Functional Overlap of Finger Representations in Human SI and SII Cortices

Cristina Simões,1 Markus Mertens,1,3 Nina Forss,1 Veikko Jousmäki,1 Bernd Lütkenhöner,1,3 and Riitta Hari1,2

 1Brain Research Unit, Low Temperature Laboratory, Helsinki University of Technology, FIN-02015 HUT Espoo;  2Department of Clinical Neurophysiology, Helsinki University, Central Hospital, FIN-00290 Helsinki, Finland; and  3Institute of Experimental Audiology, University of Münster, D-48129 Munster, Germany


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Simões, Cristina, Markus Mertens, Nina Forss, Veikko Jousmäki, Bernd Lütkenhöner, and Riitta Hari. Functional Overlap of Finger Representations in Human SI and SII Cortices. J. Neurophysiol. 86: 1661-1665, 2001. We aimed to find out to what extent functional representations of different fingers of the two hands overlap at the human primary and secondary somatosensory cortices SI and SII. Somatosensory evoked fields (SEFs) were recorded with a 306-channel neuromagnetometer from 8 subjects. Tactile stimuli, produced by diaphragms driven by compressed air, were delivered to the fingertips in three different conditions. First, the right index finger was stimulated once every 2 s. Then two other stimuli were interspersed, in different sessions, to right- or left-hand fingers (thumb, middle finger, or ring finger) between the successive right index finger stimuli. Strengths of the responses to right index finger stimuli were evaluated in each condition. Responses to right index finger stimuli were modeled by three current dipoles, located at the contralateral SI and the SII cortices of both hemispheres. The earliest SI responses, peaking around 65 ms, were suppressed by 18% (P < 0.05) when the intervening stimuli were presented to the same hand; intervening stimuli to the other hand had no effect. The SII responses were bilaterally suppressed by intervening stimuli presented to either hand: in the left SII, the suppression was 39 and 42% (P < 0.01) and in the right SII 67 and 72% (P < 0.001) during left- and right-sided intervening stimuli, respectively. Left- and right-sided intervening stimuli affected similarly the SII responses and had no effect on the response latencies. The results indicate a strong and symmetric overlap of finger representations for both hands in the human SII cortices, and a weaker functional overlap for fingers of the same hand in the SI cortex.


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INTRODUCTION
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Tactile input from the periphery activates in humans several cortical areas, starting with responses in the contralateral primary somatosensory cortex SI. Later prominent activity is observed bilaterally in the upper banks of the Sylvian fissures, in regions corresponding to the second somatosensory cortex SII.

In the SI cortex, Brodmann's area 3b has a clear somatotopical organization, whereas the more posterior areas 1 and 2 display stronger convergence of inputs (Allison et al. 1989). Responses to stimulation of different fingers (Forss et al. 1995; Hsieh et al. 1995; Ishibashi et al. 2000) and hand nerves (Biermann et al. 1998; Huttunen et al. 1992) have suggested some functional overlap in the human SI cortices.

The SII areas have extensively overlapping and bilateral receptive fields (Burton 1986) and show less spatial differentiation than SI does (Hari et al. 1990). Previous magnetoencephalographic (MEG) studies have shown that the human SII cortex responds to both contra- and ipsilateral stimuli (Hari et al. 1983; Kakigi 1994). As bilateral integration of tactile input from the two hands seems to be characteristic to the human SII cortex (Shimojo et al. 1996; Simões and Hari 1999; Wegner et al. 2000), we aimed to quantify to which extent representations of different fingers of the two hands overlap in the SI and SII cortices. We presented tactile stimuli to the tip of the right index finger and evaluated how intervening stimuli presented to the other fingers of the same or of the other hand affect the SI and SII activations.

A preliminary version of this paper has been reported in abstract form (Simões et al. 2000).


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Subjects, stimuli, and experimental conditions

Somatosensory evoked fields (SEFs) were recorded from eight healthy right-handed subjects (2 females, 6 males; ages 26-38 yr, mean 36). During the recording, the subject was sitting comfortably with the head supported against the inner vault of the magnetometer. Tactile stimuli (166 ms in duration) were delivered to the palmar skin of the fingers about 1.5 cm from the fingertips with balloon diaphragms driven by compressed air (Mertens and Lütkenhöner 2000). Air pressure was adjusted to produce clear tactile sensation and was the same for all subjects (Fig. 1, left).



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Fig. 1. Left: arrangement of tactile finger stimulators. During the experiment the subject was sitting beneath the neuromagnetometer, and the fingertips were stimulated with pressure pulses. Right: illustration of the temporal structure of the 3 different stimulation sequences.

The subjects were studied during three different conditions. First, stimuli were delivered to the right index finger (R2) alone, with an interstimulus interval of 2 s. In the other two conditions, two stimuli were interspersed among R2 stimuli, and presented to the thumb, middle, or ring finger tips of the left or right hand (L1, L3, L4, and R1, R3, R4, respectively; Fig. 1, right). The order of conditions was randomized across subjects. Subjects were instructed to ignore the stimuli.

Recording

This study received prior approval by the Ethical Committee of the Helsinki Uusimaa Hospital District, and a written informed consent was obtained from all subjects. Somatosensory evoked fields were recorded with a 306-channel helmet-shaped neuromagnetometer (Vectorview, Neuromag, Helsinki, Finland) that contains 102 identical triple sensors. Each sensor element comprises two orthogonal planar gradiometers, which detect the maximum signal just above a local source area, and one magnetometer. For overviews of MEG data collection and analysis, see, e.g., Hämäläinen et al. (1993) and Hari (1999). The exact position of the head with respect to the sensors was found by measuring magnetic signals produced by currents led into four indicator coils placed at known sites on the scalp. The locations of the coils with respect to landmarks on the head were determined with a three-dimensional (3-D) digitizer to allow alignment of the MEG and magnetic resonance (MR) image coordinate systems. The signals were recorded with a passband of 0.03-200 Hz and digitized at 600 Hz. The analysis period of 700 ms included a prestimulus baseline of 200 ms, and about 120 epochs were averaged for each condition. Epochs coinciding with signals exceeding 150 µV in the simultaneously recorded vertical electrooculogram (EOG) were automatically rejected from the analysis.

The MR images of the subjects' brains were acquired with a 1.5 tesla system (MAGNETOM, Siemens, Erlangen, Germany).

Data analysis

For source localization, based on the signals recorded by the 204 gradiometers, the head was assumed to be a sphere, the dimensions of which were found on the basis of individual magnetic resonance images.

To identify cerebral sources of evoked responses to R2 stimuli presented alone, the signals were divided into several time periods, during each of which one equivalent current dipole (ECD), best describing the most dominant source, was first found by a least-squares search using a subset of channels over the maximum response. These calculations resulted in the 3-D location, orientation, and strength of the ECD in a spherical conductor model.

The final source model consisted of three dipoles, one in the left SI cortex and one in the SII cortex of each hemisphere. In this model, the dipole locations and orientations were kept fixed, but the strengths were allowed to change as a function of time to provide the best fit to the data. The dipole model, found for R2 stimuli presented alone, was applied also to the two other conditions. The peak latencies and amplitudes of the SI and SII responses were measured from the source strength waveforms.

Similar source analysis has been applied in several of our previous SEF studies, and it has been shown to give concordant results with, e.g., minimum norm estimate approaches (cf. Forss et al. 2001).

Statistical tests

Statistical significances of differences between the three conditions were tested with Student's paired, two-tailed t-test.


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Figure 2 illustrates the distribution of SEFs of subject 4 to R2 stimuli presented alone. The first response (see inset 1) peaks in the left hemisphere 52 ms after the stimulus onset. Longer-latency responses peak at 87 ms in the left and at 96 ms in the right temporoparietal regions (insets 2 and 3, respectively).



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Fig. 2. Distribution of somatosensory evoked fields of subject 4 to right index finger stimuli. The head, viewed from the top, is flattened onto the plane. The top and bottom curves in each location represent the longitudinal and latitudinal gradients of the radial component of the magnetic field, respectively. The curves on the right show enlarged responses from the 3 encircled channels.

Figure 3 (left) shows the source areas for the same subject, superimposed on the MR images. The earliest activation arises in the posterior wall of the central fissure, in the hand area of the SI cortex. The longer-latency responses originate bilaterally in the upper banks of the Sylvian fissures, agreeing with SII locations.



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Fig. 3. Left: source locations for subject 4 superimposed on the magnetic resonance images. Right: source strengths as a function of time in a 3-dipole model, during all conditions. SIc, contralateral SI cortex; SIIc, contralateral SII cortex; SIIi, ipsilateral SII cortex.

Figure 3 (right) shows the SI and SII source waveforms for subject 4. Both right- and left-sided intervening stimuli decreased the 52-ms SI peak, but this effect was stronger when intervening stimuli were presented to the right-hand fingers. Regardless of the side of the intervening stimuli, the SII responses decreased bilaterally.

R2 stimuli presented alone activated in all subjects the contralateral SI cortex, with peak latencies of 67 ± 6 ms (mean ± SE, range 50-85 ms). The following bilateral activation SII, also observed in all subjects, showed a clear contralateral dominance. The contralateral (left) SII responses peaked at 100 ± 5 ms and the ipsilateral responses on average 12 ms (P < 0.05) later. The intervening stimuli did not change the peak latencies of SI and SII responses (Table 1). In three subjects, activation was also observed in the posterior parietal cortex at 111 ± 20 ms, as described earlier (Forss et al. 1994).


                              
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Table 1. Peak latencies and dipole moments of the contralateral SI cortex and of the contra- and ipsilateral SII cortices in all conditions

Figure 4 shows the mean (+SE) relative changes of the SI and SII source strengths during intervening stimulation. Right-sided interference suppressed the SI responses to R2 stimuli by 18 ± 5% (P < 0.05); for left-sided stimuli the suppression was not statistically significant. The SII responses were suppressed by intervening stimuli presented to either hand. Right-hand stimuli suppressed the responses by 42 ± 12% (P < 0.01) in the left SII and by 72 ± 8% (P < 0.001) in the right SII. For left-hand interference, the corresponding suppressions were 39 ± 12% (P < 0.05) in the left SII and 67 ± 6% (P < 0.001) in the right SII. The effects of left- versus right-sided interference on SII responses did not differ. The suppression was 30 ± 14% (P < 0.05) stronger in the ipsilateral (right) than in the contralateral SII, both for right- and left-sided intervening stimuli; this asymmetric effect was seen in five of eight subjects.



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Fig. 4. Mean relative changes of the source strengths from the "R2 alone" condition. The bars indicate SEs (8 subjects). The white and gray bars indicate the changes during left- and right-hand intervening stimuli, respectively.


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The present study is the first attempt to investigate interaction between purely tactile inputs from different fingers in the human SII cortex. Similar stimuli have recently been applied to study functions of the human SI cortex (Mertens and Lütkenhöner 2000). Our results showed clearly different interaction in the SI and SII cortices: whereas the SI responses were decreased only when the interspersed stimuli were presented to the same hand, the SII responses were similarly and strongly suppressed by intervening stimuli presented to either hand.

Previous studies using electric stimuli have indicated in the SI cortex a strong convergence from different nerves of the same hand at interstimulus intervals of 20-100 ms; for example, the 20-ms response to median nerve stimuli was similarly suppressed (maximally by about 70%) by preceding stimuli of both median and ulnar nerves (Huttunen et al. 1992). On the other hand, tactile stimulation at much longer interstimulus intervals revealed no indication of such a convergence in SI: the amplitudes of responses to pressure pulses applied to the right index finger at mean intervals of 2-4 s were basically unaffected by intervening stimuli presented to digits 3-5 (Mertens and Lütkenhöner 2000).

Our first SI response peaked around 65 ms, probably because of the rather slow (50 ms) stimulus risetime. This response is likely to be generated in the cytoarchitectonic area 3b, similarly as the 20-ms response to electric median nerve stimuli. Our data thus imply functional overlap between fingers of the same hand in area 3b of the SI cortex, even when the stimuli are separated by about 670 ms. Because the intervening stimuli were presented in random order, we cannot make any conclusions about the strengths of interactions between representations of different fingers. However, comparison of responses to simultaneous stimulation of two fingers of the same hand (Biermann et al. 1998) suggested that the interaction is the stronger the closer the fingers are to each other. Tactile stimuli applied to the other hand did not significantly suppress the SI responses. This is in line with anatomical data indicating only very sparse callosal connections between hand areas of SI cortices of the two hemispheres.

The representation areas of the fingers of one hand cover a strip of about 15-20 mm in the human SI cortex (Hari et al. 1993) and thus the representations of the intervening fingers in our study probably differed from that of the index finger, receiving the "standard" stimuli, by 3-6 mm, which is still in the range of horizontal cortical fibers. Therefore the observed interaction could be explained by inhibitory surround of the index finger activation. The present data indicate that this inhibitory surround is strong still 670 ms after purely tactile stimuli, in agreement with the recovery cycle of responses under study (Mertens and Lütkenhöner 2000). In line with our findings, cortical reorganization after removal of one finger suggests that the SI representations of adjacent fingers are not isolated but overlap (Manger et al. 1996).

Whereas the SI responses were suppressed maximally by about one-fifth during the intervening stimuli, the responses of the SII cortices were suppressed significantly more: in the contralateral (left) hemisphere by about 40% and in the ipsilateral hemisphere by even 70%. The suppression was strikingly similar for intervening stimuli presented to either hand, in line with the bilaterality of receptive fields in the SII cortex. In monkeys, the proportion of SII neurons with bilateral receptive fields varies from 25% (Burton 1986) to 90% (Whitsel et al. 1969), in part depending on the exact location of the recording. Our findings suggest that human SII neurons with poststimulus suppression overlasting 600-700 ms have mainly bilateral receptive fields.

Interaction between inputs from the two hands in the human SII cortex has been previously documented with electric median nerve stimuli separated by 300 ms (Simões and Hari 1999) and 1.5 s (Wegner et al. 2000). The SII cortex receives direct input from the contralateral, and probably also from the ipsilateral body parts (Forss et al. 1999). It also receives input from the ipsilateral SI cortex and via callosal connections from the SII area of the other hemisphere (Jones and Powell 1969). Altogether these results indicate that the SII cortex is in a good position to integrate sensory input from both body halves during bimanual manipulation and exploration.


    ACKNOWLEDGMENTS

This work was supported by the Academy of Finland, Foundation for Science and Technology PRAXIS XXI BD-19517/99 (Portugal), Deutsche Forschungsgemeinschaft (Grant Lu 342/5-1), and European Union's Large Scale Facility Neuro-BIRCH at the Brain Research Unit, Low Temperature Laboratory of the Helsinki University of Technology.


    FOOTNOTES

Address for reprint requests: C. Simões, Brain Research Unit, Low Temperature Laboratory, Helsinki University of Technology, PO Box 2200, FIN-02015 HUT Espoo, Finland (E-mail: cristina{at}neuro.hut.fi).

Received 12 March 2001; accepted in final form 14 June 2001.


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0022-3077/01 $5.00 Copyright © 2001 The American Physiological Society