New Tools for Studying Brain Functional Organization in Health and Disease

Two basic classes of "functional brain mapping" techniques have evolved over the last several decades: (1) those techniques that directly map electrical activity of the brain and (2) those that map local physiological or metabolic consequences of this altered brain electrical activity. Among the former are the noninvasive neural electromagnetic techniques of electroencephalography and magnetoencephalography. TMS can be used to assess physiological characteristics of the cortex, such as excitability, and to map its organization by assessing behavioral responses to cortical stimulations at different locations (Boniface and Ziemann, 2003). These methods allow exquisite temporal resolution of neural processing (typically on a 10- to 100-ms time scale), but suffer from relatively poor spatial resolution (between one and several centimeters).

fMRI methods are in the second category (see Jezzard et al., 2001, for a complete review) along with positron emission tomography (PET). They can be used to detect changes in regional blood perfusion, blood volume, or blood oxygenation that accompany neuronal activity. PET demands injection of radioactive tracers and highly specialized equipment, limiting the number of scans that can be made with any single subject and the availability of the technique. Blood oxygenation level dependent (BOLD) fMRI has become the overwhelmingly most important of these methods because it has a similar spatial (on the order of a few mm) to PET and a better temporal resolution (seconds, limited by the hemodynamic response itself). Moreover, the technique can be implemented on any modern high-field MRI system, making it widely available at a reasonable cost.

A. Principles of BOLD fMRI

BOLD fMRI relies on detecting consequences of the locally increased blood flow (and blood volume) associated with increased neuronal activity (Fig. 1) (Kim et al. 1993; Ogawa et al. 1990, 1992, 1993). Because the increase in local blood flow is in excess of the increased metabolic demands, there is reduced oxygen extraction and a higher ratio of oxy- to deoxyhemoglobin ("redder blood") in the region of neuronal activation. Greater blood oxygenation leads to greater signal on an appropriately (T2*) sensitized MRI scan. The BOLD fMRI arises from the different magnetic properties of oxygenated (oxyHb) and deoxygenated hemoglobin (deoxyHb): deoxyHb is paramagnetic (and distorts an applied magnetic field for imaging), whereas oxyHb is diamagnetic (and does not perturb the applied magnetic field significantly).

Arterioles carrying oxygenated arterial blood thus cause little distortion to the magnetic field, whereas capillaries and veins containing blood that is partially deoxygenated distort the magnetic field locally. The (microscopic) magnetic field inhomogeneities associated with distortions from deoxyHb leads to destructive interference of signal within the tissue voxel, which shortens the so-called T2* "relaxation time." A shorter T2* leads to lower signal from a voxel (and thus a darker image pixel). Alternatively, the increased oxy-/deoxy-hemoglobin ratio associated with activation leads to a longer T2*, more signal from the voxel, and a relatively brighter pixel on the gradient echo image.

In the fMRI experiment, a large (typically hundreds) series of images are acquired rapidly (using a fast imaging technique, such as echo planar imaging) while the subject performs a task in which brain activity alternates between two or more well-defined states (e.g., rest vs. movement of the hand) (Matthews and Jezzard, 2003). By correlating the signal time course from each voxel with the known time course of the task, it is possible to identify those voxels in the brain that show task-associated signal changes corresponding to "activation." Although PET provides an absolute measure of tissue metabolism, BOLD fMRI can at present be used only for determining relative signal intensity changes between different cognitive states studied within a single imaging session. Also, the magnitude of the signal intensity changes being measured with fMRI is only on the order of 0.5% to 5.0%. As this is much smaller than the intrinsic local tissue contrast (e.g., between gray matter and CSF), one of the most significant practical confounds in fMRI is an extreme sensitivity to motion, which can mix signals from

Figure I Hemodynamic parameters that change during neuronal activity. In the basal state deoxyhemoglobin in the capillaries and venules causes microscopic field gradients to be established around the blood vessels. This in turn leads to a decreased signal in a gradient-echo MRI sequence. In the activated state, there is a significant increase in flow, but only a modest increase in oxygen consumption. This results in a lower concentration of deoxyhemoglobin in the capillaries and venules, and hence to a reduction in the microscopic field gradients and to an increase in the signal intensity. (Figure modified from material provided by Prof. P. Jezzard.)

Figure I Hemodynamic parameters that change during neuronal activity. In the basal state deoxyhemoglobin in the capillaries and venules causes microscopic field gradients to be established around the blood vessels. This in turn leads to a decreased signal in a gradient-echo MRI sequence. In the activated state, there is a significant increase in flow, but only a modest increase in oxygen consumption. This results in a lower concentration of deoxyhemoglobin in the capillaries and venules, and hence to a reduction in the microscopic field gradients and to an increase in the signal intensity. (Figure modified from material provided by Prof. P. Jezzard.)

neighboring voxels over an extended series of images. If movement occurs synchronously with the task, movement-associated signal changes will be found along with those associated specifically with any brain functional changes.

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