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(Radiology. 2000;215:470-475.)
© RSNA, 2000

Neuroradiology

Limbic Lobe of the Human Brain: Evaluation with Turbo Fluid-attenuated Inversion-Recovery MR Imaging1

Toshinori Hirai, MD, Yukunori Korogi, MD, Kazuhiro Yoshizumi, MD, Yoshinori Shigematsu, MD, Takeshi Sugahara, MD and Mutsumasa Takahashi, MD

1 From the Department of Radiology, Kumamoto University School of Medicine, 1-1-1 Honjo, Kumamoto 860, Japan. From the 1998 RSNA scientific assembly. Received January 13, 1999; revision requested March 17; revision received August 11; accepted August 25. Address correspondence to T.H.


   Abstract
TOP
 Abstract
Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
PURPOSE: To determine whether brain cortices have different signal intensities on turbo fluid-attenuated inversion-recovery (FLAIR) magnetic resonance (MR) images.

MATERIALS AND METHODS: Coronal 5-mm-thick turbo FLAIR MR images in 56 neurologically normal patients (27 male and 29 female patients; age range, 12–73 years; mean age, 47 years) were evaluated retrospectively. Cortical signal intensities in the amygdala, hippocampus, cingulate gyrus, subcallosal area, insula, temporal lobe, parietal lobe, and occipital lobe were graded relative to cortical signal intensity in the frontal lobe. Contrast-to-noise ratios were compared for each cortical area.

RESULTS: Increased signal intensity was frequently seen in the amygdala, hippocampus, cingulate gyrus, and subcallosal area, regardless of patient age. Signal intensities of temporal, parietal, and occipital cortices were similar to that of frontal cortex, and signal intensity of the insula was slightly higher than that of frontal cortex. There were no significant differences with respect to sex and laterality, whereas significant differences were found among cortical regions (P < .01). The contrast-to-noise ratios of the amygdala, hippocampus, cingulate gyrus, and subcallosal area were significantly greater than those of all other gray matter structures (P < .05).

CONCLUSION: On turbo FLAIR images, high signal intensities of cortices of the limbic lobe are frequently seen in neurologically normal brain. These findings should not be considered abnormal.

Index terms: Brain, cortex, 13.91, 14.91 • Brain, gray matter, 13.91, 14.91 • Brain, MR, 13.121413, 14.121413


   Introduction
TOP
 Abstract
 Introduction
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
The cortex of the human brain can be divided into six regions: the frontal, parietal, temporal, occipital, and limbic lobes and the insula. Although the contrast between cortical gray matter and white matter is easily seen on computed tomographic and conventional magnetic resonance (MR) images, to our knowledge the variations in contrast among different areas of cortical gray matter have not been described.

Increased signal intensity in the limbic lobe on MR images obtained with a long repetition time has been reported (1–9) in patients with mesial temporal sclerosis and paraneoplastic limbic encephalitis. Recently, fluid-attenuated inversion-recovery (FLAIR) MR sequences that null the signal from cerebrospinal fluid and produce heavily T2-weighted images have been widely applied. The usefulness of FLAIR sequences for help in the assessment of various pathologic conditions has been described (10–13). It has also been reported (14) that FLAIR sequences are highly accurate for pathologic determination of mesial temporal sclerosis. However, we have often encountered high signal intensity on routine MR studies of the limbic lobe in neurologically healthy individuals. To our knowledge, there are no reports on whether the normal limbic lobe is hyperintense on FLAIR MR images.

To recognize abnormally increased signal intensity in the limbic lobe on FLAIR images, it is necessary to have reference standards for normal or physiologically hyperintense cerebral cortices. The purpose of this study was to determine whether the brain cortices have different signal intensities on turbo FLAIR MR images according to cortical location.


   MATERIALS AND METHODS
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
This study included 56 patients (27 male and 29 female patients) aged 12–73 years (mean, 47 years) who were selected from a consecutive series of patients referred for routine MR imaging. The MR images were reviewed retrospectively. MR imaging had been performed with a 1.5-T system (Gyroscan ACS-NT; Philips Medical System, Best, the Netherlands) equipped with a head coil.

The following criteria were used for inclusion in the study: no clinical evidence of neurologic disease and a normal brain MR study. The MR images were reviewed in consensus by two neuroradiologists (T.H., Y.S.). A chart review was conducted to document the normal neurologic examination results and normal neurologic history for each patient. We excluded patients with a history of neurologic disease, malignancy, stroke, or brain surgery. The distribution of the patients by age is shown in Table 1. Indications for MR imaging included headache (n = 36), dizziness (n = 11), paresthesia or dysesthesia (n = 6), psychiatric problems (n = 2), and tinnitus (n = 1).


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  		TABLE 1. Distribution of Patients according to Age and Sex
 
Turbo FLAIR MR imaging was performed in the orthogonal coronal plane with the following parameters: 6,000/120/2,000 (repetition time msec/effective echo time msec/inversion time msec), echo train length of 17, 256 x 256 matrix, one signal acquired, 5-mm section thickness, and 23-cm field of view.

The superior frontal gyrus was used for reference. The signal intensities of the amygdala, hippocampus, cingulate gyrus, subcallosal area, insula, superior frontal gyrus (frontal cortex), superior parietal lobule (parietal cortex), calcarine gyrus (occipital cortex), and superior temporal gyrus (temporal cortex) were interpreted in consensus by two neuroradiologists (T.H., Y.S.). The signal intensities of these regions were classified according to five grades: grade 1 was assigned for signal intensity definitely less than that of cortical gray matter; grade 2, for signal intensity slightly less than that of cortical gray matter; grade 3, for signal intensity equal to that of cortical gray matter; grade 4, for signal intensity slightly greater than that of cortical gray matter; and grade 5, for signal intensity definitely greater than that of cortical gray matter.

The signal intensity of each cortex was measured on FLAIR MR images of 112 cerebral hemispheres in 56 patients by using a region-of-interest function at the MR imager console. Background signal intensities were measured in the frontal lobe white matter. An image noise measurement was determined by recording the SD of the signal intensity within a region of interest outside the head (ie, in air). The contrast-to-noise ratios (CNRs) were calculated as follows: CNR = (SIcortex - SIb)/SDnoise, where SIcortex is the signal intensity of the cortex, SIb is the signal intensity of background, and SDnoise is the SD of signal intensity of air as a measure of noise.

With respect to male and female patients and left and right hemispheres, CNR differences in each cortex were tested with a two-way analysis of variance for multiple comparisons. Once the statistically significant CNR differences were identified in the location of the cortex, the Tukey studentized range test was performed. The data are presented as the mean plus or minus the SD. A P value of less than .05 was considered to indicate a statistically significant difference.


   RESULTS
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
Increased signal intensity (grade 5) was frequently seen in the amygdala, hippocampus, cingulate gyrus, and subcallosal area, regardless of patient age (Figs 1, 2). Signal intensities in the temporal, parietal, and occipital cortices were equal to (grade 3) or slightly less than (grade 2) that in frontal lobe cortex, and signal intensity in the insula often was slightly higher (grade 4) than that in frontal cortex (Fig 3).



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  		Figure 1a. Coronal turbo FLAIR brain MR images (6,000/120/2,000) in a 34-year-old woman. Double-headed arrow = phase-encoding direction. (a) Image obtained at the level of the frontal horn of the lateral ventricle shows high signal intensity (grade 5) in the subcallosal area (large arrows) and cingulate gyrus (small arrows) relative to that in frontal cortical gray matter (arrowheads). (b) Image obtained at the level of the third ventricle shows high signal intensity (grade 5) in the amygdala (thick solid arrows) relative to that in the frontal cortical gray matter (arrowheads). Signal intensity of the insula (open arrows) is slightly higher (grade 4) than that of the frontal cortex. Signal intensity of the temporal cortices (thin solid arrows) was similar (grade 3) to that of frontal lobe cortex. (c) Image obtained at the level of the red nuclei shows high signal intensity (grade 5) in the hippocampus (arrows) relative to that in frontal cortical gray matter (arrowheads).

 


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  		Figure 1b. Coronal turbo FLAIR brain MR images (6,000/120/2,000) in a 34-year-old woman. Double-headed arrow = phase-encoding direction. (a) Image obtained at the level of the frontal horn of the lateral ventricle shows high signal intensity (grade 5) in the subcallosal area (large arrows) and cingulate gyrus (small arrows) relative to that in frontal cortical gray matter (arrowheads). (b) Image obtained at the level of the third ventricle shows high signal intensity (grade 5) in the amygdala (thick solid arrows) relative to that in the frontal cortical gray matter (arrowheads). Signal intensity of the insula (open arrows) is slightly higher (grade 4) than that of the frontal cortex. Signal intensity of the temporal cortices (thin solid arrows) was similar (grade 3) to that of frontal lobe cortex. (c) Image obtained at the level of the red nuclei shows high signal intensity (grade 5) in the hippocampus (arrows) relative to that in frontal cortical gray matter (arrowheads).

 


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  		Figure 1c. Coronal turbo FLAIR brain MR images (6,000/120/2,000) in a 34-year-old woman. Double-headed arrow = phase-encoding direction. (a) Image obtained at the level of the frontal horn of the lateral ventricle shows high signal intensity (grade 5) in the subcallosal area (large arrows) and cingulate gyrus (small arrows) relative to that in frontal cortical gray matter (arrowheads). (b) Image obtained at the level of the third ventricle shows high signal intensity (grade 5) in the amygdala (thick solid arrows) relative to that in the frontal cortical gray matter (arrowheads). Signal intensity of the insula (open arrows) is slightly higher (grade 4) than that of the frontal cortex. Signal intensity of the temporal cortices (thin solid arrows) was similar (grade 3) to that of frontal lobe cortex. (c) Image obtained at the level of the red nuclei shows high signal intensity (grade 5) in the hippocampus (arrows) relative to that in frontal cortical gray matter (arrowheads).

 


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  		Figure 2a. Bar graphs show distribution of signal intensity grades on FLAIR MR images according to patient age for (a) amygdala, (b) hippocampus, (c) cingulate gyrus, and (d) subcallosal area in neurologically healthy patients. Grade 5 signal intensity was frequently seen in the limbic cortices regardless of patient age. The frequency of grade 5 signal intensity was higher in the hippocampus (b).

 


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  		Figure 2b. Bar graphs show distribution of signal intensity grades on FLAIR MR images according to patient age for (a) amygdala, (b) hippocampus, (c) cingulate gyrus, and (d) subcallosal area in neurologically healthy patients. Grade 5 signal intensity was frequently seen in the limbic cortices regardless of patient age. The frequency of grade 5 signal intensity was higher in the hippocampus (b).

 


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  		Figure 2c. Bar graphs show distribution of signal intensity grades on FLAIR MR images according to patient age for (a) amygdala, (b) hippocampus, (c) cingulate gyrus, and (d) subcallosal area in neurologically healthy patients. Grade 5 signal intensity was frequently seen in the limbic cortices regardless of patient age. The frequency of grade 5 signal intensity was higher in the hippocampus (b).

 


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  		Figure 2d. Bar graphs show distribution of signal intensity grades on FLAIR MR images according to patient age for (a) amygdala, (b) hippocampus, (c) cingulate gyrus, and (d) subcallosal area in neurologically healthy patients. Grade 5 signal intensity was frequently seen in the limbic cortices regardless of patient age. The frequency of grade 5 signal intensity was higher in the hippocampus (b).

 


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  		Figure 3a. Bar graphs show distribution of signal intensity grades on FLAIR MR images according to patient age for (a) insula, (b) temporal cortex, (c) parietal cortex, and (d) occipital cortex in neurologically healthy patients. Grade 2 or 3 signal intensity was seen in the temporal, parietal, and occipital cortices, whereas grade 4 signal intensity was frequently seen in the insula.

 


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  		Figure 3b. Bar graphs show distribution of signal intensity grades on FLAIR MR images according to patient age for (a) insula, (b) temporal cortex, (c) parietal cortex, and (d) occipital cortex in neurologically healthy patients. Grade 2 or 3 signal intensity was seen in the temporal, parietal, and occipital cortices, whereas grade 4 signal intensity was frequently seen in the insula.

 


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  		Figure 3c. Bar graphs show distribution of signal intensity grades on FLAIR MR images according to patient age for (a) insula, (b) temporal cortex, (c) parietal cortex, and (d) occipital cortex in neurologically healthy patients. Grade 2 or 3 signal intensity was seen in the temporal, parietal, and occipital cortices, whereas grade 4 signal intensity was frequently seen in the insula.

 


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  		Figure 3d. Bar graphs show distribution of signal intensity grades on FLAIR MR images according to patient age for (a) insula, (b) temporal cortex, (c) parietal cortex, and (d) occipital cortex in neurologically healthy patients. Grade 2 or 3 signal intensity was seen in the temporal, parietal, and occipital cortices, whereas grade 4 signal intensity was frequently seen in the insula.

 
In the multiple comparisons, there were no statistically significant differences with respect to sex (Table 2) or laterality (Table 3), whereas statistically significant differences were found among cortical regions (P < .01). The nine cortical areas we studied were classified into four groups. In one group, which comprised the amygdala, hippocampus, cingulate gyrus, and subcallosal area, the CNRs were significantly greater (P < .05) than those of all other gray matter structures (Fig 4). The subcallosal area and insula formed a second group, and the frontal cortex formed a third. The fourth group, which comprised the temporal, parietal, and occipital lobe cortices, showed the smallest CNRs.


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  		TABLE 2. CNR according to Laterality
 

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  		TABLE 3. CNR according to Patient Sex
 


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  		Figure 4a. Box and whisker plots show mean CNRs measured in each cortex from 112 cerebral hemispheres with attention to (a) laterality (left [L] vs right [R] hemisphere) and (b) sex (male [M] vs female [F] patients). The boxes represent the first through third quartiles for CNR measurements; horizontal lines in boxes represent the median CNR, and error bars (whiskers) indicate the first and 99th percentiles for CNR measurements. Am = amygdala, Cin = cingulate gyrus, Fro = frontal lobe cortex, Hip = hippocampus, Ins = insula, Occ = occipital lobe cortex, Par = parietal lobe cortex, Sub = subcallosal area, Tem = temporal lobe cortex.

 


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  		Figure 4b. Box and whisker plots show mean CNRs measured in each cortex from 112 cerebral hemispheres with attention to (a) laterality (left [L] vs right [R] hemisphere) and (b) sex (male [M] vs female [F] patients). The boxes represent the first through third quartiles for CNR measurements; horizontal lines in boxes represent the median CNR, and error bars (whiskers) indicate the first and 99th percentiles for CNR measurements. Am = amygdala, Cin = cingulate gyrus, Fro = frontal lobe cortex, Hip = hippocampus, Ins = insula, Occ = occipital lobe cortex, Par = parietal lobe cortex, Sub = subcallosal area, Tem = temporal lobe cortex.

 

   DISCUSSION
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
The limbic lobe is situated at the inferomedial aspect of the cerebral hemispheres and consists of two concentric gyri surrounding the corpus callosum. Broca (15) named the larger outer gyrus the limbic gyrus and the smaller inner one the intralimbic gyrus. The limbic gyrus consists of the parahippocampal gyrus, the isthmus of the cingulate gyrus, and the subcallosal area; the intralimbic gyrus consists of the hippocampus proper, the dentate gyrus, and the indusium griseum.

The hippocampus consists of two interlocking laminae of gray matter: the horn of Ammon and the dentate gyrus. In terms of cellular composition of the cortex, the limbic lobe has a different structure and is usually divided into two cortices: the allocortex, which includes the hippocampus (horn of Ammon and dentate gyrus), the proximal part of the subiculum, and the indusium griseum; and the periallocortex, which includes the cingulate and parahippocampal gyri and is composed of transitional cortex between the allocortex and isocortex (or neocortex) (16–18). The amygdala is often included in the former group.

The variation of T2 in brain tissue has been described (19–21). Although variation due to factors such as water diffusion, cellular morphology, composition of cytoplasmic and extracellular spaces, and iron concentration are expected, the cause of the relatively wide range in T2 is not understood.

The signal intensity of the limbic cortical areas was greater than that of the isocortical areas. This may be explained in terms of the following points. First, the water content of brain tissue varies according to location. In vivo water content measurements have been obtained by means of gravimetric assays of brain tissue. The values for white matter water content range from 0.70 to 0.72 g of water per gram of tissue, and those for gray matter range from 0.82 to 0.85 (22–24). To our knowledge, however, there are no reports of measurements of the differences in brain water content among the cortices with this method. Whittall et al (21) measured the water content in normal human brain by using T2 decay curves. In their study, the mean water content of the cingulate gyrus and insular cortex was greater than that of gray matter in the isocortex. In our study, the signal intensities of the cingulate gyrus and insular cortex were greater than that of isocortical gray matter. The water content of gray matter may affect signal intensity on FLAIR MR images.

The second point concerns the cellular composition of the cortex. Among the cortices of the limbic lobe, the hippocampus had the highest signal intensity. The hippocampus has a different cellular composition than that of the other cortices. The horn of Ammon and dentate gyrus of the hippocampus, which has three layers of neurons, are the simplest and most primitive parts of the cortex (allocortex), as compared with the more complex and developed isocortex, which has the usual six layers of neurons (16–18). In our study, the signal intensities of the periallocortex and the allocortex were higher than that of the isocortex. Cortical signal intensity on FLAIR images might be correlated with the cellular composition induced by cortical development.

The third point is related to vascularization of the cortex. The vascularization of gray matter in human brain varies according to location. The hippocampal vascular network differs in many respects from that of the isocortex (25–27). The long tangential course of arteries and veins in the hippocampus contrasts with the pattern of isocortical blood vessels, which follow a course perpendicular to the surface, with a palisade aspect. There also are differences in the density of capillary networks in many gray matter regions. A high-density capillary network is seen in the hippocampus. In its structure, the molecular layers of the horn of Ammon and dentate gyrus, both of which are poor in neurons, show the highest vascular density. Thus, vascularization of the cortex might be associated with signal intensity on FLAIR images.

Among the isocortical areas, the signal intensity of the frontal cortex was higher than that of the other isocortical areas. This could be due to the iron content of the cortex. Hallgren and Sourander (28) reported quantitative age-related measurements of nonheme iron in the human brain. They mentioned that the iron content in the cerebral isocortex increases with age. The frontal cortex shows the lowest iron levels among cerebral isocortical areas, with iron content that is nearly 3.0 mg per 100 g of tissue in patients older than 60 years. Cortical signal intensity increases as the cortical content of nonheme iron decreases. Thus, our quantitative results corresponded to the histochemical findings of Hallgren and Sourander. Although FLAIR sequences may have a limitation with regard to detection of the effects of magnetic susceptibility due to the use of a fast spin-echo technique (29), iron content may affect the signal intensity of the cerebral cortex.

It has been reported (7–9) that increased signal intensity in the hippocampus on T2-weighted images is a useful MR imaging finding for the diagnosis of mesial temporal sclerosis. Jack et al (14) mentioned that the FLAIR sequence provides high accuracy for the diagnosis of mesial temporal sclerosis. Limbic encephalitis has been characterized in terms of high signal intensity in the medial temporal lobe, which can sometimes be identified on T2-weighted MR images. The most commonly involved sites in cases of limbic encephalitis include the hippocampus, amygdala, and other medial temporal lobe structures. Because the normal hippocampus is frequently seen as a high-signal-intensity structure on FLAIR MR images, careful evaluation of this structure is needed. Knowledge of the appearance of the limbic lobe on FLAIR images of normal brain is important to the recognition of these disorders.

This study had some limitations. First, frontal lobe white matter was used as the background tissue for the quantitative analysis. Although the iron content of white matter increases with age, that of the frontal lobe remains nearly stable over the age of 30 years (28). Because most of the patients in our study were older than 30 years, we believe that the effect of iron content was small and that frontal white matter could be used as a reference background.

Second, it may be difficult to visually assess signal intensity differences among cortices depicted on different sections. The parietal and occipital cortices are not located on the same section as the frontal cortex on coronal images. However, it was easy to visually assess the signal intensity of each cortical area of the limbic lobe, because most of these cortices are located in the same plane on coronal images as the frontal cortex. The use of the frontal cortex as a reference seems to be suitable for evaluation of the limbic lobe. Although surrounding structures might have some effect on our visual grading, we believe that our grades correlated with cortical signal intensity because our visual grading results showed good agreement with our quantitative results.

Third, partial volume effects may have presented a limitation. We used images with a section thickness of 5 mm with a 1-mm intersection gap. Partial volume effects may not be negligible when evaluating cortical signal intensity. Brain atrophy, especially cortical atrophy, associated with aging might affect cortical signal intensity.

In conclusion, we evaluated the normal appearance of the cerebral cortex on FLAIR MR images. High signal intensity in the limbic lobe and insula is frequently seen in the normal brain regardless of patient age, sex, and laterality. The results of this study may be useful for the recognition of abnormalities of the limbic cortex caused by various pathologic conditions.


   Acknowledgments
 
The authors thank Seiji Ozawa, MD, for his collaboration, Tatsuhiro Mitsumori for statistical analysis, and Yoko Kitajima for preparing data.


   Footnotes
 
Abbreviations: CNR = contrast-to-noise ratio FLAIR = fluid-attenuated inversion recovery

Author contributions: Guarantor of integrity of entire study, T.H.; study concepts and design, T.H.; definition of intellectual content, T.H.; literature research, T.H.; clinical studies, K.Y., T.S., T.H.; data acquisition, T.H.; data analysis, T.H., Y.S.; manuscript preparation, T.H.; manuscript editing and review, Y.K., M.T.


   References
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

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Evaluation of the Human Limbic Lobe Drs Hirai and Korogi respond:
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