Abstract

Characterizing the cortical representation of the body surface is fundamental to understanding the neural basis of human somatic sensation. Monkey studies benefited from the detailed somatotopic maps obtained from electrophysiology methods. Advances in noninvasive neuroimaging techniques now permit such questions to be probed in humans. The present study characterizes the detailed somatotopic representation of individual digits within subregions of the postcentral gyrus in humans using high-spatial resolution functional magnetic resonance imaging and surface-based mapping. Four areas of consistent activation included area 3b, area 2, and 2 discrete foci within area 1. Area 3b and the superior area 1 foci demonstrated an orderly somatotopic distribution for all digits of the hand, whereby the thumb was represented most lateral, anterior, and inferior and the fifth digit was most medial, posterior, and superior. Compared with area 3b, somatotopic variability was greater in area 1 and the digits spanned less cortical territory. This study additionally identified the specific digit pairs that are separable in areas 3b and 1 using current imaging methods. Somatotopy was not resolved in area 2 or in the inferior area 1 foci.

Introduction

The classic cytoarchitectural studies of Brodmann identified cortical areas 3, 1, and 2 within the postcentral gyrus of humans (Brodmann 1909), and area 3 was subsequently divided into 3a and 3b (Vogt and Vogt 1919). Recent anatomical studies continue to support these delineations (Geyer et al. 1997; White et al. 1997). Parallel anatomical subdivisions of the postcentral gyrus exist in monkeys (Merzenich et al. 1978; Kaas et al. 1979) and decades of physiological studies have detailed the response properties characteristic of each area. Area 3a is located in the fundus of the central sulcus and is driven by proprioceptive input (Iwamura et al. 1993). Areas 3b and 1 are located in the anterior bank and crown of the postcentral gyrus, respectively, and receive their dominant input from cutaneous sources (Powell and Mountcastle 1968; Sur et al. 1980). Area 2 occupies the posterior crown of the postcentral gyrus and the postcentral sulcus, and responds to a combination of proprioceptive and cutaneous inputs (Hyvarinen and Poranen 1978; Iwamura and Tanaka 1978). The progressive increase in receptive field size, and the convergence of submodal input from anterior to posterior areas suggests a hierarchy in the organization of processing within the postcentral gyrus (Iwamura 1998), a feature consistent with other mammalian sensory systems.

Electrophysiological studies in monkeys define 4 discrete somatotopic representations of the body surface, one in each of 3a, 3b, 1, and 2 (Sur et al. 1982), with a mirror reversal of representation along the 3b and area 1 border (Kaas et al. 1979). Variability in the somatotopic distributions is observed between and within monkey species (Merzenich et al. 1987) and may reflect use dependent plasticity (Xerri et al. 1996). There are also reports of distinct representations within area 1 each representing submodal inputs of pressure, flutter, and vibration (Friedman et al. 2004).

In the human postcentral gyrus, Penfield demonstrated the existence of a single somatotopic map (Penfield and Jasper 1954), presumed to be in area 1 due to the location of the stimulating electrodes on the cortical surface (Mountcastle 2005). Neuroimaging studies demonstrate 1 (magnetoencephalography [MEG]; Baumgartner et al. 1991; Yang et al. 1993), fMRI; (Disbrow et al. 1998), 2 (positron emission tomography [PET]; Burton et al. 1997), fMRI; (Francis et al. 2000; Kurth et al. 2000; Moore et al. 2000), and 4 (Gelnar et al. 1998) distinct representations following stimulation of a body part, with a mirror reversal in some instances across the 3b/1 border (Blankenburg et al. 2003). Imaging studies support a hand-level somatotopic arrangement in area 3b with the thumb located lateral, anterior, and inferior to the other digit tested (D1 vs. D5, Kurth et al. 2000; D2 vs. D5, Kurth et al. 1998), though not all studies agree (Gelnar et al. 1998). Digit-level somatotopy is reported using MEG (Nakamura et al. 1998) and fMRI (van Westen et al. 2004) such that adjacent fingers on the hand occupy adjacent cortical territory. Less is known about the representation of the hand in area 1, though a general hand-level somatotopic representation is reported (D1 vs. D5, Kurth et al. 2000; D2 vs. D4, (Butterworth et al. 2003). Using electrical stimulation Penfield and Rasmusson (1950) identified 2 finger regions within probable area 1; the “hand” area evoked sensations in all digits and the hand, and the “digit” area was associated with percepts localized to single but more often multiple digits.

Delineating fine somatotopy of the hand is necessary for related studies of cortical plasticity such as in stroke and focal hand dystonia, and for drawing parallels between the hand representation in human and nonhuman primates. These parallels are an essential link to understanding the neural basis for human somatic sensation. The goal of this study was to investigate the somatotopic organization for individual digits within the cortical areas of the postcentral gyrus. This was achieved using high-resolution fMRI, surface-based mapping, and a vibrotactile stimulus that evokes reproducible, robust activation in the postcentral gyrus of both humans (Aparicio et al. 2005; Moore et al. 2005) and monkeys (Nelson et al. 2007). It was hypothesized that area 1 would exhibit an orderly, sequential distribution amongst digits (digit-level somatotopy), supporting the electrophysiology mapping studies obtained in monkeys (Sur et al. 1982). We additionally sought to confirm digit-level somatotopy in area 3b (van Westen et al. 2004) and investigate somatotopy in area 2.

Materials and Methods

Twelve healthy right-handed subjects (8 females, mean age 45 years, range 25–66 years) participated for 1 h of MRI scanning. The right hand was studied in each participant. This study was approved by the University Health Network Research Ethics Board.

Imaging Techniques

fMRI was conducted on a 3-T GE scanner using an 8-channel volume headcoil to optimize signal. Anatomical images were acquired with 3D fast spoiled gradient recalled inversion recovery prepped using a 20 cm field of view (FOV) (256 × 256) for 172 slices in total. Functional runs were acquired with gradient echo planar imaging over 32 contiguous coronal slices of 2.4 mm thickness with an in-plane resolution of 2.08 mm (FOV = 20 cm, 96 × 96 matrix, time repetition [TR] = 2 s, time echo = 30 ms, flip angle = 85°). Slice acquisition was centered over the central sulcus and the 7.6 cm of coverage generally extended from the precentral sulcus to the posterior parietal cortex. The voxel resolution (∼10 mm3) was similar to that used at 4 T (Maldjian et al. 1999) and exceeds that used elsewhere (Gelnar et al. 1998; Kurth et al. 2000; Moore et al. 2000; Krause et al. 2001; van Westen et al. 2004).

Stimulation Parameters

Vibrotactile stimuli were delivered via a piezoelectric bimorph bender (Noliac, Denmark) that drove a small mounted plastic post (3 mm diameter) upwards into the volar surface of the fingertip. The prone fingertip rested on a 5-mm hole in a custom-built acrylic surface and the plastic post was displaced 0.5 mm into the digit tip prior to the onset of vibration. The vibration frequency of 23 Hz was chosen to potentially bias the recruitment of Meissner corpuscle mechanoreceptors in the skin surface (Jones and Lederman 2006) though coactivation of multiple afferent types cannot be excluded (Tommerdahl et al. 2005). Labview software was used to control the timing, frequency, and amplitude of sinusoid waveforms, and the output was sent to a 15× linear amplifier (Sensor Technologies, Canada). The amplitude of vibration was 80 μm based on 150 V used to drive the piezoceramic (Nelson et al. 2007); this value is only approximate given the inevitable variability in skin compliance across subjects. Control of vibrotactile amplitude is necessary given the increase in fMRI signal intensity and spatial spread as a consequence of increasing stimulus intensity (Krause et al. 2001; Nelson et al. 2004) that could result from changes in surround inhibition (Simons et al. 2005). Each scan was 300 s (TR = 2 s) and consisted of 10 cycles of alternating periods of no vibration (22 s) and vibration (8 s), always beginning with a period of no vibration. The duration of stimulation is another important consideration and recent optical imaging data confirms that longer duration vibration (i.e., 5 s vs. 2, 1, or 0.5 s) evoke responses across a smaller spatial extent (Chiu et al. 2005; Simons et al. 2007), suggesting that blocked and not event-related designs may be better suited to expose fine somatotopy. All digit tips of the right hand were stimulated in separate scans. The order of digit stimulation was randomized across subjects and when possible, multiple runs were acquired for each digit for within-session reproducibility.

Division of the Primary Somatosensory Cortex (SI) into Subregions

Identifying the omega-shaped folding of the central sulcus in the axial plane assisted with localizing the hand region within the postcentral gyrus (White et al. 1997). This region was identified for each subject and the anatomical data was further subdivided into probable areas 3a, 3b, 1, and 2 using the sulcal and gyral borders from the surface-inflated maps. Delineations are similar to previous publications (Moore et al. 2000; van Westen et al. 2004) and abide by the definitions based on cytoarchitecture and receptor mapping (Geyer et al. 1997). Area 3a was defined as the region occupying the fundus of the central sulcus. Area 3b was defined as the gray matter occupying the posterior bank of the central sulcus extending to but not including the crown of the postcentral gyrus. Area 1 was defined as the crown of the postcentral gyrus from the central sulcus (anterior) and included the “border” region described elsewhere (Moore et al. 2000). Area 2 was defined as the anterior bank of the postcentral sulcus, although it is known that area 1 may also occupy this territory (Geyer et al. 1997).

FMRI Analyses

fMRI statistical map analyses used a combination of software including Analysis of Functional Neuroimages, with the surface-based mapping tool SUMA (Cox 1996), and Freesurfer (Dale et al. 1999). Time-series data were first motion corrected in 3 spatial dimensions to reduce the effects of small head motion (Cox and Jesmanowicz 1999). Time-series analysis was performed with an orthogonalized boxcar correlation (Bandettini et al. 1993; Cox and Jesmanowicz 1999) where the temporal profile of the hypothesized hemodynamic response function followed the off and on vibration cycles and was shifted 2 TR (4 s) to accommodate the response lag. To preserve the spatial resolution obtained during acquisition, no spatial smoothing was applied to the time-series data or to the statistical maps, and all the analyses were conducted within individual subjects.

Freesurfer software was used to generate a model of the cortical surface using the structural T1-weighted image for each subject—a process that involves intensity normalization, skull removal, segmentation, and tessellation (Dale et al. 1999). Statistical maps were aligned with the cortical surface with the software SUMA and the Talairach transform was applied to both the surface and the statistical maps. This step allows the observed activation to be reported in standardized space while preserving the anatomical–functional relationship within subjects. Activation in subregions was deemed significant if a cluster was formed that met or exceeded 2 contiguous voxels at a threshold of P = 0.001. The Talairach coordinates from the highest correlated voxel within the cluster were used for further analysis. This study was not designed to investigate the overlap amongst adjacent digits.

Statistical Analyses

Two statistical approaches were used to assess somatotopy within each region. The first examined the separation of 2 digits in 3-dimensional space. The Euclidean distance was computed between digit 1 and all other digits using the following formula: 

graphic

Euclidean distances were then compared for each adjacent digit pair (D1 vs. D2, D2 vs. D3, D3 vs. D4, D4, vs. D5) using the nonparametric Wilcoxon signed-rank test (van Westen et al. 2004). Significance was set at P ≤ 0.0125 for a 2-tailed test with alpha corrected for 4 comparisons.

The second approach investigated digit separation within a single image axis: x (medial–lateral), y (anterior–posterior), and z (inferior–superior). The Talairach coordinates for each image axis were subjected to a Wilcoxon signed-rank test for adjacent digit pairs (D1 vs. D2, D2 vs. D3, D3 vs. D4, D4 vs. D5) for each subregion activated. A total 4 comparisons were performed for each axis and significance was set as described above.

Results

Identification of Subregions within SI

Activation was observed in the posterior bank of the central sulcus (area 3b), the crown of the postcentral gyrus (area 1), and the anterior bank of the postcentral sulcus (area 2). Two discrete activation foci were observed within the crown of the postcentral gyrus (putative area 1), one in close proximity and superior to 3b activation and the other at an anterior, and inferior location. To our knowledge this observation has not been reported and we therefore refer to the superiorly located activation as area 1s and the inferior activation as area 1i. Area 3b was activated in all subjects for almost all digits stimulated. Other areas were responsive in most but not all subjects, with the lowest response occurrence for stimulation of the 4th or 5th digit (Table 1). Activation in probable area 3a was infrequent (3 out of 12 subjects) and when present, occurred most often by vibration of digit 1 or 2. The low incidence of 3a activity is similar to that reported elsewhere (Moore et al. 2000) is likely attributable to the nonproprioceptive nature of the probing stimulus. Data obtained from 3a were not used in the analysis of somatotopy.

Table 1

Occurrence of activation within subregions of the postcentral gyrus (1s and 1i correspond to the superior and inferior foci in putative area 1, respectively)

 D1 D2 D3 D4 D5 
3b 12 12 12 12 11 
1s 10 11 10 
1i 10 10 10 
10 11 10 
 D1 D2 D3 D4 D5 
3b 12 12 12 12 11 
1s 10 11 10 
1i 10 10 10 
10 11 10 

The location of the 4 identified subregions (Talairach space, mm) is plotted in Figure 1. This figure emphasizes the spatial separation between areas; area 1s and 1i are separated by 7.9 ± 1.6 mm (Euclidean distance), and area 2 and 1i are 4.7 ± 0.6 mm apart, differentiated only in the anterior–posterior direction. The figure also demonstrates the spatial relationship amongst the 4 areas in the postcentral gyrus using a standardized atlas for future comparisons. The averaged Talairach location for each focus (averaged across all digits) is reported in Table 2. Also reported are the Euclidean distances spanned by the most widely separated digit pair (D1–D5 for all areas) within each area. An example of the areas of activation is shown for 1 subject in Figure 2 (top).

Table 2

Average Talaraich coordinates and Euclidean distance spanned across digits

 x y z Distance (D1–D5 mm) 
3b 43.0 (4.7) 20.2 (4.4) 51.0 (6.4) 17.9 (4.6) 
1s 43.4 (5.4) 20.9 (5.9) 58.4 (4.2) 14.9 (3.9) 
1i 53.6 (4.4) 14.9 (3.0) 46.7 (4.3) 4.4 (3.8) 
53.9 (4.4) 21.7 (4.0) 46.8 (5.6) 6.8 (7.1) 
 x y z Distance (D1–D5 mm) 
3b 43.0 (4.7) 20.2 (4.4) 51.0 (6.4) 17.9 (4.6) 
1s 43.4 (5.4) 20.9 (5.9) 58.4 (4.2) 14.9 (3.9) 
1i 53.6 (4.4) 14.9 (3.0) 46.7 (4.3) 4.4 (3.8) 
53.9 (4.4) 21.7 (4.0) 46.8 (5.6) 6.8 (7.1) 
Figure 1.

Localization of subregions in Talairach space (mm). Inferior–superior (I, S) plotted against medial–lateral (M, L, top), and anterior–posterior (A, P, bottom) for the average coordinates obtained within each subregion (1s, 3b, 1i, 2). Five data points are shown for each subregion and correspond to the digit stimulated. Digit-specific information is suppressed to highlight the distribution pattern and spatial relation among subregions.

Figure 1.

Localization of subregions in Talairach space (mm). Inferior–superior (I, S) plotted against medial–lateral (M, L, top), and anterior–posterior (A, P, bottom) for the average coordinates obtained within each subregion (1s, 3b, 1i, 2). Five data points are shown for each subregion and correspond to the digit stimulated. Digit-specific information is suppressed to highlight the distribution pattern and spatial relation among subregions.

Figure 2.

Area 3b somatotopy—individual subject. Top: Surface-based map of 1 subject demonstrating activation in areas 3b, 1s, 1i, and occasionally area 2 for each digit stimulated. Note that the surface map unfolds the central sulcus to improve visualization of activated regions (green line). Digit representation in areas 3b and 1s move superiorly in the transition from D1 through D5. Area 1i remains relatively unaltered and area 2 activation is inconsistent across the digits stimulated. Bottom: Surface-based map plotted on image slices to highlight somatotopy in 3b in the inferior–superior and lateral–medial planes. Talairach coordinate in top left of each image.

Figure 2.

Area 3b somatotopy—individual subject. Top: Surface-based map of 1 subject demonstrating activation in areas 3b, 1s, 1i, and occasionally area 2 for each digit stimulated. Note that the surface map unfolds the central sulcus to improve visualization of activated regions (green line). Digit representation in areas 3b and 1s move superiorly in the transition from D1 through D5. Area 1i remains relatively unaltered and area 2 activation is inconsistent across the digits stimulated. Bottom: Surface-based map plotted on image slices to highlight somatotopy in 3b in the inferior–superior and lateral–medial planes. Talairach coordinate in top left of each image.

Somatotopy within Subregions

Area 3b demonstrated a clear somatotopic organization; D1 was located most lateral, anterior, and inferior and D5 most medial, posterior, and superior. Intervening digits followed an orderly topography thereby supporting the predicted digit-level somatotopy. Surface-based maps demonstrate the inferior to superior progression from D1 to D5 for area 3b as shown in a single subject (Fig. 2, top). For ease of comparison with published works, the identical data are displayed on axial and sagittal slices (below); note the inferior–superior and lateral–medial somatotopy. An example of area 3b from a different subject is shown in Figure 3 to highlight the between-subject variability in the absolute superior-inferior (S-I) location of each digit representation (e.g., D1 is at z = 46 in Fig. 3 and at z = 41 for different subject in Fig. 2) yet digit somatotopy is preserved in both cases.

Figure 3.

Area 3b somatotopy—individual subject. Area 3b activation in a single subject demonstrate somatotopic shift in the inferior–superior axes. Note also the between-subject variability in the z-distance spanned by all digits (8 mm vs. 14 mm in the subject shown in Figure 2).

Figure 3.

Area 3b somatotopy—individual subject. Area 3b activation in a single subject demonstrate somatotopic shift in the inferior–superior axes. Note also the between-subject variability in the z-distance spanned by all digits (8 mm vs. 14 mm in the subject shown in Figure 2).

To assess whether adjacent digits in area 3b are separable in 3-dimensional space the Euclidean distance was calculated for each digit relative to the location of D1 and resulting distances were subjected to a Wilcoxon signed-rank nonparametric test. The average Euclidean distance (with standard error) between D1 and each digit is shown in Figure 4 (top, left) for the group. As predicted, distance increases between D1 and each sequential digit representation. Adjacent digit pairs that are significantly separable in 3-dimensional space include D1 versus D2 (P = 0.002) and D3 versus D4, (P = 0.003). D1 and D2 are separated by 7.2 mm (±0.3) and all other digit pairs are separated by ∼4 mm with the exception of D4 and D5 that exist within ∼1.5 mm in the group averaged data. Figure 4 (top, right) plots the Euclidean distances obtained for each participant. Note that all subjects demonstrate hand-level somatotopy (i.e., between D1 and D5), and all but one subject demonstrates digit-level somatotopy (subject shown in bright green whereby D3 is closer to D1 than D2). In summary, measures of digit representation in Euclidean distance allow each digit to be dissociated from an adjacent digit, with the exception of D5 that could not be resolved from D4.

Figure 4.

Area 3b somatotopy—group data. (A) Euclidean distance from thumb to other digits for group (n = 12) and individual subjects (right). Note the increasing distance from D1 from D2 to D5. *P ≤ 0.0125. (B) Group averaged Talairach coordinates for each digit in the inferior–superior axes versus medial–lateral (left) and anterior–posterior (right). Talairach distance is expressed in mm. Error bars represent standard errors.

Figure 4.

Area 3b somatotopy—group data. (A) Euclidean distance from thumb to other digits for group (n = 12) and individual subjects (right). Note the increasing distance from D1 from D2 to D5. *P ≤ 0.0125. (B) Group averaged Talairach coordinates for each digit in the inferior–superior axes versus medial–lateral (left) and anterior–posterior (right). Talairach distance is expressed in mm. Error bars represent standard errors.

To determine whether adjacent digits in 3b are separable within a single image axis, a Wilcoxon signed-rank test was performed on each adjacent digit pair using the Talairach coordinates for each digit representation (Table 3, Figure 4 bottom) displays the average location for each digit in Talairach space in the medial–lateral (left) and anterior–posterior (right) image planes. This analyses revealed the significant dissociations between adjacent digit representations within a single imaging plane; digits dissociable in the inferior–superior direction include D1 versus D2 (P = 0.002), D2 versus D3 (P = 0.003), and D3 versus D4 (P = 0.003) but not D4 versus D5 (P = 0.07). In the medial–lateral direction dissociations include D1 versus D2 (P = 0.007) and D3 versus D4 (P = 0.006). No adjacent digits were separable in the anterior–posterior direction. In-plane 3b somatotopy is therefore best observed in the inferior–superior direction and in the medial–lateral axis for most digits. Adjacent digit pairs could not be dissociated in the anterior–posterior direction, despite the observed digit-level somatotopy in this image plane.

Table 3

Average Talaraich coordinates for each digit in each subregion

 3b 1s 1i 
D1 47.9, 17.0, 43.3 (3.2, 3.6, 3.4) 48, 17.2, 53.6 (5.2, 4.8, 4.0) 53, 15.8, 47 (3.8, 3.3, 4.7) 54.1, 22.4, 46.1 (5.8, 5.1,6.1) 
D2 44.0, 18.3, 47.1 (3.9, 4.4, 3.7) 44.5, 19.4, 57.5 (3.2, 5.8, 3.7) 55.1, 15, 46 (4.2, 3.1, 4.138) 54.1, 21.7, 46.9 (4.2, 4.4, 6.5) 
D3 42.9, 19.5, 51.4 (4.3, 3.8, 4.5) 42.6, 20.6, 58.6 (3.8, 4.4, 2.4) 53.9, 15.5, 46.2 (4.8, 3.1, 5.2) 53.2, 22.6, 48.6 (3.9, 2.6, 5.0) 
D4 40.2, 22, 56.0 (3.5, 3.6, 3.6) 42.2, 22.6, 61.1 (6.6, 6.3, 3.1) 53.2, 13.8, 47 (4.8, 2.64, 3.8) 54.3, 21.5, 46.8 (5.1, 3.9, 5.8) 
D5 39.9, 24.1, 57.0 (3.7, 3.4, 3.6) 39.3, 25.6, 61.8 (4.8, 5.5, 2.5) 52.6, 14.2, 47.8 (4.8, 3.2, 4.2) 54.1, 20, 45.2 (3.0, 4.1, 4.9) 
 3b 1s 1i 
D1 47.9, 17.0, 43.3 (3.2, 3.6, 3.4) 48, 17.2, 53.6 (5.2, 4.8, 4.0) 53, 15.8, 47 (3.8, 3.3, 4.7) 54.1, 22.4, 46.1 (5.8, 5.1,6.1) 
D2 44.0, 18.3, 47.1 (3.9, 4.4, 3.7) 44.5, 19.4, 57.5 (3.2, 5.8, 3.7) 55.1, 15, 46 (4.2, 3.1, 4.138) 54.1, 21.7, 46.9 (4.2, 4.4, 6.5) 
D3 42.9, 19.5, 51.4 (4.3, 3.8, 4.5) 42.6, 20.6, 58.6 (3.8, 4.4, 2.4) 53.9, 15.5, 46.2 (4.8, 3.1, 5.2) 53.2, 22.6, 48.6 (3.9, 2.6, 5.0) 
D4 40.2, 22, 56.0 (3.5, 3.6, 3.6) 42.2, 22.6, 61.1 (6.6, 6.3, 3.1) 53.2, 13.8, 47 (4.8, 2.64, 3.8) 54.3, 21.5, 46.8 (5.1, 3.9, 5.8) 
D5 39.9, 24.1, 57.0 (3.7, 3.4, 3.6) 39.3, 25.6, 61.8 (4.8, 5.5, 2.5) 52.6, 14.2, 47.8 (4.8, 3.2, 4.2) 54.1, 20, 45.2 (3.0, 4.1, 4.9) 

Activation in area 1s revealed a digit-level somatotopic pattern that paralleled area 3b and is shown in Figures 2 and 5 for 2 subjects. On average, the 3-dimensional distance progressively increases between D1 and each sequential digit representation though only adjacent pair D1 and D2 showed significant separation (P = 0.005) in 3-dimensional space (Fig. 6, top, left). In general, D1 is represented most lateral, anterior, and inferior, D5 is most medial, posterior, and superior, and all other digits follow an orderly transition between these 2 representations. The somatotopic trends for each subject who activated 1s for all digits are shown in Figure 6 (top, right). All subjects demonstrate hand-level somatotopy and only 2 subjects fail to exhibit digit-level organization (brown line at D3, pink line at D4). Average Talairach coordinates for each digit representation within area 1s are plotted in Figure 6 (bottom). To further assess the statistical ability to dissociate digit pairs in 1s, each digit and its second nearest neighbor were compared and significant separation was observed for D1 versus D3 (P = 0.005). The second statistical analysis revealed that only D1 and D2 could be modestly separated within a single plane, the inferior-superior axis (P = 0.011). To summarize, area 1s demonstrates digit-level somatotopy and only adjacent digits D1 and D2 are separable, all other digits are resolvable from D1 only.

Figure 5.

Area 1s somatotopy—individual subject. Activation in area 1s in a single subject. Note that 1s follows an inferior–superior and lateral–medial progression from D1 to D5 as shown here in axial and sagittal planes.

Figure 5.

Area 1s somatotopy—individual subject. Activation in area 1s in a single subject. Note that 1s follows an inferior–superior and lateral–medial progression from D1 to D5 as shown here in axial and sagittal planes.

Figure 6.

Area 1s somatotopy—group data. (A) Group averaged (left) and individual subject (right) Euclidean distances (mm) for each digit from D1. Error bars represent standard errors. (B) Group averaged Talairach coordinates for each digit in the inferior–superior axes versus medial–lateral (left) and anterior–posterior (right). Talairach distance is expressed in mm. *P ≤ 0.0125.

Figure 6.

Area 1s somatotopy—group data. (A) Group averaged (left) and individual subject (right) Euclidean distances (mm) for each digit from D1. Error bars represent standard errors. (B) Group averaged Talairach coordinates for each digit in the inferior–superior axes versus medial–lateral (left) and anterior–posterior (right). Talairach distance is expressed in mm. *P ≤ 0.0125.

Activation in area 1i and area 2 is shown in Figure 7. The top row demonstrates activation in 1 subject to highlight the proximity of the 2 foci with respect to each other, and to show the relatively unchanging focus of activation for different digits stimulated. The same observation can be seen in a different subject below. The average Talairach coordinates are plotted on 2 axes in Figure 8. A modest anterior to posterior somatotopy can be seen in area 1i, with D1 most posterior and D4/D5 most anterior—a reversal of that observed in 3b and 1s. A similar observation is made in area 2; D5 is anterior relative to other digits. Despite these observations, statistical analyses revealed that adjacent digits could not be separated in 3-dimensional space (i.e., no digit-level somatotopy), and widely separated digits (D1 vs. D5) were also not separable indicating the lack of hand-level somatotopy. No digit representations were dissociable within a single axis in areas 1i and area 2.

Figure 7.

Activation in area 1i and area 2. Top—Gyral maps from 1 subject demonstrating the location of area 1i and 2 relative to each other. Bottom—activation maps for 1 subject for area 1i. No clear somatotopic organization is observed and specific localization of activation is shared amongst digits.

Figure 7.

Activation in area 1i and area 2. Top—Gyral maps from 1 subject demonstrating the location of area 1i and 2 relative to each other. Bottom—activation maps for 1 subject for area 1i. No clear somatotopic organization is observed and specific localization of activation is shared amongst digits.

Figure 8.

Activation in area 1i and area 2—group data. Top—Group averaged Talairach coordinates for each digit representation in area 1s for the medial–lateral (left) and anterior–posterior (right) axes. A general medial (M)–lateral (L) orderly representation is observed, however D1 fails to obey this order in the Medial-Lateral and inferior (I)–superior (S) axes. Anterior–posterior plot (right) suggests that D4 and D5 are positioned anterior to D1, D2 and D3, a reversal of A–P somatotopy observed in area 3b and 1i. Bottom—Group averaged Talairach coordinates for area 2 reveal a similar anterior–posterior distribution where D4 and D5 are localized anterior to other digit representations. Error bars represent standard errors.

Figure 8.

Activation in area 1i and area 2—group data. Top—Group averaged Talairach coordinates for each digit representation in area 1s for the medial–lateral (left) and anterior–posterior (right) axes. A general medial (M)–lateral (L) orderly representation is observed, however D1 fails to obey this order in the Medial-Lateral and inferior (I)–superior (S) axes. Anterior–posterior plot (right) suggests that D4 and D5 are positioned anterior to D1, D2 and D3, a reversal of A–P somatotopy observed in area 3b and 1i. Bottom—Group averaged Talairach coordinates for area 2 reveal a similar anterior–posterior distribution where D4 and D5 are localized anterior to other digit representations. Error bars represent standard errors.

Discussion

The quest to resolve somatotopy in the postcentral gyrus of humans has a lengthy history that began with identifying a single representation of the body surface (Penfield and Boldrey 1937; Penfield and Jasper 1954). Modern neuroimaging methods confirm multiple representations of body surfaces, some of which are assigned to area 3b, area 1, and area 2 (Gelnar et al. 1998; Moore et al. 2000). The goal of this study was to delineate fine somatotopy of the fingers within the cortical areas of the postcentral gyrus using high-resolution fMRI with surface-based mapping. High-resolution fMRI was achieved using an 8-channel headcoil at 3 T and limiting the coverage to the pre- and postcentral cortex yielding a voxel resolution of ∼10 mm3. We have described 4 areas of activation in the hand area; 1 focus in area 3b, 2 within the surface of the postcentral gyrus (area 1), and 1 in area 2. The observation of 2 discrete foci within the defined area 1 boundary was unexpected, and only one focus demonstrated a somatotopic arrangement similar to that observed in area 3b. No evidence for digit or hand-level somatotopy was observed in area 2.

The present study reports digit-level somatotopy in area 3b in support of van Westen et al. (2004). Using high-spatial resolution (27 mm3) at 3 T the latter authors report several observations that are remarkably similar to that reported here such as the distance spanned by D1–D5 (17.2 mm vs. our 17.9 mm), the increasing Euclidean distance between D1 and each sequential digit on the hand, and the resolution of D1 versus D2 in the inferior–superior axis. We additionally report that each digit on the hand is distinguishable from adjacent digits with the exception of D5. Results from other fMRI studies have varied, likely the result of a variety of methods used. At 1.5 T using electrical stimulation, hand-level somatotopic organization was observed in 5 of 20 subjects (D2 vs. D5, Kurth et al. 1998) and 7 out of 10 subjects (D1 vs. D5, Kurth et al. 2000) with the interdigit distance spanning 12 and ∼16 mm, respectively. Although Maldjian et al. (1999) did not assign activation to areas within the postcentral gyrus, inspection of the reported coordinates suggests somatotopy in area 3b was observed in 3 of 5 subjects at 4 T using vibrotactile stimuli.

We report the existence of digit-level somatotopy within area 1s with an orderly distribution in the anterior–posterior, medial–lateral, and inferior–superior directions. Kurth et al. (2000) compared the representation of D1 versus D5 whose distance spanned 14.2 mm with D1 represented medially. Though no coordinates are reported, inspection of their figures suggests that the activation focus corresponds to area 1s reported here, and we also report a D1–D5 distance of 14.9 mm. Despite the improved resolution and clear somatotopic pattern in area 1s, only adjacent digits D1 and D2 were separable, and all other digits were distinguishable only if compared with D1. This may relate to the statistical power (i.e., n = 9 and 11 for areas 1s and 3b, respectively), or may result from the lower resolution in the anterior-posterior (A-P) direction (2.4 mm) compared with the other axes (2.08 mm).

Somatotopic organization of area 3b differed from that observed in area 1s. First, digit representations in area 1s more frequently deviated from strict somatotopy, a finding supported by a recent study with electrical stimulation to D2 and D3 (Ruben et al. 2006). Second, the digits occupied a smaller total spatial extent in area 1s (14.9 vs. 17.9 mm), and if each digit is assumed to occupy equal width the average interdigit separation in area 3b is ∼5 mm, compared with ∼4 mm in area 1s. This observation could be the result of greater digit overlap in area 1s and/or decreased cortical territory allocated to each digit. Monkey studies report similar differences such that digit representation in area 1 occupies a smaller spatial extent (Sur et al. 1980), with greater overlap (Iwamura et al. 1983; Tommerdahl et al. 2002), and larger variability (Merzenich et al. 1987) that leads to less strict topography compared with area 3b (Mountcastle 2005). One feature common to 3b and 1s was the interdigit separation between D1 and D2: it is greater than all other adjacent digits and is ∼7 mm in both areas. This observation may support the larger spatial extent occupied by the thumb in 3b (Nakamura et al. 1998) and, compared with area 3b suggests an even larger thumb representation in area 1s where the overall territory dedicated to the digits was smaller. The latter suggestion would be predicted from Penfield's classic sensory homunculus though the schematic was not intended for literal interpretation (Penfield and Rasmusson 1950).

Area 2 of monkeys consists of a complete map of the body surface. However, in area 2 neurons have multidigit receptive fields, multiple representations for single digits (Pons et al. 1985; Pons et al. 1987) and data in awake macaques do not support the somatotopic segregation of each finger (Iwamura et al. 1980). In humans, activation in probable area 2 has been observed in neuroimaging studies (Gelnar et al. 1998; Kurth et al. 2000; Moore et al. 2000). Our data suggest that the spatial extent of the digit representation in area 2 is relatively small being ∼7 mm and that the exact location is highly variable between subjects. We did not observe any resemblance of an orderly topographic representation in the medial–lateral or inferior–superior directions but did note the possibility of an anterior–posterior pattern; D5 is located anterior to all other digits. If digit somatotopy does exist in human area 2, it is beyond the spatial resolution of this investigation. Further, given the converging input in area 2 by cutaneous and proprioceptive input (Iwamura et al. 1980), other stimulus types that combine these submodalities may be better suited to expose the somatotopic organization.

We identified a second activation focus in the surface of postcentral gyrus that also corresponds to probable area 1 as defined by cytoarchitecture and receptor-based mapping (Geyer et al. 1997). This focus occupied a small spatial extent (4.4 ± 3.8 mm) that was clearly distinct from the area 1 site on the crown of the postcentral gyrus; the 2 areas were separated by ∼5 mm in the S-I and medial-lateral (M-L) planes and ∼2 mm in the A–P axis. These distances and the observation that activation within each area survived high, conservative thresholds suggest that they are indeed, different activation sites within putative area 1. This second focus, positioned anterior, inferior, and close to the 3b border did not demonstrate somatotopy and was activated by stimulation to all digits. To our knowledge this is the first neuroimaging report of an additional focus in human area 1 and calls into question the widely accepted view of a singular representation of the body surface originally proposed in humans (Penfield and Boldrey 1937).

A review of the findings of Penfield and Rasmusson (1950) and the schematic sensory homunculus exposes 2 representations of the hand within area 1—one referred to as the “hand” area and the other representing each of the digits. As reported by the authors, electrical stimulation to the “hand” area evoked sensations in the hand and the digits, and occasionally other body surfaces (Penfield and Rasmusson 1950, p. 33). Electrical stimulation of the digit area rarely evoked percepts in single fingers and sensations typically encompassed multiple digits casting doubt on the differentiated digits depicted in the homunculus. Nonetheless, the classic data suggest that 2 foci within area 1 are associated with sensations on the digits. Support for multiple subregions within area 1 of humans is also found in the historical cytoarchitectural works of Brodmann (1909) who, in his description of area 1 identifies a “mixed cortical type” at the lower end of the postcentral gyrus that is notably different than area 43 on the Rolandic cortex (Garey 1999). More recently, Geyer et al. (1997) report 2 distinct regions within area 1 that were distinguishable neurochemically but not cytoarchitectonically and speculated that the subdivisions may have functional relevance. Collectively, functional and anatomical data in humans suggest that area 1 may be comprised of multiple subregions, of which 2 appear to be dedicated to processing input from the fingers.

In addition to findings in humans, several studies in awake monkeys have identified multiple, spatially distinct representations of the digits within area 1. In the macaque, vibrotactile and brushing stimulation of digit 2 evoked 2-deoxyglucose uptake in 2 discrete patches that, by visual inspection are separated by ∼2 mm in the inferior–superior plane within area 1 (Juliano et al. 1981). Electrophysiology studies in awake macaques demonstrate multidigit receptive fields within area 1 located proximal to the 3b border (Iwamura et al. 1980; McKenna et al. 1982) and single-digit receptive fields at more posterior penetrations (McKenna et al. 1982). In the anesthetized squirrel monkey, optical imaging demonstrates activation zones ∼1 mm beyond the topographically appropriate digit location (Friedman et al. 2004), and also support spatially discrete representations for “pressure,” “flutter,” and “vibration.” Using similar methods in anesthetized macaques, 2 discrete foci within area 1 were reported; digit somatotopy was observed in 1 focus and the second area, referred to as “the common patch” was activated by light tactile stimuli to all digits, the hand and even the wrist and forearm (Shoham and Grinvald 2001). Subsequent electrophysiology confirmed both findings and demonstrated multidigit receptive fields within the “common patch” area (Shoham and Grinvald 2001). Similar to the available data in humans, the aforementioned studies in monkeys suggest the existence of multiple representations of the hand in area 1.

How do the current findings in somatosensory cortex compare with the representation of finger movements in the primary motor cortex of humans? Unlike the clear somatotopy in area 3b, single-digit movements in M1 demonstrate distributed and overlapping activations that do not exhibit an orderly somatotopic arrangement when direct fMRI mapping techniques are applied (Dechent and Frahm 2003). However, differential mapping reveals a topographic ordering of all digits with ∼12–17 mm between D1 and D5 (Dechent and Frahm 2003), similar to the distance observed in somatosensory areas 3b and 1s. Further, digit representation in area 1s appears to resemble that reported in M1 given the observation of somatotopy with nonresolvable adjacent digit pairs (with the exception of D1 and D2) and the presence of 2 activation foci in support of a distributed representation of digits. It appears from the writing of Penfield and Rasmusson (1950, p. 56) that they too inferred similarities between area 1 and M1 when they commented: “Movement of hand with fingers, like sensation in hand and fingers, seems to have a separate representation from movement and sensation of fingers alone.”

The orderly representation of the body surface is a well-studied organizing feature characteristic of the somatosensory cortex in primates. The finding of somatotopic representation in human area 1 parallels the digit-level organization observed in monkeys and creates an inferential link to understanding the neural circuitry that underpins human sensation. Cross-species dissimilarities may reflect evolutionary distinctions, or our technical limitations using noninvasive mapping in humans. Further investigations will probe the possibility of modality-specific organization within the newly identified focus in area 1 and also area 2.

Funding

Canadian Institutes of Health Research (CIHR); Dystonia Medical Research Foundation; and CIHR fellowship to A.J.N.

We thank Frank Vidic for computing support and Carolyn Gunraj for subject assistance. Conflict of Interest: None declared.

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