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Fingersomatotopy in area 3b: an fMRI-study

Fingersomatotopy in area 3b: an fMRI-study Background: The primary sensory cortex (S1) in the postcentral gyrus is comprised of four areas that each contain a body map, where the representation of the hand is located with the thumb most laterally, anteriorly and inferiorly and the little finger most medially, posteriorly and superiorly. Previous studies on somatotopy using functional MRI have either used low field strength, have included a small number of subjects or failed to attribute activations to any area within S1. In the present study we included twenty subjects, who were investigated at 3 Tesla (T). We focused specifically on Brodmann area 3b, which neurons have discrete receptive fields with a potentially more clearcut somatotopic organisation. The spatial distribution for all fingers' peak activation was determined and group as well as individual analysis was performed. Results: Activation maps from 18 subjects were of adequate quality; in 17 subjects activations were present for all fingers and these data were further analysed. In the group analysis the thumb was located most laterally, anteriorly and inferiorly with the other fingers sequentially positioned more medially, posteriorly and superiorly. At the individual level this somatotopic relationship was present for the thumb and little finger, with a higher variability for the fingers in between. The Euclidian distance between the first and fifth finger was 17.2 mm, between the first and second finger 10.6 mm and between the remaining fingers on average 6.3 mm. Conclusion: Results from the group analysis, that is both the location of the fingers and the Euclidian distances, are well comparable to results from previous studies using a wide range of modalities. On the subject level the spatial localisation of the fingers showed a less stringent somatotopic order so that the location of a finger in a single subject cannot be predicted from the group result. lished in 1937 by using intra-operative electrical Background The first somatotopic maps of the homuncular organisa- stimulation of the brain surface [1]. Subsequent, non- tion of the primary somatosensory cortex (S1) were estab- invasive investigations in humans on the hand Page 1 of 6 (page number not for citation purposes) BMC Neuroscience 2004, 5:28 http://www.biomedcentral.com/1471-2202/5/28 representation in S1 have described a somatotopic organ- analyzed. In the one volunteer excluded from the analysis, isation along the central sulcus with the thumb located activation was present for four fingers. The spatial distri- laterally, anteriorly and inferiorly to the little finger [2-6]. bution of the activations in the contralateral S1 for tactile Studies in non-human primates have revealed the cytoar- stimulation versus rest in one subject is shown in Figure 2. chitectonic subdivisions of S1, namely areas 3a, 3b, 1 and 2, that outline the cortex in the postcentral gyrus [7]. Area A somatotopic organisation with the representation of the 3a occupies the fundus of the central sulcus, area 3b the thumb located laterally to the little finger was present in anterior wall of the postcentral gyrus, area1 its crown and 16 out of 17 subjects, with the thumb located anteriorly to area 2 its posterior wall. Each area contains a fairly com- the little finger in 14 out of 17 subjects and with the plete map of the body surface and is the cortical represen- thumb located inferiorly to that of the little finger in 16 tation of different somatosensory receptors. In area 3b the out of 17 subjects. neurons are predominantly responsive to stimulation of cutaneous receptors. As opposed to neurons in area 1, that Group averages of the distances from D2 to D1 (D2-D1), also receive input from cutaneous receptors, those in area D3 to D1(D3-D1), D4 to D1 (D4-D1) and D5 to D1 (D5- 3b possess discrete receptive fields with a homuncular D1) are presented in the Table and shown as graphs in Fig- organisation that may be more distinct [8]. ure 3. Combined these indicate a strict somatotopy with the distance to D1 increasing for every finger in each of the Previous studies on somatotopy in the hand area using three directions. Distances to D1 were compared for functional Magnetic Resonance Imaging (fMRI) have neighbouring fingers. In the medial-lateral direction, the yielded varying results. Gelnar et al. failed to show a distance D4-D1 was different from D3-D1. In the somatotopy in S1 when applying vibratory stimuli to anterior-posterior direction a significant difference was three of the fingers of the right hand [5]. Maldjian et al. observed between D4-D1 and D3-D1. Finally, in the supe- demonstrated somatotopy in 3 out of 5 subjects [3]. Sim- rior-inferior direction the distances D2-D1 and D3-D1 as ilarly, Kurth et al., using electrical stimulation of two fin- well as D3-D1 and D4-D1 differed; the location of D2, as gers, found somatotopically arranged activation patterns determined by its distance to D1, was different from the in 5 out of 20 subjects [9]. In a follow-up study where acti- location of D1 [0, 0, 0]; no difference was found between vation of all fingers in area 3b was found in 7 out of 10 the distances D5-D1 and D4-D1. Considering that the subjects, the same authors reported a general somatotopy, three coordinates [x, y and z] together define one point in without further specification [4]. the 3D Cartesian space, the coordinates of D3, D4 and D5, differed from those of D1, p now <0.05/3, corrected Methods differ considerably between these three studies for multiple comparisons (not in Table). with regard to anatomical considerations, number of sub- jects studied, and the field strength used. Maldjian et al. The Euclidian distance from D1 to D2 was 10.6 mm (SEM used the highest field strength, 4 Tesla (T), while both ± 1.5). The distance from D2 to D3 was 5.5 mm (± 0.9), Kurth et al. and Gelnar et al. used 1.5 T [3-5]. However, from D3 to D4 7.4 mm (± 1.1) and from D4 to D5 6.8 Maldjian et al. did not contribute activations to any area mm (± 1.2), resulting in an average for D2-D3, D3-D4 in S1. Also Maldjian et al. included the smallest number and D4-D5 of 6.6 mm. of subjects (5); data from one were discarded due to motion artefacts and group analysis was based on data The spatial extension of the representation of the hand in from the remaining 4. area 3b, defined as the Euclidian distance between D1 and D5 was 17.2 mm (± 2.0 mm). In the present study we readdressed the issue of somatot- opy in the hand area as assessed with fMRI. Our aim was Discussion to optimise results by including a larger number of sub- In the group average from the present study the strict jects, by focussing on area 3 b, where homuncular organ- somatotopic organisation in the primary sensory cortex isation expectedly is most distinct and by performing known from studies using a variety of modalities, was fMRI at 3 Tesla (T). reproduced [2-6]. The fingers' average activations were laid out on the body map, with the thumb located most laterally, anteriorly and inferiorly and the little finger Results Tactile stimulation of the fingers of the dominant hand most medially, posteriorly and superiorly and the remain- yielded activation in contra-and ipsilateral S1, contra- or ing fingers in between, the distance to the thumb increas- bilateral secondary sensory cortex (S2), ipsilateral cerebel- ing for every finger in each of the three directions. In lum, and in some subjects the contralateral thalamus. Sig- individual subjects the arrangement in the hand represen- nificant activation for all five fingers in area 3b was tation with the thumb located laterally, anteriorly and present in seventeen subjects and these data were further inferiorly to the little finger is frequently found, while the Page 2 of 6 (page number not for citation purposes) BMC Neuroscience 2004, 5:28 http://www.biomedcentral.com/1471-2202/5/28 Table Distance to finger 1 Finger x L → My A → Pz I → SEuclidian D1 0 (0) 0 (0) 0 (0) 0 (0) D2 2.9 (1.6) 0.4 (1.8) 4.8 (1.0) 10.6 (1.5) D3 3.6 (1.4) 1.4 (1.5) 6.8 (1.2) 11.2 (1.5) D4 6.9 (1.4) 4.6 (1.7) 9.4 (1.4) 15.4 (1.7) D5 7.4 (1.7) 6.8 (1.2) 10.4 (2) 17.2 (2.0) Distance from each finger (D2, D3, D4, D5) to the thumb (D1) ± standard error of the mean (SEM) (mm). The lateral-to-medial direction is named 'x', the anterior-to-posterior direction 'y' and the inferior-to-superior direction 'z'. Underlined are those distances to D1 that differ significantly from the distance of the previous finger to D1 (Wilcoxon matched pairs test, p < 0.05). remaining fingers may or may not display the orderly lat- In one subject excluded from the analysis, activation was eral-to-medial, anterior-to-posterior and inferior-to-supe- present for four fingers and another was excluded due to rior organisation 'D1-D2-D3-D4-D5' [2,3,10,11]. We general lack of activation. Lack of activation may be due chose to present group averages as it is our belief our to subjects being 'low-activators' in fMRI experiments, due results would have greater significance if a regular soma- to inadequate stimulation or to some other, unknown totopy was present at the group level. Body maps in non- factor. human primates demonstrating the regular sequence mentioned above, were established with cortical single The type of stimulation used is decisive of what area in S1 unit recordings and are supposedly the golden standard. can be expected to be activated. For example, neurons in The present study is based on data from 20 subjects, gen- area 3a are responsive to deep receptor and proprioceptive erating results available for analysis from 18 of these; the stimulation and in one study punctate tactile stimulation spatial representation of all fingers in area 3b of the pri- did not activate area 3a [13]. Also, receptive fields are mary somatosensory cortex was localised in 17 subjects. maximally focused in area 3b, while in area 1 receptive fields become larger and more complex. In area 2, recep- The average extension of the hand representation in area tive fields are even more complex with reduplications. 3b of 17 mm with a somatotopic arrangement of fingers This combined knowledge made area 3b the area of our 1-5 as described above is consistent with results from pre- choice to study somatotopy and explains why we chose vious studies using a range of modalities [2-4,7]. Also the not to report on activations in areas 3a, 1 and 2. mean distance between D2-D3, D3-D4 and D4-D5 of 6.6 mm and 6.3 mm for main and differential effects, respec- We found activation in the anterior wall of the postcentral tively, is in good agreement with human electrophysio- gyrus, defined as area 3b according to our operational def- logical and fMRI data [2,4]. The larger distance between inition during tactile stimulation (Fig 1). More pro- the thumb and index finger as compared to distances nounced activation was noticed frequently in the crown between subsequent fingers suggests a larger representa- or posterior wall of the postcentral gyrus, defined as areas tion for the thumb. This finding is in agreement with 1 and 2 (Fig 2). Similar observations have been made in results from a study using electrocorticography with sub- other studies using both fMRI and PET [5,14]. According dural electrodes in three patients [1,12]. to studies in non-human primates the representation of the distal fingertips in area 1 points posteriorly, a finding With the spatial resolution used in this study, 3 × 3 × 3 confirmed in a recent fMRI-study on humans [15]. Area 2 3 3 mm , resampled to 1.5 × 1.5 × 1.5 mm , activation for all then is the mirror-image of area 1 with the fingertips five fingers was found in 17 of 18 subjects. For compari- pointing anteriorly. The activation in the posterior wall son, Kurth et al. used a resolution of 1.7 × 1.7 × 1.7 mm3 might represent activation in both areas 1 and 2 localised and electrical stimulation with ring electrodes and found at their meeting point, i.e. the fingertips. The larger cluster activation in area 3b for all five fingers in 7 out of 10 sub- size of this activation is explained by the clusters arising jects (70%) [4]. The present study showed activations for from area 1 and 2 being contiguous and therefore addi- all fingers in 94 % of subjects. This difference might be tive. In the present study the activation of area 1 and 2 is due to the higher field strength used in this study as the probably due to hierarchical processing in the rostrocau- higher magnetisation vector and sensitivity to changes in dal direction within S1. A previous observation that elec- susceptibility increase the signal-to-noise ratio. trical stimulation of the cutaneous afferents of the median nerve resulted in evoked potentials in area 3b after 30 Page 3 of 6 (page number not for citation purposes) BMC Neuroscience 2004, 5:28 http://www.biomedcentral.com/1471-2202/5/28 A p Figure 1 o rst-mortem bra eas of S1 as defined in cyto ins [18, 19] architectonic studies on 10 Activation in the contralatera tactile stimulation of the fingers ('main effec Figure 2 ts') in a single subject l somatosen of the right ha sory cortex during nd versus rest Areas of S1 as defined in cytoarchitectonic studies on 10 Activation in the contralateral somatosensory cortex during post-mortem brains [18, 19]: area 3a occupies the fundus of tactile stimulation of the fingers of the right hand versus rest the central sulcus (dark blue), area 3b the anterior wall of the in a single subject. The first column shows transverse ana- postcentral gyrus (red), area1 its crown (light blue) and area tomical image with z-coordinate indicated. Subsequent col- 2 its posterior wall (green). The black arrow indicates the umns show the activation patterns in S1 overlayed on central sulcus. magnified T1-weighted images for each finger. The location of the peak voxel in area 3b is indicated by blue crosshairs. msec while a potential in area 1 was seen after another 5 msec lends support to this assumption [16]. the local ethics committee and written informed consent was obtained. All volunteers had normal images on a Conclusion fluid-attenuated inversion recovery (FLAIR) sequence. In the group analysis, a somatotopic organisation for all the fingers in the hand representation of area 3b could be Stimulation demonstrated using fMRI; the Euclidian distance between Tactile stimulation consisted of brushing the glabrous the thumb and the little finger was well comparable to skin of the two distal phalanges of each finger continu- that determined in previous studies. On the subject level ously forwards and backwards with a commercially avail- the cortical somatosensory representation of the thumb able tooth brush. During the experiment, volunteers were was located laterally, anteriorly, and inferiorly to that of positioned on the MR table with their right arm from the the little finger in 14 out of 17 subjects. The spatial local- elbow down in a padded cast, that also provided support isation of the remaining fingers showed a less stringent for the dorsal part of the hand. They were instructed to rest somatotopic order when compared individually. their arm against the magnet bore so that both arm and hand were relaxed. Pieces of soft cloth were placed Methods between the fingers in order to avoid that stimulation also Subjects involved a neighbouring finger. Twenty healthy, self-reportedlly right-handed volunteers (6 male and 14 female, age 21–43 years, mean 29.4 years) The frequency was 1 Hz; no forced pressure was exerted. were included in the study. The protocol was approved by Consistency was tested on a finger model firmly taped Page 4 of 6 (page number not for citation purposes) BMC Neuroscience 2004, 5:28 http://www.biomedcentral.com/1471-2202/5/28 Postprocessing Image processing and analysis were carried out using the SPM99 soft ware package [17]. All functional images were resliced to a voxel size of 1.5 × 1.5 × 1.5 mm and then rea- ligned to the first image and coregistered to the T1- weighted image volume. All data were spatially filtered using an isotropic 4 mm, full-width, half-maximum Gaus- sian kernel. A high pass filter (cut off frequency 0.008 Hz) was applied to eliminate low frequency signal fluctua- tions. In order to preserve each subject's somatotopic arrangement in area 3b no normalization to a common brain atlas was performed. Distan m Figure 3 onds) ce to the thum and SEM (errorbar b (D1) s)for each fin , as presented in Table ger (mm), mean (dia- Data analysis Distance to the thumb (D1) for each finger (mm), mean (dia- Functional data from two subjects were excluded due to monds) and SEM (errorbars), as presented in Table. The major motion artefacts (subject no. 7) and global lack of coordinates for D1 are defined as origo [0, 0, 0]. Distances activation (subject no.18). Task specific effects were esti- to D1 are shown in the medial-lateral (M-L) direction, in the mated using the general linear model (GLM) that left panel also in the posterior-anterior (P-A) direction and in included a box car function convolved with the canonical the right panel also in the superior-inferior (S-I) direction. hemodynamic response function in SPM99. The effect of The fingers are sequentially positioned more medially, poste- sensory stimulation of each finger versus rest was deter- riorly and superiorly. mined using a one-sample t-test of pertinent linear con- trasts of parameter estimates in each subject with a significance level of p < 0.001 (uncorrected). Then the spatial coordinates of the peak activation voxel in area 3b onto a computerized electronic scale (Biopac Systems, DA were determined. Due to lack of neuroanatomical land- 100B, MP 100A; Macintosh Powerbook G3 with software marks, exact delineation of the cytoarchitectonically AcqKnowledge 3.5): the intra-examiner error was 18% defined areas within S1 cannot be achieved in MR images. based on a mean pressure of 6.64 g, standard deviation Therefore we used an operational definition based on 1.199 g. cytoarchitectonic studies of S1 on 10 post-mortem brains. In >50 % of these brains area 3a was located in the fundus Imaging of the central sulcus, area 3b in the rostral bank of the MRI was performed using a 3 T head scanner (Siemens postcentral gyrus and area 1 on its crown reaching down Allegra) with a quadrature birdcage coil. Morphological into the postcentral sulcus [18,19]. Fig 1 illustrates these T1-weighted images with a resolution of 1 × 1 × 1 mm locations, that continue along the central sulcus. As inter- using a magnetisation prepared gradient echo sequence areal borders vary across brains, the same authors con- (MPRAGE) were acquired. Functional echo-planar image structed probability maps for each area by superimposing volumes of the whole brain (number of slices = 49, thick- histological volumes of the individual brains on a compu- ) sensitised to the ness = 3 mm, voxel size = 3 × 3 × 3 mm terized reference brain. Volumes of interest (VOIs) were Blood Oxygenation Level Dependent (BOLD)-effect defined for each area in which >50 % of the brains had a (echo time = 30 ms) were acquired. Five scanning sessions representation of that area. Despite close relationship of were performed. Each session included 92 functional vol- areas 3a, 3b and 1 in the postcentral gyrus, the three VOIs umes with a temporal resolution of 3 seconds. The first overlapped by <1% of their volumes. These probability two volumes in each session were discarded from further maps were at hand when the spatial coordinates of the analysis to allow for initial T1-equilibrium effects. peak activation voxel in area 3b were determined. Acti- vated peak voxels were labelled as belonging to area 3b Experimental protocol when they were located within the anterior wall of the Fingers 1 to 5 (D1 = thumb, D5 = little finger) of the right postcentral gyrus (Figure 1). hand were stimulated sequentially in separate sessions according to a block design that included four periods of The spatial coordinates of the peak voxel for the thumb stimulation and five of rest for each finger. The epoch (D1) was defined as being at origo [0, 0, 0] in a 3D Carte- length for both stimulation and rest periods was 30 sian coordinate system.When the spatial coordinates for seconds. all fingers were known in all subjects, somatotopy was assessed by determining the average distances for the whole group from each finger to the thumb. Page 5 of 6 (page number not for citation purposes) BMC Neuroscience 2004, 5:28 http://www.biomedcentral.com/1471-2202/5/28 8. Kaas JH: Multiple representations of the body within the pri- Euclidian distances between fingers as well as from each mary somatosensory cortex of primates. Physiol Rev 1983, finger to the thumb (D1) were calculated as: 63(1):206-231. 9. Kurth R, Villringer K, Mackert BM, Schwiemann J, Braun J, Curio G, Villringer A, Wolf KJ: fMRI assessment of somatotopy in human () x −+ x (yy− )+(zz− ) DI DII DI DII DI DII Brodmann area 3b by electrical finger stimulation. NeuroRe- port 1998, 9(2):207-212. 10. Mogilner A, Grossman JA, Ribary U, Joliot M, Volkmann J, Rapaport with x , y and z representing the coordinates of the DI DI DI D, Beasley RW, Llinás RR: Somatosensory cortical plasticity in finger DI and x , y and z representing the coordi- DII DII DII adult humans revealed by magnetoencephalography. Proc nates of DII in the three directions x, y, z in a system where Natl Acad Sci 1993, 90:3593-3597. 11. Baumgartner C, Doppelbauer A, Sutherling WW, Zeitlhofer J, Lind- the coordinates of D1 are at origo [0, 0, 0]. inger G, Lind C, Deecke L: Human somatosensory cortical fin- ger representation as studied by combined neuromagnetic Statistics and neuroelectric measurements. Neurosci Lett 1991, 16(134(1)):103-8. Each finger's distance to the first finger was compared to 12. Sutherling WW, Levesque MF, Baumgartner C: Cortical sensory that of the directly neighbouring fingers using the Wil- representation of the human hand: size of finger regions and nonoverlapping digit somatotopy. Neurology 1992, coxon matched pairs test with a significance level of p < 42:1020-1028. 0.05. The Euclidian distances to the first finger were com- 13. Moore CI, Stern CE, Corkin S, Fischl B, Gray AC, Rosen BR, Dale AM: pared for each finger using the Wilcoxon matched pairs Segregation of somatosensory activation in the human rolandic cortex using fMRI. J Neurophysiol 2000, 84(1):558-69. test with a significance level of p < 0.05. 14. Burton H, MacLeod AM, Videen TO, Raichle ME: Multiple foci in parietal and frontal cortex activated by rubbing embossed grating patterns across fingerpads: a positron emission tom- Authors' contributions ography study in humans. Cereb Cortex 1997, 7:3-17. DvW conceived of the study, performed the image analy- 15. Blankenburg F, Ruben J, Meyer R, Schwiemann J, Villringer A: Evi- sis and drafted the manuscript. PF guided the image anal- dence for a rostral-to-caudal somatotopic organization in human primary somatosensory cortex with mirror-reversal ysis. JO designed the MR-parameters. EML participated in in areas 3b and 1. Cereb Cortex 2003, 13:987-993. the design of the study. BR and GL initiated and con- 16. Allison T, McCarthy G, Wood CC, Darcey TM, Spencer DD, William- ducted the stimulation consistency study. All authors read son PD: Human cortical potentials evoked by stimulation of the median nerve. I. Cytoarchitectonic areas generating and approved the final manuscript. short-latency activity. J Neurophysiol 1989, 62(3):694-710. 17. Statistical Parametric Mapping [http://www.fil.ion.ucl.ac.uk/ spm] Acknowledgments 18. Geyer S, Schleicher A, Zilles K: Areas 3a, 3b and 1 of Human pri- The authors thank dr S Geyer, Research Center Jülich, Germany for prob- mary Somatosensory cortex, 1. Microstructural organisa- ability maps delineating areas 3a, 3b and 1. This study was supported by the tion and interindividual variability. NeuroImage 1999, 10:63-83. Swedish Medical Research Council, the Swedish Brain Foundation, the 19. Geyer S, Schormann T, Mohlberg H, Zilles K: Areas 3a, 3b and 1 of Human primary Somatosensory cortex, 2. Spatial normali- Medical Faculty at Lund University, the Skåne County Council Research and sation to standard anatomical space. NeuroImage 2000, Development Foundation and the Royal Physiographic Society in Lund.. 11:684-696. Part of this work was presented at the annual meeting of the European Society for Magnetic Resonance in Medicine and Biology, Rotterdam 2003. References 1. Penfield W, Boldrey E: Somatic motor and sensory representa- tion in the cerebral cortex of man as studied by electrical stimulation. Brain 1937, 60:389-443. 2. Hari R, Karhu J, Hamalainen M, Knuutila J, Salonen O, Sams M, Vilk- man V: Functional organization of the human first and second somatosensory cortices: a neuromagnetic study. Eur J Neurosc 1993, 5:724-734. 3. Maldjian JA, Gottschalk A, Patel RS, Detre JA, Alsop DC: The sen- sory somatotopic map of the human hand demonstrated at 4 Tesla. NeuroImage 1999, 10:55-62. 4. Kurth R, Villringer K, Curio G, Wolf KJ, Krause T, Repenthin J, Schw- Publish with Bio Med Central and every iemann J, Deuchert M, Villringer A: fMRI shows multiple somato- scientist can read your work free of charge topic digit representations in human primary somatosensory cortex. NeuroReport 2000, 11:1487-1491. "BioMed Central will be the most significant development for 5. Gelnar PA, Krauss BR, Szeverenyi NM, Apkarian AV: Fingertip rep- disseminating the results of biomedical researc h in our lifetime." resentation in the human somatosensory cortex: an fMRI study. NeuroImage 1998, 7:261-283. Sir Paul Nurse, Cancer Research UK 6. Buchner H, Fuchs M, Wischmann HA, Dossel O, Ludwig I, Knepper Your research papers will be: A, Berg P: Source analysis of median nerve and finger stimu- lated somatosensory evoked potentials: multichannel simul- available free of charge to the entire biomedical community taneous recording of electric and magnetic fields combined peer reviewed and published immediately upon acceptance with 3D-MR tomography. Brain Topogr 1994, 6(4):299-310. 7. Kaas JH, Nelson RJ, Sur M, Lin CS, Merzenich MM: Multiple repre- cited in PubMed and archived on PubMed Central sentations of the body within the primary somatosensory yours — you keep the copyright cortex of primates. Science 1979, 204:521-523. BioMedcentral Submit your manuscript here: http://www.biomedcentral.com/info/publishing_adv.asp Page 6 of 6 (page number not for citation purposes) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png BMC Neuroscience Springer Journals

Fingersomatotopy in area 3b: an fMRI-study

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Copyright © 2004 by van Westen et al; licensee BioMed Central Ltd.
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Biomedicine; Neurosciences; Neurobiology; Animal Models
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Abstract

Background: The primary sensory cortex (S1) in the postcentral gyrus is comprised of four areas that each contain a body map, where the representation of the hand is located with the thumb most laterally, anteriorly and inferiorly and the little finger most medially, posteriorly and superiorly. Previous studies on somatotopy using functional MRI have either used low field strength, have included a small number of subjects or failed to attribute activations to any area within S1. In the present study we included twenty subjects, who were investigated at 3 Tesla (T). We focused specifically on Brodmann area 3b, which neurons have discrete receptive fields with a potentially more clearcut somatotopic organisation. The spatial distribution for all fingers' peak activation was determined and group as well as individual analysis was performed. Results: Activation maps from 18 subjects were of adequate quality; in 17 subjects activations were present for all fingers and these data were further analysed. In the group analysis the thumb was located most laterally, anteriorly and inferiorly with the other fingers sequentially positioned more medially, posteriorly and superiorly. At the individual level this somatotopic relationship was present for the thumb and little finger, with a higher variability for the fingers in between. The Euclidian distance between the first and fifth finger was 17.2 mm, between the first and second finger 10.6 mm and between the remaining fingers on average 6.3 mm. Conclusion: Results from the group analysis, that is both the location of the fingers and the Euclidian distances, are well comparable to results from previous studies using a wide range of modalities. On the subject level the spatial localisation of the fingers showed a less stringent somatotopic order so that the location of a finger in a single subject cannot be predicted from the group result. lished in 1937 by using intra-operative electrical Background The first somatotopic maps of the homuncular organisa- stimulation of the brain surface [1]. Subsequent, non- tion of the primary somatosensory cortex (S1) were estab- invasive investigations in humans on the hand Page 1 of 6 (page number not for citation purposes) BMC Neuroscience 2004, 5:28 http://www.biomedcentral.com/1471-2202/5/28 representation in S1 have described a somatotopic organ- analyzed. In the one volunteer excluded from the analysis, isation along the central sulcus with the thumb located activation was present for four fingers. The spatial distri- laterally, anteriorly and inferiorly to the little finger [2-6]. bution of the activations in the contralateral S1 for tactile Studies in non-human primates have revealed the cytoar- stimulation versus rest in one subject is shown in Figure 2. chitectonic subdivisions of S1, namely areas 3a, 3b, 1 and 2, that outline the cortex in the postcentral gyrus [7]. Area A somatotopic organisation with the representation of the 3a occupies the fundus of the central sulcus, area 3b the thumb located laterally to the little finger was present in anterior wall of the postcentral gyrus, area1 its crown and 16 out of 17 subjects, with the thumb located anteriorly to area 2 its posterior wall. Each area contains a fairly com- the little finger in 14 out of 17 subjects and with the plete map of the body surface and is the cortical represen- thumb located inferiorly to that of the little finger in 16 tation of different somatosensory receptors. In area 3b the out of 17 subjects. neurons are predominantly responsive to stimulation of cutaneous receptors. As opposed to neurons in area 1, that Group averages of the distances from D2 to D1 (D2-D1), also receive input from cutaneous receptors, those in area D3 to D1(D3-D1), D4 to D1 (D4-D1) and D5 to D1 (D5- 3b possess discrete receptive fields with a homuncular D1) are presented in the Table and shown as graphs in Fig- organisation that may be more distinct [8]. ure 3. Combined these indicate a strict somatotopy with the distance to D1 increasing for every finger in each of the Previous studies on somatotopy in the hand area using three directions. Distances to D1 were compared for functional Magnetic Resonance Imaging (fMRI) have neighbouring fingers. In the medial-lateral direction, the yielded varying results. Gelnar et al. failed to show a distance D4-D1 was different from D3-D1. In the somatotopy in S1 when applying vibratory stimuli to anterior-posterior direction a significant difference was three of the fingers of the right hand [5]. Maldjian et al. observed between D4-D1 and D3-D1. Finally, in the supe- demonstrated somatotopy in 3 out of 5 subjects [3]. Sim- rior-inferior direction the distances D2-D1 and D3-D1 as ilarly, Kurth et al., using electrical stimulation of two fin- well as D3-D1 and D4-D1 differed; the location of D2, as gers, found somatotopically arranged activation patterns determined by its distance to D1, was different from the in 5 out of 20 subjects [9]. In a follow-up study where acti- location of D1 [0, 0, 0]; no difference was found between vation of all fingers in area 3b was found in 7 out of 10 the distances D5-D1 and D4-D1. Considering that the subjects, the same authors reported a general somatotopy, three coordinates [x, y and z] together define one point in without further specification [4]. the 3D Cartesian space, the coordinates of D3, D4 and D5, differed from those of D1, p now <0.05/3, corrected Methods differ considerably between these three studies for multiple comparisons (not in Table). with regard to anatomical considerations, number of sub- jects studied, and the field strength used. Maldjian et al. The Euclidian distance from D1 to D2 was 10.6 mm (SEM used the highest field strength, 4 Tesla (T), while both ± 1.5). The distance from D2 to D3 was 5.5 mm (± 0.9), Kurth et al. and Gelnar et al. used 1.5 T [3-5]. However, from D3 to D4 7.4 mm (± 1.1) and from D4 to D5 6.8 Maldjian et al. did not contribute activations to any area mm (± 1.2), resulting in an average for D2-D3, D3-D4 in S1. Also Maldjian et al. included the smallest number and D4-D5 of 6.6 mm. of subjects (5); data from one were discarded due to motion artefacts and group analysis was based on data The spatial extension of the representation of the hand in from the remaining 4. area 3b, defined as the Euclidian distance between D1 and D5 was 17.2 mm (± 2.0 mm). In the present study we readdressed the issue of somatot- opy in the hand area as assessed with fMRI. Our aim was Discussion to optimise results by including a larger number of sub- In the group average from the present study the strict jects, by focussing on area 3 b, where homuncular organ- somatotopic organisation in the primary sensory cortex isation expectedly is most distinct and by performing known from studies using a variety of modalities, was fMRI at 3 Tesla (T). reproduced [2-6]. The fingers' average activations were laid out on the body map, with the thumb located most laterally, anteriorly and inferiorly and the little finger Results Tactile stimulation of the fingers of the dominant hand most medially, posteriorly and superiorly and the remain- yielded activation in contra-and ipsilateral S1, contra- or ing fingers in between, the distance to the thumb increas- bilateral secondary sensory cortex (S2), ipsilateral cerebel- ing for every finger in each of the three directions. In lum, and in some subjects the contralateral thalamus. Sig- individual subjects the arrangement in the hand represen- nificant activation for all five fingers in area 3b was tation with the thumb located laterally, anteriorly and present in seventeen subjects and these data were further inferiorly to the little finger is frequently found, while the Page 2 of 6 (page number not for citation purposes) BMC Neuroscience 2004, 5:28 http://www.biomedcentral.com/1471-2202/5/28 Table Distance to finger 1 Finger x L → My A → Pz I → SEuclidian D1 0 (0) 0 (0) 0 (0) 0 (0) D2 2.9 (1.6) 0.4 (1.8) 4.8 (1.0) 10.6 (1.5) D3 3.6 (1.4) 1.4 (1.5) 6.8 (1.2) 11.2 (1.5) D4 6.9 (1.4) 4.6 (1.7) 9.4 (1.4) 15.4 (1.7) D5 7.4 (1.7) 6.8 (1.2) 10.4 (2) 17.2 (2.0) Distance from each finger (D2, D3, D4, D5) to the thumb (D1) ± standard error of the mean (SEM) (mm). The lateral-to-medial direction is named 'x', the anterior-to-posterior direction 'y' and the inferior-to-superior direction 'z'. Underlined are those distances to D1 that differ significantly from the distance of the previous finger to D1 (Wilcoxon matched pairs test, p < 0.05). remaining fingers may or may not display the orderly lat- In one subject excluded from the analysis, activation was eral-to-medial, anterior-to-posterior and inferior-to-supe- present for four fingers and another was excluded due to rior organisation 'D1-D2-D3-D4-D5' [2,3,10,11]. We general lack of activation. Lack of activation may be due chose to present group averages as it is our belief our to subjects being 'low-activators' in fMRI experiments, due results would have greater significance if a regular soma- to inadequate stimulation or to some other, unknown totopy was present at the group level. Body maps in non- factor. human primates demonstrating the regular sequence mentioned above, were established with cortical single The type of stimulation used is decisive of what area in S1 unit recordings and are supposedly the golden standard. can be expected to be activated. For example, neurons in The present study is based on data from 20 subjects, gen- area 3a are responsive to deep receptor and proprioceptive erating results available for analysis from 18 of these; the stimulation and in one study punctate tactile stimulation spatial representation of all fingers in area 3b of the pri- did not activate area 3a [13]. Also, receptive fields are mary somatosensory cortex was localised in 17 subjects. maximally focused in area 3b, while in area 1 receptive fields become larger and more complex. In area 2, recep- The average extension of the hand representation in area tive fields are even more complex with reduplications. 3b of 17 mm with a somatotopic arrangement of fingers This combined knowledge made area 3b the area of our 1-5 as described above is consistent with results from pre- choice to study somatotopy and explains why we chose vious studies using a range of modalities [2-4,7]. Also the not to report on activations in areas 3a, 1 and 2. mean distance between D2-D3, D3-D4 and D4-D5 of 6.6 mm and 6.3 mm for main and differential effects, respec- We found activation in the anterior wall of the postcentral tively, is in good agreement with human electrophysio- gyrus, defined as area 3b according to our operational def- logical and fMRI data [2,4]. The larger distance between inition during tactile stimulation (Fig 1). More pro- the thumb and index finger as compared to distances nounced activation was noticed frequently in the crown between subsequent fingers suggests a larger representa- or posterior wall of the postcentral gyrus, defined as areas tion for the thumb. This finding is in agreement with 1 and 2 (Fig 2). Similar observations have been made in results from a study using electrocorticography with sub- other studies using both fMRI and PET [5,14]. According dural electrodes in three patients [1,12]. to studies in non-human primates the representation of the distal fingertips in area 1 points posteriorly, a finding With the spatial resolution used in this study, 3 × 3 × 3 confirmed in a recent fMRI-study on humans [15]. Area 2 3 3 mm , resampled to 1.5 × 1.5 × 1.5 mm , activation for all then is the mirror-image of area 1 with the fingertips five fingers was found in 17 of 18 subjects. For compari- pointing anteriorly. The activation in the posterior wall son, Kurth et al. used a resolution of 1.7 × 1.7 × 1.7 mm3 might represent activation in both areas 1 and 2 localised and electrical stimulation with ring electrodes and found at their meeting point, i.e. the fingertips. The larger cluster activation in area 3b for all five fingers in 7 out of 10 sub- size of this activation is explained by the clusters arising jects (70%) [4]. The present study showed activations for from area 1 and 2 being contiguous and therefore addi- all fingers in 94 % of subjects. This difference might be tive. In the present study the activation of area 1 and 2 is due to the higher field strength used in this study as the probably due to hierarchical processing in the rostrocau- higher magnetisation vector and sensitivity to changes in dal direction within S1. A previous observation that elec- susceptibility increase the signal-to-noise ratio. trical stimulation of the cutaneous afferents of the median nerve resulted in evoked potentials in area 3b after 30 Page 3 of 6 (page number not for citation purposes) BMC Neuroscience 2004, 5:28 http://www.biomedcentral.com/1471-2202/5/28 A p Figure 1 o rst-mortem bra eas of S1 as defined in cyto ins [18, 19] architectonic studies on 10 Activation in the contralatera tactile stimulation of the fingers ('main effec Figure 2 ts') in a single subject l somatosen of the right ha sory cortex during nd versus rest Areas of S1 as defined in cytoarchitectonic studies on 10 Activation in the contralateral somatosensory cortex during post-mortem brains [18, 19]: area 3a occupies the fundus of tactile stimulation of the fingers of the right hand versus rest the central sulcus (dark blue), area 3b the anterior wall of the in a single subject. The first column shows transverse ana- postcentral gyrus (red), area1 its crown (light blue) and area tomical image with z-coordinate indicated. Subsequent col- 2 its posterior wall (green). The black arrow indicates the umns show the activation patterns in S1 overlayed on central sulcus. magnified T1-weighted images for each finger. The location of the peak voxel in area 3b is indicated by blue crosshairs. msec while a potential in area 1 was seen after another 5 msec lends support to this assumption [16]. the local ethics committee and written informed consent was obtained. All volunteers had normal images on a Conclusion fluid-attenuated inversion recovery (FLAIR) sequence. In the group analysis, a somatotopic organisation for all the fingers in the hand representation of area 3b could be Stimulation demonstrated using fMRI; the Euclidian distance between Tactile stimulation consisted of brushing the glabrous the thumb and the little finger was well comparable to skin of the two distal phalanges of each finger continu- that determined in previous studies. On the subject level ously forwards and backwards with a commercially avail- the cortical somatosensory representation of the thumb able tooth brush. During the experiment, volunteers were was located laterally, anteriorly, and inferiorly to that of positioned on the MR table with their right arm from the the little finger in 14 out of 17 subjects. The spatial local- elbow down in a padded cast, that also provided support isation of the remaining fingers showed a less stringent for the dorsal part of the hand. They were instructed to rest somatotopic order when compared individually. their arm against the magnet bore so that both arm and hand were relaxed. Pieces of soft cloth were placed Methods between the fingers in order to avoid that stimulation also Subjects involved a neighbouring finger. Twenty healthy, self-reportedlly right-handed volunteers (6 male and 14 female, age 21–43 years, mean 29.4 years) The frequency was 1 Hz; no forced pressure was exerted. were included in the study. The protocol was approved by Consistency was tested on a finger model firmly taped Page 4 of 6 (page number not for citation purposes) BMC Neuroscience 2004, 5:28 http://www.biomedcentral.com/1471-2202/5/28 Postprocessing Image processing and analysis were carried out using the SPM99 soft ware package [17]. All functional images were resliced to a voxel size of 1.5 × 1.5 × 1.5 mm and then rea- ligned to the first image and coregistered to the T1- weighted image volume. All data were spatially filtered using an isotropic 4 mm, full-width, half-maximum Gaus- sian kernel. A high pass filter (cut off frequency 0.008 Hz) was applied to eliminate low frequency signal fluctua- tions. In order to preserve each subject's somatotopic arrangement in area 3b no normalization to a common brain atlas was performed. Distan m Figure 3 onds) ce to the thum and SEM (errorbar b (D1) s)for each fin , as presented in Table ger (mm), mean (dia- Data analysis Distance to the thumb (D1) for each finger (mm), mean (dia- Functional data from two subjects were excluded due to monds) and SEM (errorbars), as presented in Table. The major motion artefacts (subject no. 7) and global lack of coordinates for D1 are defined as origo [0, 0, 0]. Distances activation (subject no.18). Task specific effects were esti- to D1 are shown in the medial-lateral (M-L) direction, in the mated using the general linear model (GLM) that left panel also in the posterior-anterior (P-A) direction and in included a box car function convolved with the canonical the right panel also in the superior-inferior (S-I) direction. hemodynamic response function in SPM99. The effect of The fingers are sequentially positioned more medially, poste- sensory stimulation of each finger versus rest was deter- riorly and superiorly. mined using a one-sample t-test of pertinent linear con- trasts of parameter estimates in each subject with a significance level of p < 0.001 (uncorrected). Then the spatial coordinates of the peak activation voxel in area 3b onto a computerized electronic scale (Biopac Systems, DA were determined. Due to lack of neuroanatomical land- 100B, MP 100A; Macintosh Powerbook G3 with software marks, exact delineation of the cytoarchitectonically AcqKnowledge 3.5): the intra-examiner error was 18% defined areas within S1 cannot be achieved in MR images. based on a mean pressure of 6.64 g, standard deviation Therefore we used an operational definition based on 1.199 g. cytoarchitectonic studies of S1 on 10 post-mortem brains. In >50 % of these brains area 3a was located in the fundus Imaging of the central sulcus, area 3b in the rostral bank of the MRI was performed using a 3 T head scanner (Siemens postcentral gyrus and area 1 on its crown reaching down Allegra) with a quadrature birdcage coil. Morphological into the postcentral sulcus [18,19]. Fig 1 illustrates these T1-weighted images with a resolution of 1 × 1 × 1 mm locations, that continue along the central sulcus. As inter- using a magnetisation prepared gradient echo sequence areal borders vary across brains, the same authors con- (MPRAGE) were acquired. Functional echo-planar image structed probability maps for each area by superimposing volumes of the whole brain (number of slices = 49, thick- histological volumes of the individual brains on a compu- ) sensitised to the ness = 3 mm, voxel size = 3 × 3 × 3 mm terized reference brain. Volumes of interest (VOIs) were Blood Oxygenation Level Dependent (BOLD)-effect defined for each area in which >50 % of the brains had a (echo time = 30 ms) were acquired. Five scanning sessions representation of that area. Despite close relationship of were performed. Each session included 92 functional vol- areas 3a, 3b and 1 in the postcentral gyrus, the three VOIs umes with a temporal resolution of 3 seconds. The first overlapped by <1% of their volumes. These probability two volumes in each session were discarded from further maps were at hand when the spatial coordinates of the analysis to allow for initial T1-equilibrium effects. peak activation voxel in area 3b were determined. Acti- vated peak voxels were labelled as belonging to area 3b Experimental protocol when they were located within the anterior wall of the Fingers 1 to 5 (D1 = thumb, D5 = little finger) of the right postcentral gyrus (Figure 1). hand were stimulated sequentially in separate sessions according to a block design that included four periods of The spatial coordinates of the peak voxel for the thumb stimulation and five of rest for each finger. The epoch (D1) was defined as being at origo [0, 0, 0] in a 3D Carte- length for both stimulation and rest periods was 30 sian coordinate system.When the spatial coordinates for seconds. all fingers were known in all subjects, somatotopy was assessed by determining the average distances for the whole group from each finger to the thumb. Page 5 of 6 (page number not for citation purposes) BMC Neuroscience 2004, 5:28 http://www.biomedcentral.com/1471-2202/5/28 8. Kaas JH: Multiple representations of the body within the pri- Euclidian distances between fingers as well as from each mary somatosensory cortex of primates. Physiol Rev 1983, finger to the thumb (D1) were calculated as: 63(1):206-231. 9. Kurth R, Villringer K, Mackert BM, Schwiemann J, Braun J, Curio G, Villringer A, Wolf KJ: fMRI assessment of somatotopy in human () x −+ x (yy− )+(zz− ) DI DII DI DII DI DII Brodmann area 3b by electrical finger stimulation. NeuroRe- port 1998, 9(2):207-212. 10. Mogilner A, Grossman JA, Ribary U, Joliot M, Volkmann J, Rapaport with x , y and z representing the coordinates of the DI DI DI D, Beasley RW, Llinás RR: Somatosensory cortical plasticity in finger DI and x , y and z representing the coordi- DII DII DII adult humans revealed by magnetoencephalography. Proc nates of DII in the three directions x, y, z in a system where Natl Acad Sci 1993, 90:3593-3597. 11. Baumgartner C, Doppelbauer A, Sutherling WW, Zeitlhofer J, Lind- the coordinates of D1 are at origo [0, 0, 0]. inger G, Lind C, Deecke L: Human somatosensory cortical fin- ger representation as studied by combined neuromagnetic Statistics and neuroelectric measurements. Neurosci Lett 1991, 16(134(1)):103-8. Each finger's distance to the first finger was compared to 12. Sutherling WW, Levesque MF, Baumgartner C: Cortical sensory that of the directly neighbouring fingers using the Wil- representation of the human hand: size of finger regions and nonoverlapping digit somatotopy. Neurology 1992, coxon matched pairs test with a significance level of p < 42:1020-1028. 0.05. The Euclidian distances to the first finger were com- 13. Moore CI, Stern CE, Corkin S, Fischl B, Gray AC, Rosen BR, Dale AM: pared for each finger using the Wilcoxon matched pairs Segregation of somatosensory activation in the human rolandic cortex using fMRI. J Neurophysiol 2000, 84(1):558-69. test with a significance level of p < 0.05. 14. Burton H, MacLeod AM, Videen TO, Raichle ME: Multiple foci in parietal and frontal cortex activated by rubbing embossed grating patterns across fingerpads: a positron emission tom- Authors' contributions ography study in humans. Cereb Cortex 1997, 7:3-17. DvW conceived of the study, performed the image analy- 15. Blankenburg F, Ruben J, Meyer R, Schwiemann J, Villringer A: Evi- sis and drafted the manuscript. PF guided the image anal- dence for a rostral-to-caudal somatotopic organization in human primary somatosensory cortex with mirror-reversal ysis. JO designed the MR-parameters. EML participated in in areas 3b and 1. Cereb Cortex 2003, 13:987-993. the design of the study. BR and GL initiated and con- 16. Allison T, McCarthy G, Wood CC, Darcey TM, Spencer DD, William- ducted the stimulation consistency study. All authors read son PD: Human cortical potentials evoked by stimulation of the median nerve. I. Cytoarchitectonic areas generating and approved the final manuscript. short-latency activity. J Neurophysiol 1989, 62(3):694-710. 17. Statistical Parametric Mapping [http://www.fil.ion.ucl.ac.uk/ spm] Acknowledgments 18. Geyer S, Schleicher A, Zilles K: Areas 3a, 3b and 1 of Human pri- The authors thank dr S Geyer, Research Center Jülich, Germany for prob- mary Somatosensory cortex, 1. Microstructural organisa- ability maps delineating areas 3a, 3b and 1. This study was supported by the tion and interindividual variability. NeuroImage 1999, 10:63-83. Swedish Medical Research Council, the Swedish Brain Foundation, the 19. Geyer S, Schormann T, Mohlberg H, Zilles K: Areas 3a, 3b and 1 of Human primary Somatosensory cortex, 2. Spatial normali- Medical Faculty at Lund University, the Skåne County Council Research and sation to standard anatomical space. NeuroImage 2000, Development Foundation and the Royal Physiographic Society in Lund.. 11:684-696. Part of this work was presented at the annual meeting of the European Society for Magnetic Resonance in Medicine and Biology, Rotterdam 2003. References 1. Penfield W, Boldrey E: Somatic motor and sensory representa- tion in the cerebral cortex of man as studied by electrical stimulation. Brain 1937, 60:389-443. 2. Hari R, Karhu J, Hamalainen M, Knuutila J, Salonen O, Sams M, Vilk- man V: Functional organization of the human first and second somatosensory cortices: a neuromagnetic study. Eur J Neurosc 1993, 5:724-734. 3. Maldjian JA, Gottschalk A, Patel RS, Detre JA, Alsop DC: The sen- sory somatotopic map of the human hand demonstrated at 4 Tesla. NeuroImage 1999, 10:55-62. 4. Kurth R, Villringer K, Curio G, Wolf KJ, Krause T, Repenthin J, Schw- Publish with Bio Med Central and every iemann J, Deuchert M, Villringer A: fMRI shows multiple somato- scientist can read your work free of charge topic digit representations in human primary somatosensory cortex. NeuroReport 2000, 11:1487-1491. "BioMed Central will be the most significant development for 5. Gelnar PA, Krauss BR, Szeverenyi NM, Apkarian AV: Fingertip rep- disseminating the results of biomedical researc h in our lifetime." resentation in the human somatosensory cortex: an fMRI study. NeuroImage 1998, 7:261-283. Sir Paul Nurse, Cancer Research UK 6. Buchner H, Fuchs M, Wischmann HA, Dossel O, Ludwig I, Knepper Your research papers will be: A, Berg P: Source analysis of median nerve and finger stimu- lated somatosensory evoked potentials: multichannel simul- available free of charge to the entire biomedical community taneous recording of electric and magnetic fields combined peer reviewed and published immediately upon acceptance with 3D-MR tomography. Brain Topogr 1994, 6(4):299-310. 7. Kaas JH, Nelson RJ, Sur M, Lin CS, Merzenich MM: Multiple repre- cited in PubMed and archived on PubMed Central sentations of the body within the primary somatosensory yours — you keep the copyright cortex of primates. Science 1979, 204:521-523. BioMedcentral Submit your manuscript here: http://www.biomedcentral.com/info/publishing_adv.asp Page 6 of 6 (page number not for citation purposes)

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