies of a more severely impaired population might reveal even more extensive abnormalities.
The patients and controls did not perform differently on the continuous-performance test. The test was designed to be easy enough to yield performance measures for even the most seriously impaired subjects, such as patients with schizophrenia and hallucinations. The normal controls, on average, correctly identified 166 target stimuli (tones) out of a possible 210, against a background of about 450 incorrect targets. The patients with hyperactivity might have performed less well on a more difficult task. The literature on the development of attentional skills in persons with hyperactivity, as measured by such tests as the continuous-performance test (reviewed by Klorman26), indicates that adolescents with hyperactivity continue to perform less well than other subjects on measures of attention.
On the basis of our anatomical localization of the ability to perform this particular continuous-performance test in normal subjects21 (the right middle prefrontal area), the reduced metabolism we noted in the hyperactive group does not appear to be specific to this task and cerebral glucose metabolism should therefore be evident in hyperactive patients at rest.
We feel confident that neither the small number of women in our sample nor the presence of patients with specific reading or arithmetic disabilities accounts for the differences we observed between patients and controls. That the inclusion of these subgroups had only a minimal effect on the data provides evidence in support of the association of metabolic abnormalities with the specific syndrome of hyperactivity.
Although the differences between the groups in the normalized metabolic rates appear in Figure 3 to have been confined to the left brain, inspection of the metabolic differences in the right brain revealed similar reductions in the patients, as compared with the controls, that did not reach statistical significance. Thus, the absolute differences that we observed in cerebral glucose metabolism were widespread, unidirectional, and bilateral. The areas with the greatest depression in glucose metabolism (as judged by the levels of significance of the differences between the groups) include but are not limited to the premotor and superior prefrontal regions.
Our findings support speculation27 , 28 that the frontal lobes may have a role in the pathophysiologic processes of hyperactivity, as do the recent results of neuropsychological tests of frontal-lobe function in children with attention deficit disorder with hyperactivity.29 The data, however, do not rule out a more general role for abnormal "arousal" in this disorder. These findings raise three main questions about the pathophysiologic nature of hyperactivity: Why is hypometabolism seen in patients with hyperactivity? Are the results reported here consistent with those of existing studies of prefrontal and premotor functioning in humans and nonhuman primates? Could these abnormal findings lead to the symptoms of attention deficit disorder with hyperactivity (motor restlessness, impulsiveness, and inattentiveness)?
The prefrontal areas are important biologic determinants of attention.30 Disorders of the prefrontal regions often result in inattentiveness, distractibility, and an inability to inhibit inappropriate responses.30 Wise's review31 of the literature on the premotor cortex concludes that the premotor cortex has a role in the preparation of specific voluntary movement, especially movement that depends on external cues. Defects in these regions could produce motor restlessness, particularly if the premotor areas normally inhibit other areas responsible for motor behavior in the adjacent motor cortex. For example, the premotor cortex appears to be critical in the "suppression of relatively automatic responses to certain sensory stimuli."32 Clinically, hyperactive children commonly have difficulties because of their constant calling out in class, verbal interruptions, and, in general, acting before thinking.
Important differences in absolute metabolic rates were not confined to the frontal regions in our study, however. The reductions in glucose metabolism in left parietal, temporal, and rolandic structures (the last bilateral), in addition to subcortical structures, are more difficult to incorporate into a comprehensive theory of the pathophysiology of this disorder.
In summary, we noted differences in cerebral glucose metabolism between hyperactive adults and normal adult controls, specifically in regions of the brain that have been postulated to be important in the control of preparation for motor activity, motor activity itself, inhibition of inappropriate response, and attention.
We are indebted to Nancy Etzel, Cheryl Credle, Precious Thomas, Garrett Bagley, Glinda Fitzgerald, Jerry Foer, Ashley Hanahan, and the positron-emission—tomography technologists at the National Institutes of Health for technical assistance and to John Werry, M.D., for his critical review of the manuscript.
Source Information
From the Section on Clinical Brain Imaging, Laboratory of Cerebral Metabolism (A.J.Z., T.E.N., M.G., A.C.K., W.E.S., R.M.C.), and the Child Psychiatry Branch (J.R., S.H.), National Institute of Mental Health, Bethesda, Md. Address reprint requests to Dr. Zametkin at the Section on Clinical Brain Imaging, National Institute of Mental Health, NIH, Bldg. 10 4N317, 9000 Rockville Pike, Bethesda, MD 20892.
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