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Layer-Specific Variation of Iron Content in Cerebral Cortex As a Source Of Layer-specific variation of iron content in cerebral cortex as a source of MRI contrast Masaki Fukunagaa,1, Tie-Qiang Lia, Peter van Gelderena, Jacco A. de Zwarta, Karin Shmuelia, Bing Yaoa, Jongho Leea, Dragan Maricb, Maria A. Aronovac, Guofeng Zhangc, Richard D. Leapmanc, John F. Schenckd, Hellmut Merklea, and Jeff H. Duyna aAdvanced MRI, Laboratory of Functional and Molecular Imaging, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD 20892; bLaboratory of Neurophysiology, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD 20892; cLaboratory of Bioengineering and Physical Science, National Institute of Biomedical Imaging and Bioengineering, National Institutes of Health, Bethesda, MD 20892; and dGeneral Electric Global Research Center, Niskayuna, NY 12309 Edited* by Leslie G. Ungerleider, National Institute of Mental Health, Bethesda, MD, and approved January 4, 2010 (received for review September 28, 2009) Recent advances in high-field MRI have dramatically improved the and is, together with the resonance frequency, particularly sen- visualization of human brain anatomy in vivo. Most notably, in sitive to spatial magnetic susceptibility variations. Most notably, cortical gray matter, strong contrast variations have been observed contrast based on resonance frequency shifts of tissue, derived that appear to reflect the local laminar architecture. This contrast from the phase of gradient-echo signals, has allowed the robust has been attributed to subtle variations in the magnetic properties visualization of laminar structure in a number of neocortical of brain tissue, possibly reflecting varying iron and myelin content. regions, including primary visual and motor cortices (17) (Fig. 1). To establish the origin of this contrast, MRI data from postmortem Despite this progress, the origin of cortical laminar contrast brain samples were compared with electron microscopy and observed with high-field MRI remains unclear. What causes the histological staining for iron and myelin. The results show that iron magnetic properties to vary over cortical layers? Both iron and is distributed over laminae in a pattern that is suggestive of each myelin have been suggested to alter the magnetic susceptibility region’s myeloarchitecture and forms the dominant source of the (17, 19, 20), but experimental confirmation is lacking. In occipital observed MRI contrast. cortex, the laminar pattern observed with MRI is consistent with the known myelin distribution (17), which would support a myelin | ferritin | laminar variation | brain structure | magnetic susceptibility myelin-dominated contrast mechanism. However, the suscepti- bility differences seen in this region are opposite to what is uch of the human cerebral cortex is organized in a network expected for myelin-rich regions based on the contrast differ- Mof functionally specialized regions. This understanding ences between white matter and cortex and therefore argue forms the basis of studies that attempt to expose the brain’s inner against the notion of a myelin-dominated contrast mechanism workings using modern functional imaging techniques such as (17). Conversely, if iron was the main contributor to the observed PET and MRI (1, 2). Some of this functional specialization is contrast, this would suggest the intriguing possibility of a laminar reflected in the local cortical architecture, and may be observed variation of iron, which, like the myelin distribution, may be in postmortem brain samples from the laminar and columnar indicative of cortical functional specialization. variation in a number of tissue properties including cell shape To investigate the possibility of a laminar variation of iron, we (3), myelin content (4), metabolic state (5), neurochemical pro- used a variety of imaging methods, including MRI, histochemical fl file (6), and receptor density (7). and immuno uorescence staining, and electron microscopy. We One of the most striking examples of this structure–function demonstrate that, in the human occipital cortex, (i) there is relationship is in the primary visual cortex (V1, or Brodmann indeed a laminar variation of iron that resembles the frequency fi ii area 17), which is involved in the early stages of visual infor- contrast seen in recent high- eld MRI studies; ( ) this iron is a iii mation processing. Visual area V1 can be readily identified with dominant contributor to R2* and frequency contrast; and ( ) postmortem tissue analysis based on the prominence of myeli- much of this iron appears to be stored within ferritin. nated fibers in layer IVb, known as the line of Gennari. Many Results other brain areas show characteristic myelination patterns (8, 9), and systematic analyses of this type of structural information may Cortical Iron Distribution Is Consistent with MRI Contrast. Although provide important clues about the brain’s functional organ- it has been recognized that iron is responsible for much of the ization. Whole-brain postmortem studies of cellular distributions MRI susceptibility-based contrast in iron-rich brain regions such as the subcortical nuclei (19–22), very little is known about the and myelin content in human brain sections at high resolution ’ have previously been described (8, 10). element s distribution in the cortex or its possible role in the A number of attempts have been made to reveal laminar laminar variation of MRI contrast. To explore the potential cortical structure in vivo with structural MRI, by exploiting contribution of iron in MRI, correlative MRI with histochemical contrast based on the altered density and NMR relaxation times staining was performed on postmortem human brain tissue. Both of water protons in myelin-rich environments (11–15). Although iron and myelin staining were performed on a coronal slab, these studies have had some success, their impact has not been sectioned from the occipital lobe containing a substantial portion widespread as a result of the rather limited contrast and reso- lution available with conventional MRI. Nevertheless, much Author contributions: M.F., T.-Q.L., and J.H.D. designed research; M.F., T.-Q.L., P.v.G., J.A.d. progress has been made over the last few years. Recent devel- Z., K.S., B.Y., J.L., D.M., M.A.A., G.Z., R.D.L., J.S., H.M., and J.H.D. performed research; P.v.G. opments in high-field MRI (≥7 T) have increased spatial reso- contributed new reagents/analytic tools; M.F., T.-Q.L., and J.H.D. analyzed data; and M.F. lution to less than 300 μm (16–18), and improved the ability to and J.H.D. wrote the paper. detect subtle variations in the magnetic susceptibility of tissue. The authors declare no conflict of interest. These variations are reflected in a number of intrinsic MRI *This Direct Submission article had a prearranged editor. parameters, including the longitudinal relaxation rate R1, the 1To whom correspondence should be addressed. E-mail: [email protected]. transverse relaxation rates R2 and R2*, and the NMR resonance This article contains supporting information online at www.pnas.org/cgi/content/full/ frequency. R2* indicates the reversible transverse relaxation rate 0911177107/DCSupplemental. 3834–3839 | PNAS | February 23, 2010 | vol. 107 | no. 8 www.pnas.org/cgi/doi/10.1073/pnas.0911177107 Downloaded by guest on September 27, 2021 AB myelin sheets surrounding nerve fibers (26, 27). In fact, higher magnification views in histochemical stains (Fig. S2) suggest that R2* weighted much of the iron is associated with axonal fibers. Comparison of iron and myelin stains obtained in this study suggests that this colocalization occurs not only in white matter fibers, but also in intracortical fibers. This is consistent with earlier findings (25) and furthermore suggests that myelin-associated iron is the dominant source of intracortical magnetic susceptibility–based contrast. To confirm that the observed iron is indicative of ferritin, we frequency -8 Hz 8 Hz performed double immunofluorescence staining with antibodies to myelin basic protein (MBP) and ferritin storage protein. The results (Fig. 3) clearly show a widespread colocalization of ferritin and myelinated fibers in both gray and white matter similar to what was observed for iron distribution patterns using histochemical stain. Ferritin Iron Content Is Sufficient to Explain MRI Contrast. Although the data presented here are consistent with the notion that ferritin Fig. 1. Example of in vivo MRI contrast in the occipital lobe. (A) Localizer is the primary source of the observed intracortical MRI contrast, it image shows region of interest for (B). (B)R2* weighted magnitude and frequency images. The frequency image reflecting resonance frequency remains unclear whether the magnetic susceptibility of ferritin is shifts. Intracortical contrast is particularly strong in the frequency image, sufficient to explain the MRI data. To clarify this, one would need revealing the centrally located Line of Gennari (arrows). to quantify both the concentration as well as the average iron loading of ferritin storage proteins. In previous work, the average gray matter content of ferritin-bound iron has been reported to be of V1 as well as parts of the secondary visual cortex (V2), and a in the range of 30 to 50 μg/g tissue (wet weight) (28), but infor- section of the superior parietal cortex, respectively. mation about the laminar distribution is lacking. As can be seen from the results (Fig. 2 and Fig. S1), MRI con- To investigate laminar differences, we performed transmission trast and iron staining show strong similarities. Areas of increased EM (TEM) on brain samples obtained from regions within the line R2* relaxation in the white matter show increased iron staining. In of Gennari and more superficial layers (layers II–III; Fig. 4). Data NEUROSCIENCE the gray matter, a laminar distribution of iron is observed with a from 100 fields (700 × 700 × 100 nm) showed average iron particle pattern that resembles the MRI contrast. Moreover, the laminar concentrations of 351 ± 27 and 115 ± 51 (mean ± SD) for these two iron staining pattern exhibits strong similarities with that of myelin.
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