Magnetic resonance imaging of neuronal function in the spinal cord: spinal FMRI

Abstract

A review of the current literature on magnetic resonance imaging of neuronal function in the spinal cord (spinal fMRI) is presented. The unique challenges of spinal fMRI are identified as being the small cross-sectional dimensions of the spinal cord, magnetic field inhomogeneity caused by the bone and cartilage in the spine, and motion of cerebrospinal fluid, blood, adjacent tissues and organs and of the spinal cord itself. Techniques have been developed to overcome or compensate for these challenges and the result is a fMRI method which is distinct from that used for mapping function in the brain. Evidence that the current spinal fMRI method provides accurate and sensitive maps of neuronal function is also discussed. Studies presented in the literature have demonstrated areas of neuronal activity corresponding with spinal cord neuroanatomy as a result of thermal and electrical stimuli and motor tasks with the hands, arms and legs. Signal intensity changes detected in active areas have also been demonstrated to depend on the intensity of the stimuli with both thermal stimulation and a motor task, providing evidence of the correspondence between spinal fMRI results and neuronal activity in the spinal cord.

Figure 1.

Signal intensity time courses observed with a one-hand motor task (ball squeezing) with gradient-echo (GE) and spin-echo (SE) image acquisition at 1.5 tesla. Black lines and symbols indicate gradient-echo data, whereas gray lines and symbols indicate spin-echo data with the dominant and non-dominant hands. The exercise periods of the stimulation paradigm are indicated with the solid black bars at the bottom of the plot. Error bars indicate the standard error of the mean (SEM).

Figure 2.

Fractional signal changes (ΔS/S) observed with spin-echo fMRI data in the cervical spinal cord as a function of echo time at 1.5 tesla. Data are average values from 15 healthy volunteers. Average values for the 1^st and 2^nd measures obtained with echo time = 11 msec are plotted separately. The solid line demonstrates the result of fitting with a non-linear model, whereas the dashed line demonstrates a linear fit to data with echo time >33 msec only. Error bars indicate the standard error of the mean.

Figure 3.

Activity in the lumbar spinal cord in response to a 10°C thermal stimulus applied to the L4 dermatome on the right leg (medial to anteromedial skin roughly 10 cm below the knee). The images are overlaid with the combined activity from 13 subjects demonstrating the consistent areas of activity. Red indicates the greatest consistency (greatest overlap) across subjects with the degree indicated by colors decreasing in spectral order. The schematic inlay (bottom right) shows the expected areas of activity in the spinal cord with a sensory or noxious stimulus. The approximate spinal cord segmental levels that are represented are indicated at the top of each frame. Images are in radiological orientation with the right side of the body to the left and the dorsal aspect of the spine toward the bottom of the images.

Figure 4.

Combined data from the same subjects and same region of the spinal cord shown in figure 3 ▶, demonstrating regions of activity arising only in the latter 24.75 sec of the 33 sec duration cold stimulation at 10°C. The color scale used for the consistent areas of activity and the schematic inlay are the same as that used in figure 3 ▶. Again, images are oriented with the right side of the body to the left, and the dorsal aspect of the spine toward the bottom of the images.

Figure 5.

Example of one set of normalized results obtained from a single experiment with data obtained in thin contiguous sagittal slices. The figure shows a number of axial slices (right side) and one selected sagittal and coronal slice (as indicated on the left). The positions of the axial slices are indicated in the sagittal and coronal views with green lines, and the positions of the sagittal and coronal slices are indicated in each axial slice. Axial slices are in radiological orientation with the right side of the bottom toward the left side of the frame and dorsal is toward the bottom. Sagittal and coronal slices are oriented with rostral toward the left. Dorsal is toward the bottom in the sagittal slice and the left side of the body is toward the bottom of the coronal slices. The axial slices are in order from rostral to caudal, from left to right, and demonstrate the alternated pattern of dorsal (sensory) and ventral (motor) activity within a single spinal cord segment.

Figure 6.

Spinal fMRI signal intensity response in the lumbar spinal cord to stimulation of the L4 dermatome over a range of temperatures. Black circles indicate results from healthy volunteers, × symbols indicate results from subjects with complete spinal cord injuries, and triangles indicate results from subjects with incomplete injuries to the spinal cord. Signal intensity changes are relative to the baseline temperature at 32°C.

Figure 7.

Areas of neuronal activity detected in the spinal cord (A–E) and brain (F) obtained simultaneously in the three functional MRI experiments in the same rat (rows 1 to 3, respectively). The spinal images are superimposed on anatomical images at five different levels of the cervical spinal cord: images corresponding to T2/T1, T1/C8, C7, C6 and C5 cervical levels from left to right (A–E) respectively with the ventral surface at the top, dorsal surface at the bottom. Left-right direction is according to radiology convention. The color of the activation corresponds to the level of the correlation to the paradigm: red corresponds to the highest, yellow to medium, and green the lowest correlation coefficients, respectively (all P<0.001). (Courtesy of K. Majcher et al.51)