Department of Neurology, Charité, Humboldt-University, Berlin, Germany
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Abstract |
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Introduction |
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In addition to this medial-to-lateral somatotopic organization, studies in non-human primates demonstrated a rostral-to-caudal-somatotopic arrangement of body regions within these cytoarchitectonic areas (Paul et al., 1972; Merzenich et al., 1978
; Kaas et al., 1979
). For the hand region of area 3b, the representation of the fingertip has been shown to be located most rostrally, whereas more proximal parts of the finger are represented at slightly more caudal positions (the terms rostral and caudal always referred to a flattened cortex in these studies; we maintain this classification here too). In human subjects, there are so far only two studies that have explicitly addressed the possible rostral-to-caudal somatotopic organization in area 3b of SI (Hashimoto et al., 1999a
,b
). In these studies using magnetencephalography (MEG), no clear evidence was found of a possible rostral-to-caudal somatotopic arrangement within this area. This finding may be explained by the limits of spatial resolution in MEG. Taking advantage of the superior spatial resolution of functional magnetic resonance imaging (fMRI), we performed electrical stimulation of five adjacent skin areas located along the distal-to-proximal axis on the third finger and the palm of the right hand in order to address the following questions.
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Material and Methods |
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Eight right-handed volunteers (seven male, one female; mean age 30 years, range 2539 years) without any history of neurological or psychiatric disorders were investigated. The study was approved by the local ethics committee and written consent was obtained from each subject prior to investigation.
Electrical Stimulation
Somatosensory stimulation consisted of innocuous electrical stimuli generated by a clinical constant current neurostimulator device (Neuropack 2, Nihon Kohden, Tokyo, Japan). Monophasic square-wave current pulses (frequency 7 Hz, single pulse duration 0.2 ms) were delivered to five electrodes located in-line on the third finger and the palm of the subjects right hand. Electrodes consisted of a central anode (tip diameter 4 mm) and a concentric cathode (width 2 mm, diameter 12 mm) in order to obtain focal stimulation of a circumscribed skin area. The electrodes were attached to the glabrous skin at the following positions: distal (P1), middle (P2) and proximal phalanx (P3) of the third finger and over the caput (P4) and base (P5) of the third metacarpal bone (Fig. 1). The amplitude for each stimulation site was individually adjusted to 1 mA below threshold intensity for pain sensation. The mean stimulation intensities were 12.9 mA (P1), 11.1 mA (P2), 10.6 mA (P3), 10.7 mA (P4) and 14.0 mA (P5).
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MR imaging was performed on a 1.5 T clinical scanner (Magnetom Vision, Siemens, Erlangen, Germany) using a surface coil (CP Flex) for the functional measurements and a head coil for acquisition of the anatomical data sets. The centre of the surface coil was placed over the left parietal cortex approximately at the C3' position according to the extended 10/20 EEG system. The subjects head was immobilized by means of a vacuum pad and fixation tape in order to minimize movement-related artefacts. BOLD (blood oxygenation level dependent) sensitive (Bandettini et al., 1992; Frahm et al., 1992
; Kwong et al., 1992
; Ogawa et al., 1992
) echoplanar images (TR = 3 s, TE = 66 ms, flip angle = 90°) were acquired consisting of eight slices (FOV = 256 mm, matrix = 128 x 128, voxel size = 2 x 2 x 3 mm, gap = 0.75 mm, interleaved order of slice acquisition) that were orientated in parallel to the bicommisural plane. A manual shim in the region of interest (postcentral gyrus) was performed to improve the homogeneity of the static magnetic field. For every subject, two successive runs with 420 images each were performed. Within a single run, each site (P1P5) was stimulated alternately in a blocked order (30 s rest, 30 s stimulation) four times ending with a final rest period (30 s). The initial 10 images were discarded due to T1 saturation effects. Stimulations were applied in a sequential order (P1, P2, P3, P4 and P5) in both runs and since there was no additional task involved, intrinsic attentional effects were rather negligible. For anatomical co-registration a FLASH (fast low angle shot) sequence (TR = 20 ms, TE = 5 ms, flip angle = 30°, 180 slices, voxel size = 1 x 1 x 1 mm) covering the whole brain was applied.
Data Analysis
Functional images were motion-corrected (sinc interpolation) with SPM99 (Wellcome Department of Cognitive Neurology, London, UK). Subsequent data analysis was performed using BrainVoyager® 4.2 (BrainVision, Maastricht, The Netherlands). Functional images were aligned to the anatomical data set and both were transformed into Talairach space. First, the data sets were rotated in stereotactic space after the anterior commissure (AC) and the posterior commissure (PC) as well as the midsagittal plane had been determined manually. Then the borders of the cerebrum were specified and together with the AC and PC coordinates the 3D volumes were finally scaled to Talairach space using a piecewise affine and continuous transformation for each of the 12 resulting subvolumes (Talairach and Tournoux, 1988). Functional image data was interpolated to 1 mm isovoxel size and, after linear trend removal, spatially and temporally smoothed with a Gaussian filter (FWHM = 4 mm and FWHM = 2 s, respectively). For computation of statistical maps, multiple regression analysis was employed using the general linear model. A boxcar function (shift of onset = 6 s) was used as a regressor for each of the five stimulation conditions (P1P5). T-maps of each condition were computed for the individual subjects and the group analysis (n = 8). The thresholds for the statistical maps were set to P < 10-5 uncorrected for multiple comparisons due to a strong a priori hypothesis for the expected activations.
The hand area of SI was determined as the region just posterior to the hand area of the primary motor cortex, which can be identified on axial slices through the brain due to its omega- or epsilon-like shape (Yousry et al., 1997). In order to account for the activation of the different cytoarchitectonic subdivisions of SI, the postcentral gyrus was investigated for discrete activation foci. As cytoarchitectonically defined areas cannot be identified precisely on anatomical landmarks alone (Geyer et al., 1999
), for the assignment of the activation foci to these subdivisions an operational definition was used according to a set of recent fMRI studies (Gelnar et al., 1998
; Francis et al., 2000
; Moore et al., 2000
): (i) the fundus of the central sulcus corresponds to area 3a; (ii) the posterior bank of the central sulcus to area 3b; (iii) the crown of the postcentral gyrus to area 1; and (iv) the anterior bank of the postcentral sulcus to area 2. The statistical maps were visualized superimposed onto the individual reconstructed brain surfaces, this being achieved by segmenting and tessellating the grey/white matter boundary and inflating the resulting surface mesh (Linden et al., 1999
). The statistical maps of the group analysis were also visualized onto an individual brain surface; in order to exclude that the results were based on the specific individual neuroanatomy of that brain, the T-maps were visualized onto different brains.
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Results |
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Within area 3b, activations due to stimulation of adjacent sites on the hand were seen at slightly different locations in the rostral-to-caudal direction. The general finding was that the fingertip (P1) was represented most rostrally, i.e. most deeply within the posterior bank of the central sulcus, whereas the representations of the more proximal parts of the finger (P2, P3) and of the distal palm (P4) were located at more caudal positions. Results of the group analysis are given in Figure 1. From a dorsal view, successive activations associated with stimulations of P1, P2, P3 and P4 can be seen within the posterior bank of the central sulcus, which corresponds to area 3b. The most rostral activation occurred due to stimulation of P1. The representation site of P2 was seen caudally adjacent to that of P1 and is followed by that of P3. Activation due to stimulation of P4 was located most caudally. From a lateral view, activation sites on the crown of the postcentral gyrus can also be seen in Figure 1
. At this anatomical location, which most probably corresponds to area 1, a pattern of discrete representations was again seen. Caudal to the single P4 activation (which is also visible in Fig. 1
, upper part), an activation due to stimulation of P3 is seen. This activation is followed caudally by a second P2 activation. The most caudal activation occurs due to stimulation of P1. In comparison to the closely grouped activations along the rostral- to-caudal direction in response to stimulation of P1, P2, P3 and P4, stimulation of P5 led to an activation at a more medial position within the posterior bank of the central sulcus (area 3b). The Talairach coordinates of the activations of the group analysis are listed in Table 1
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Discussion |
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In contrast to the extensive investigations concerning the medial-to-lateral somatotopic organization of human SI, less attention has been given to its potential rostral-to-caudal somatotopy. In non-human primates, microelectrode recordings demonstrated a rostral-to-caudal somatotopic arrangement of body areas within the different cytoarchitectonic subdivisions of SI (Paul et al., 1972; Merzenich et al., 1978
; Kaas et al., 1979
). Within area 3b, a single finger has been found to be represented in a rostral-to-caudal sequence, starting with the fingertip most rostrally followed by the adjacent skin areas of the middle and proximal phalanx. Our data are in agreement with these findings. The fingertip (P1) was represented most rostrally within the depth of the posterior bank of the central sulcus, whereas the representations of P2 and P3 were found to be located at successively more caudal positions. This finding of a somatotopic arrangement within area 3b is in contrast to results of recent MEG studies by Hashimoto and colleagues using a 122-channel whole-head planar gradiometer system (Hashimoto et al., 1999a
) and a 37-channel first-order axial gradiometer system (Hashimoto et al., 1999b
). In these studies, a vibratory stimulus of 200 Hz was used to stimulate several circumscribed areas, from the tip of the index finger most distally to the palm of the hand most proximally. In both studies, dipole localization revealed no statistically significant differences in the locations of the dipoles with regard to the peripheral site of stimulation. However, whereas in one study a trend was reported for the finger tip to be located most deeply within the posterior bank of the central sulcus (Hashimoto et al., 1999a
), in the second study a reversed order of representations was found (Hashimoto et al., 1999b
). The authors mainly explained their findings either by a blurring of the rostral-to-caudal somatotopic organization in humans as compared to non-human primates or by a lack of spatial resolution in their MEG approach. In order to overcome the latter problem, in this study we performed fMRI using a surface coil that allowed us to measure functional data with an improved in-plane resolution of 2 x 2 mm at an increased signal-to-noise ratio. We assume that the higher spatial resolution of our fMRI approach is the main factor that enabled us to demonstrate the rostral-to-caudal somatotopic arrangement within human area 3b, although there were also differences concerning the stimulation paradigm (i.e. electrical versus vibratory stimulation).
Within area 1 of non-human primates, discrete representations of distal and proximal parts of a single finger have also been described (Paul et al., 1972; Merzenich et al., 1978
; Kaas et al., 1979
). The representations of the distal and proximal parts of the finger in area 1 were found to be arranged in a reversed order in comparison to area 3b, i.e. proximal parts of the finger were found to be represented rostrally, whereas the fingertip was located caudally (Merzenich et al., 1978
; Kaas et al., 1979
). In our study, evidence for discrete representations of proximal and distal parts of a single finger within area 1 can be inferred from the group analysis. On the crown of the postcentral gyrus, caudally to the P4 activation, a discrete representation pattern in the order P3, P2 and P1 can be seen in a rostral-to-caudal direction. The solitary P4 activation on the anterior crown of the postcentral gyrus might be considered to be located at the border between area 3b and area 1 and, therefore, to reflect the activation of both areas. Compared to area 3b, the representation pattern within area 1 appears to be mirror-reversed and the P4 activation may be regarded as the inflection point. Thus, our data suggest the unexpected curiosity that the arrangement in humans is similar to that in owl monkeys, for which the inflection point between areas 3b and 1 has also been reported to be at the distal palm (Merzenich et al., 1978
). In contrast, it seems to differ from the situation described in macaques, where the inflection point was at the proximal phalanx or base of the fingers (Nelson et al., 1980
).
For area 2 of non-human primates, there is evidence for a representation pattern similar to that of area 3b, i.e. the fingertip was found to be located rostrally and the proximal parts of the finger were represented caudally (Pons et al., 1985). Extensive overlap of the activations within area 2 in our data prevents any conclusions regarding a somatotopic arrangement within human area 2. A less distinct somatotopy in area 2 is in agreement with previous reports. Whereas overlap between activation sites has been reported for each of the subdivisions of SI, the extent of overlap is different with regard to a particular cytoarchitectonic area. In general, the extent of overlap steadily increases from area 3b to area 2. This finding may be explained by differences in the receptive field characteristics. Microelectrode mapping studies have demonstrated that in the postcentral finger region of alert monkeys, neurons in area 1 and area 2 tended to have larger and more complex receptive fields than in area 3b (Hyvarinen and Poranen, 1978
; Sur et al., 1980a
). Similarly, Iwamura and colleagues reported a continuous increase in the number of neurons with receptive fields covering multiple fingers or finger and palm from area 3b to area 2 and, as a consequence, the representations of fingers and skin areas on the palm were found to be rather overlapping within area 1 and 2 (Iwamura et al., 1980
, 1983a
,Iwamura et al., b
). In agreement with these invasively recorded data, in a previous fMRI study in human subjects it was shown that the overlap between finger representation sites increased from area 3b to area 1 and 2 (Krause et al., 2001
).
The most proximal point of stimulation over the base of the metacarpal bone (P5) was found to be represented medially to the rostral-to-caudal axis of the finger (P1, P2, P3) and distal palm (P4) representations. Microelectrode mapping studies in non-human primates have demonstrated a representation for the radial part of the glabrous hand at a location laterally to the representation of the thumb, whereas the representation of the ulnar part was found medially to the representation of the fifth finger (Merzenich et al., 1978; Kaas et al., 1979
; Nelson et al., 1980
; Pons et al., 1985
). Thus, one explanation for our finding may be that the stimulation site of P5 in our study excited neurons with receptive fields belonging to the ulnar part of the hand.
The data of the group analysis show the feasibility of mapping the rostral-to-caudal somatotopic arrangement within areas 3b and 1 by means of fMRI. This study, furthermore, represents a non-invasive functional approach to determine the border between these anatomically defined areas. As some inter-individual variability has been reported concerning the exact locations between the cytoarchitectonically defined sub-divisions of SI (Geyer et al., 1999), further improvements in imaging technique (for example, by employing higher field strengths) might offer the possibility of determining functionally the borders of the subdivisions, even in individual subjects. In analogy to the visual system, a delineation in this manner may thus serve as basis for properly characterizing the functional impact of each somatosensory subdivision non-invasively in humans.
In summary, this study gives evidence for the existence of a rostral-to-caudal somatotopic organization of human area 3b. A rostral-to-caudal somatotopic arrangement was also observed within area 1, whereas in area 2 an overlapping representation pattern predominated. Representations within areas 3b and 1 were mirror images of each other.
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Notes |
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Address correspondence to Felix Blankenburg, Department of Neurology, Charité, Humboldt-University, Schumannstrasse 20/21, 10117 Berlin, Germany. Email: felix.blankenburg{at}charite.de.
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References |
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