Content uploaded by Srikantan S Nagarajan
Author content
All content in this area was uploaded by Srikantan S Nagarajan
Content may be subject to copyright.
Available via license: CC BY 2.0
Content may be subject to copyright.
BioMed Central
Page 1 of 14
(page number not for citation purposes)
BMC Neuroscience
Open Access
Research article
Spatiotemporal integration of tactile information in human
somatosensory cortex
Zhao Zhu
1,2
, Elizabeth A Disbrow
1,2,3
, Johanna M Zumer
1
,
David J McGonigle
1,4
and Srikantan S Nagarajan*
1
Address:
1
Biomagnetic Imaging Laboratory, Department of Radiology, University of California, San Francisco, San Francisco, CA, 94143-0628,
USA ,
2
Center for Neuroscience, University of California, Davis, Davis, CA, 95616, USA ,
3
Department of Neurology, University of California,
Davis, Davis, CA, 95616, USA and
4
Center for Functional Imaging Studies, Western General Hospital, University of Edinburgh, Edinburgh,
Scotland, EH4 2XU, UK
Email: Zhao Zhu - zhaozhu@radiology.ucsf.edu; Elizabeth A Disbrow - liz.disbrow@radiology.ucsf.edu;
Johanna M Zumer - johannaz@radiology.ucsf.edu; David J McGonigle - dmcgonig@staffmail.ed.ac.uk;
Srikantan S Nagarajan* - sri@radiology.ucsf.edu
* Corresponding author
Abstract
Background: Our goal was to examine the spatiotemporal integration of tactile information in
the hand representation of human primary somatosensory cortex (anterior parietal somatosensory
areas 3b and 1), secondary somatosensory cortex (S2), and the parietal ventral area (PV), using
high-resolution whole-head magnetoencephalography (MEG). To examine representational overlap
and adaptation in bilateral somatosensory cortices, we used an oddball paradigm to characterize
the representation of the index finger (D2; deviant stimulus) as a function of the location of the
standard stimulus in both right- and left-handed subjects.
Results: We found that responses to deviant stimuli presented in the context of standard stimuli
with an interstimulus interval (ISI) of 0.33s were significantly and bilaterally attenuated compared
to deviant stimulation alone in S2/PV, but not in anterior parietal cortex. This attenuation was
dependent upon the distance between the deviant and standard stimuli: greater attenuation was
found when the standard was immediately adjacent to the deviant (D3 and D2 respectively), with
attenuation decreasing for non-adjacent fingers (D4 and opposite D2). We also found that
cutaneous mechanical stimulation consistently elicited not only a strong early contralateral cortical
response but also a weak ipsilateral response in anterior parietal cortex. This ipsilateral response
appeared an average of 10.7 ± 6.1 ms later than the early contralateral response. In addition, no
hemispheric differences either in response amplitude, response latencies or oddball responses
were found, independent of handedness.
Conclusion: Our findings are consistent with the large receptive fields and long neuronal recovery
cycles that have been described in S2/PV, and suggest that this expression of spatiotemporal
integration underlies the complex functions associated with this region. The early ipsilateral
response suggests that anterior parietal fields also receive tactile input from the ipsilateral hand.
The lack of a hemispheric difference in responses to digit stimulation supports a lack of any
functional asymmetry in human somatosensory cortex.
Published: 14 March 2007
BMC Neuroscience 2007, 8:21 doi:10.1186/1471-2202-8-21
Received: 23 September 2006
Accepted: 14 March 2007
This article is available from: http://www.biomedcentral.com/1471-2202/8/21
© 2007 Zhu et al; licensee BioMed Central Ltd.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0
),
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
BMC Neuroscience 2007, 8:21 http://www.biomedcentral.com/1471-2202/8/21
Page 2 of 14
(page number not for citation purposes)
Background
The spatiotemporal integration of tactile inputs from dif-
ferent skin regions and across body parts is an important
function of human somatosensory cortex. For example,
the integration of inputs across the digits is vital for the
successful manual manipulation and identification of
objects. However, the mechanism of this integration is
not well understood. Good candidates for the perform-
ance of this function are the second somatosensory area,
S2, and the parietal ventral area, PV. These two fields are
mirror symmetric representations of the body's surface [1-
4], joined at the representation of the hand. Because it is
difficult to distinguish between the hand representations
of S2 and PV using functional imaging techniques we refer
to this region as S2/PV.
Electrophysiological recording studies in monkeys indi-
cate that neuronal receptive fields in S2 [2,5,6] and PV
[2,4,7] are large, encompassing multiple digits or even the
entire hand. Further, these receptive fields are often bilat-
eral, including, for example, both the contra- and ipsilat-
eral hand. Studies of neuroanatomical connections also
show that, beside the local homotopic connections in the
ipsilateral hemisphere, both S2 [1,7] and PV [1,4,7] have
dense bilateral connections.
There is also evidence from human imaging studies that
inputs from different skin regions interact in S2/PV. For
example, bilateral integration of inputs from the hands
takes place in human S2/PV [8-12]. In addition, the acti-
vation in human S2 evoked by stimulation of one finger
can be modulated by simultaneous [11] or non-simulta-
neous [8,9,12] stimulation of other fingers of the same
hand.
Another possibility is that integration of inputs from dif-
ferent skin regions takes place, at least to some extent, in
anterior parietal areas 3a, 3b, 1 and 2 [9,11-15]. Previous
MEG studies have confirmed that tactile stimulation to
the human finger evokes responses in both contralateral
anterior parietal fields as well as bilateral S2/PV [16,17].
Each finger has a distinguishable somatotopic representa-
tion in contralateral anterior parietal cortex [18,19]. How-
ever, there is some evidence that interaction among digit
representations may also occur in anterior parietal cortex.
For example, the strength of the early response to stimula-
tion of a single finger was attenuated by simultaneous
[11,14,15] or non-simultaneous stimulation of another
finger at short (<100 ms) ISIs [13]. Further, the magnitude
of spatial integration decreased with the distance of sepa-
ration of the digit representations in anterior parietal
fields [11,14]. There is also evidence from electrophysio-
logical recording [20] and optical imaging [21] studies in
monkeys that simultaneous stimuli from different skin
regions could be merged together into a single activation
zone in anterior parietal cortex.
However, in contrast to S2/PV, human MEG studies sug-
gest that responses in anterior parietal cortex to stimula-
tion of one hand are not affected by stimulation of the
opposite hand [10-12]. This finding is supported by neu-
roanatomical results in monkeys indicating that the hand
representation in 3b is largely acallosal [1,22-25]. Previ-
ous MEG work also suggests that the spatial integration of
inputs across the digits is much stronger in S2/PV than in
anterior parietal fields [9,11,12]. However, the extent of
spatial integration in S2/PV, and the difference in extent
and timing of integration between anterior parietal fields
and S2/PV has not been quantified. These differences may
represent different steps in the complex process of spatio-
temporal integration.
In this study, we measured somatosensory evoked fields
(SEFs) during non-simultaneous tactile stimulation of
digits of both hands with an oddball paradigm. We com-
pared the extent of spatial integration in the hand repre-
sentations in human S2/PV and anterior parietal fields,
and discuss the difference in the timing of integration in
these two areas.
Results
Contra- and ipsilateral responses to index finger
stimulation
1). Dipole orientation and localization
In all subjects, dipoles were fit for both the early (30–70
ms) and late (70–130 ms) response windows. Figure 1
contains the actual contour plots of MEG sensor data and
the plots of the averaged magnetic fields measured using
275 axial gradiometers from a single right-handed subject
showing responses to index finger stimulation (average of
'deviants' alone at low rate, ISI = 2s). The left and right col-
umns show responses to right index finger (RD2) and left
index finger (LD2) stimulation, respectively. Identified
dipole sources of responses in the right hemisphere were
superimposed on this subject's MRI and are shown in Fig-
ure 2.
Interestingly, bilateral activation appeared during both
early and late time periods in this subject for both LD2
and RD2 stimulation, though the early responses were of
larger amplitude and shorter latency in the contralateral
(e.g. the first peak at 45 ms in Figure 1e) versus the ipsilat-
eral (e.g. the first peak at 51 ms in Figure 1f) hemisphere.
The dipole direction and location of the ipsilateral (left
hemisphere) response to LD2 stimulation were similar to
those of the contralateral (left hemisphere) response to
RD2 stimulation and likewise for the right hemisphere
responses. The dipole directions tended to be mirror
images in the two hemispheres. Dipole analysis and co-
BMC Neuroscience 2007, 8:21 http://www.biomedcentral.com/1471-2202/8/21
Page 3 of 14
(page number not for citation purposes)
registration of the MEG localization information with the
MRI scans verified that the anterior parietal area (the pos-
terior wall of the central sulcus) was the primary contrib-
utor to both contralateral and ipsilateral early (30–70 ms)
responses and that the S2 region (the upper bank of the
Sylvian fissure) was the primary contributor to the late
(70–130 ms) responses in this subject (Figure 2).
The average current dipole positions were specified in
Talairach coordinates (x, y, z in mm): the early contralat-
Time courses of MEG maps and waveformsFigure 1
Time courses of MEG maps and waveforms. Averaged responses to index finger tactile stimulation at low rate (stimula-
tion condition 1 in Figure 6; the strongest response was observed under this condition) were recorded from a right-handed
subject. The left and right columns show responses to RD2 and LD2 stimulation, respectively. The two top (a and d) panels
represent the series of contour plots of sensor data showing the time course of the averaged evoked magnetic fields. Each plot
shows the sensor data interpolated between the 275 sensors at different latencies. The nasion is pointing up, the right ear is to
the right, and the left ear is to the left (top view). Panels b, c, e and f show averaged evoked magnetic field responses; each line
depicts an average of the data from a single sensor over all trials for one condition. Panels b and e show response waveforms
recorded from half of all sensors over the hemisphere contralateral to the stimulated index finger, c and f from the hemisphere
ipsilateral to the stimulated index finger.
BMC Neuroscience 2007, 8:21 http://www.biomedcentral.com/1471-2202/8/21
Page 4 of 14
(page number not for citation purposes)
eral response dipoles in left and right hemispheres were (-
49.2 ± 1.6, -19.2 ± 2.5, 45.8 ± 2.4) and (48.0 ± 1.4, -14.5
± 1.4, 51.3 ± 3.7); the late contralateral response dipoles
in left and right hemispheres were (-61.9 ± 3.7, -16.6 ±
3.4, 6.9 ± 3.8) and (56.2 ± 2.4, -5.4 ± 4.7, 13.9 ± 4.8),
respectively. These localizations in Talairach space were
consistent with the locations of anterior parietal fields and
S2/PV in both hemispheres.
Early ipsilateral responses for LD2 stimulation were found
in 12/15 right- and 2/6 left-handed subjects, while 7/15
right- and 2/6 left-handed subjects showed early ipsilat-
eral responses to stimulation of RD2. Figure 3 shows two
more examples of early ipsilateral responses (one right-
handed and one left-handed). The source of early ipsilat-
eral responses was identified in anterior parietal fields.
Late ipsilateral responses were recorded from all 21 sub-
jects. Like the late contralateral responses, the late ipsilat-
eral responses also originated from the upper banks of the
Sylvian fissure, in the S2 region.
2). Latency
The peak latencies of responses from a single subject (con-
tralateral early and late responses, ipsilateral early and late
responses) are shown in Figure 1. The early contralateral
responses from both hemispheres of the same subject
peaked at 45 ms, while late contralateral responses peaked
at about 100 ms (Figure 1a, b and 1d, e). Early and late
ipsilateral responses in the right hemisphere peaked at 60
and 120 ms (Figure 1a and 1c). The early ipsilateral
responses in the left hemisphere peaked at 51 ms. Later
responses, which looked more complex with multiple
peaks, peaked around 110 ms (Figure 1d and 1f). Thus,
both early and late ipsilateral response peaks appeared
Source localizations of responses to index finger stimulation aloneFigure 2
Source localizations of responses to index finger stimulation alone. Identified dipole sources of responses in the right
hemisphere shown in Figure 1 are superimposed on this subject's MRI. The left horizontal (a) and sagittal (b) slices show the
locations of early contralateral response (green dot in right anterior parietal field) to LD2 stimulation and early ipsilateral
response (red dot) to RD2 stimulation. The coronal (c) and sagittal (d) slices in the right column show the locations of the late
contralateral response (yellow dot in right S2) to LD2 stimulation and late ipsilateral response (cyan dot) to RD2 stimulation.
The tails of those dots indicate dipoles' strength and direction.
BMC Neuroscience 2007, 8:21 http://www.biomedcentral.com/1471-2202/8/21
Page 5 of 14
(page number not for citation purposes)
later than contralateral peaks in both hemispheres in this
subject.
The average early and late contralateral response latencies
for all subjects (right- and left-handed) were not signifi-
cantly different across hemispheres (p > 0.05). The ipsilat-
eral early (56.2 ± 6.6 ms) and late (116.6 ± 13.1 ms)
responses appeared significantly later than contralateral
early (46.8 ± 6.9 ms) and late (108.8 ± 12.5 ms) responses
in all subjects. The mean delay of the early ipsilateral
responses relative to the contralateral responses was 10.7
± 6.1 ms (range: 3.5–24 ms), while the delay of the late
ipsilateral responses relative to the contralateral responses
was 12.7 ± 13.1 ms (range 3.0–30.8 ms). The mean differ-
ence between delays for the early versus late responses was
not significant (p > 0.05).
3). Amplitude
The subject's data from Figure 1 clearly show the early
ipsilateral responses above the noise level (Figure 1c and
1f). The amplitudes of this subject's early ipsilateral
responses were 47.3 and 35.8 fT (RMS), while the noise
levels were 13.6 and 9.8 fT (RMS), in the left and right
hemispheres, respectively. The average amplitude of the
early ipsilateral response (37.9 ± 2.0 fT) across all subjects
was significantly higher (p < 0.01) than the average noise
level (14.5 ± 0.9 fT) based on the pre-stimulation period
of 50 ms.
The average amplitude of early and late responses for all
subjects did not show a significant difference between
hemispheres (p > 0.05), nor was there a significant differ-
ence in amplitude of response for right- versus left-hand-
ers (p > 0.05). As the strength of early and late responses
did not show a significant difference between hemi-
spheres, the responses to left and right hand stimulation
were combined for further analysis.
The mean amplitude of the early response was signifi-
cantly smaller (p < 0.01) for the early ipsilateral response
Two ipsilateral early responses examplesFigure 3
Two ipsilateral early responses examples. The top two averaged sensor data plots are from a right-handed subject, the
bottom two are from a left-handed subject. Figures in the left column show the two subjects' sensor plots at the early ipsilat-
eral (left hemisphere) response peak moment under the LD2 stimulation condition. The peak ipsilateral (left hemisphere)
response is still weaker than the contralateral (right hemisphere) response, though the right hemisphere response is not at its
peak at this time. Figures in the right column show similar results for RD2 stimulation. Both LD2 and RD2 stimulation elicited
bilateral early responses in these two subjects.
BMC Neuroscience 2007, 8:21 http://www.biomedcentral.com/1471-2202/8/21
Page 6 of 14
(page number not for citation purposes)
(37.9 ± 2.0 fT) than for the early contralateral response
(66.9 ± 3.3 fT). Similarly, the late ipsilateral response
(50.4 ± 4.8 fT) was significantly weaker (p < 0.01) than
the late contralateral response (69.3 ± 5.6 fT). Further, the
mean amplitude of the early contralateral response (66.9
± 3.3 fT) was not significantly different from the late con-
tralateral response (69.3 ± 5.6 fT; p > 0.05), while the late
ipsilateral response (50.4 ± 4.8 fT) was significantly
stronger than the early ipsilateral response (37.9 ± 2.0 fT;
p < 0.01; see Figure 4).
Spatial integration between digit representations
1). Latency
Figure 5 is an example of the spatial interaction from a
typical right-handed subject. This figure shows the aver-
aged magnetic field responses recorded from all 275 sen-
sors under the different stimulus conditions. Each line is
the average over all trials for a given sensor. The left col-
umn in Figure 5 shows contralateral (right hemisphere)
sensor waveforms for LD2 stimulation, and the right col-
umn shows the contralateral (left hemisphere) sensor
waveforms for RD2 stimulation. The latencies of both
early and late responses did not change under different
stimulation conditions.
2). Amplitude
In an example subject, low rate index finger stimulation
(mean ISI: 2s) clearly elicited both early and later
responses (Figure 5a and 5f). The response amplitude was
markedly decreased for high rate stimulation (ISI: 0.33 s),
and the late response (S2/PV) almost disappeared in both
hemispheres (Figure 5b and 5g). The intervened standard
stimuli (D3, D4 and opposite D2) suppressed the late
response for D2 (deviant) stimulation in both hemi-
spheres. There appeared to be the greatest attenuation for
the same (D2) digit high rate stimulation compared to
alternate standard digit (D3, D4 and opposite D2) stimu-
lation, and greater attenuation for adjacent (D3) com-
pared to non-adjacent (D4 and opposite D2) digit
stimulation (Figure 5b–e and 5g–j). The standard stimuli
reduced the amplitude of the early response for D2 (devi-
ant) stimulation in some conditions for this subject (Fig-
ure 5c and 5j).
Grand averaged sensor amplitude (RMS; contralateral
hemisphere only) and dipole moment (nAm) response
values to deviant stimuli are displayed in Figure 4. Both
sensor and moment values of early responses were statis-
tically significantly smaller for high rate index finger stim-
ulation (ISI: 0.33s) compared to low rate index finger
stimulation (mean ISI: 2s). Both contralateral and ipsilat-
eral early amplitude of responses to single finger stimula-
tion (D2) were not significantly affected by stimulation of
the other fingers (D3, D4 and opposite D2).
As with the early responses, sensor and moment values of
the late responses were statistically significantly smaller
for high rate index finger stimulation (ISI: 0.33s) com-
pared to low rate index finger stimulation (mean ISI: 2s).
The late response decreased more than the early response
regardless of handedness (p < 0.01; also see Figure 5).
Further, the intervened standard stimuli (D3, D4, and
opposite D2) significantly reduced the late contralateral
and ipsilateral responses to deviant (D2) stimuli. In the
contralateral hemisphere this effect was greater for the
adjacent finger (D3) compared to the non-adjacent fin-
gers (D4 or opposite D2). The attenuation of the late con-
tralateral response was significantly greater for the same
finger high rate stimulation (D2 alone at high rate) com-
pared to non-adjacent finger (D4 or opposite D2) stimu-
lation. For the ipsilateral response, there were no
differences in amplitude reduction related to the location
of intervened standard stimulation. Only opposite D2
stimulation differed from high rate D2 stimulation in the
late ipsilateral response. The suppressive effect of opposite
D2 stimulation was significantly stronger for the contral-
ateral than the ipsilateral late response (Figure 4).
Discussion
In summary, we examined the spatiotemporal integration
across digit representations within anterior parietal soma-
tosensory areas and S2/PV, as well as interhemispheric
integration, using non-simultaneous tactile stimulation.
We have shown 1) spatial integration of responses in S2/
PV, with a decrease in interaction with the increase in sep-
aration of digit representations; 2) greater temporal inte-
gration of inputs within one digit representation in S2/PV
versus anterior parietal fields; 3) both contra- and ipsilat-
eral early responses in anterior parietal fields to cutaneous
mechanical stimulation. The early ipsilateral response has
a longer latency and lower amplitude than the early con-
tralateral response; and 4) processing of cutaneous inputs
is symmetrical across hemispheres. What follows is a dis-
cussion of these findings in light of previous work from
human and non-human primates.
Spatiotemporal integration between digit representations
in S2/PV
The distance-dependence of spatial integration between
digit representations in the S2/PV area was examined in
this study. We found that the amplitude of the contralat-
eral late responses to deviant stimuli (D2) decreased
when standard stimuli (D3, D4 and opposite D2) were
intervened. Like the distance-dependence of spatial inte-
gration in anterior parietal areas [11,14], the attenuation
decreased with the increasing distance of separation
between receptive fields, toward greater attenuation for
adjacent fingers (D3) compared to non-adjacent fingers
(D4 and opposite D2).
BMC Neuroscience 2007, 8:21 http://www.biomedcentral.com/1471-2202/8/21
Page 7 of 14
(page number not for citation purposes)
Spatial integrationFigure 4
Spatial integration. Grand average of the peak sensor amplitude (a: RMS) and dipole moment (b: Q) values for early (ante-
rior parietal area) and late (S2/PV) responses under different experimental conditions are compared. Asterisks indicate that the
responses are significantly (*: p < 0.05; **: p < 0.01) different from others that are linked to it by the lines, using the Bonferroni
post-hoc test. c, i, E and L stand for contralateral, ipsilateral, early and later response, respectively. S1 and S2 stand for anterior
parietal areas and S2/PV respectively. D2 Low: D2 stimulation alone at low rate (condition 1 in Figure 6; mean ISI: 2s); D2 High:
D2 stimulation alone at high rate (condition 2 in Figure 6; ISI: 0.33s); D2d (D3s): D2 deviant plus D3 standard stimuli (condition
3 in Figure 6; ISI: 0.33s); D2d (D4s): D2 deviant plus D4 standard stimuli (condition 4 in Figure 6; ISI: 0.33s); D2d (oD2s): D2
deviant plus opposite D2 standard stimuli (condition 5 in Figure 6; ISI: 0.33s).
BMC Neuroscience 2007, 8:21 http://www.biomedcentral.com/1471-2202/8/21
Page 8 of 14
(page number not for citation purposes)
An example of spatial integration obtained from a right-handed subjectFigure 5
An example of spatial integration obtained from a right-handed subject. The waveforms show the time courses of
the averaged magnetic field responses recorded from 275 sensors under the different conditions. The left and right columns
show contralateral sensor response waveforms for LD2 and RD2 stimulation, respectively. a and f: D2 stimulation alone at low
rate (condition 1 in Figure 6; mean ISI: 2s); b and g: D2 stimulation alone at high rate (condition 2 in Figure 6; ISI: 0.33s); c and
h: D2 deviant plus D3 standard stimulation (condition 3 in Figure 6; ISI: 0.33s); d and i: D2 deviant plus D4 standard stimulation
(condition 4 in Figure 6; ISI: 0.33s); e and j: D2 deviant plus opposite D2 standard stimulation (condition 5 in Figure 6; ISI:
0.33s).
BMC Neuroscience 2007, 8:21 http://www.biomedcentral.com/1471-2202/8/21
Page 9 of 14
(page number not for citation purposes)
In agreement with previous MEG work on digit response
interaction in S2/PV [8,9,11,12,26], our data show that
the standard stimuli significantly attenuate responses in
bilateral S2/PV to deviant (D2) stimulation. The pattern
of spatial integration in S2/PV is consistent with the fact
that neurons in S2 and PV have large receptive fields, fre-
quently encompassing multiple digits [2,4-7,27], while
cells in anterior parietal areas do not [28,29].
We also found significant temporal integration in the S2/
PV region. The amplitude of the late response was smaller
for high rate versus low rate index finger stimulation, and
the late responses decreased more than the early responses
with high rate stimulation, as previous SEP [30] and SEF
[26,31-34] investigations have shown. This result is con-
sistent with previous studies revealing the shorter recovery
cycle or refractory period for neurons in anterior parietal
areas than in S2 [35,36].
Some non-human primate studies have suggested serial
information processing from anterior parietal areas to S2/
PV [37,38], with tactile inputs from anterior parietal fields
converging onto S2 [27,39]. However, other studies sug-
gest hierarchical equivalence of anterior parietal areas and
S2 for tactile processing in cats and new-world primates
[40-42]. To date, the debate about serial versus parallel
organization of somatosensory cortex in humans is unre-
solved. Both early [43] and late [44,45] concurrent activi-
ties in anterior parietal and lateral sulcal areas have been
reported in humans. In contrast, a recent MEG study
revealed that the onset latency of response following tran-
scutaneous electrical stimulation was longer in S2/PV
than in anterior parietal areas [46]. However, we cannot
rule out the contribution of activity in S2/PV to early
responses and anterior parietal areas to late responses. It
is possible that both serial and parallel processing play a
role in tactile perception.
Serial convergence may account for the spatial and tempo-
ral specialties in S2/PV. Unlike anterior parietal areas with
restricted and defined neural receptive fields, the large,
complex receptive fields within S2/PV may play an impor-
tant role in integrating tactile inputs over space and time.
For example, the digit representations in S2 and surround-
ing fields lack fine somatotopy, and some cells responded
better to proprioceptive rather than cutaneous stimuli
[27]. In addition, studies have found that 23% of cells in
the S2 region were orientation tuned, often across multi-
ple digit pads [27]. These receptive field properties, tuned
for relatively long-range spatial and temporal integration,
go some way towards explaining S2's purported involve-
ment in functions like tactile object exploration and iden-
tification [47-50], bimanual coordination [2,4,6,7], and
tactile learning and memory [49,50]. Consistent with this
idea is evidence in humans that damage to parietotempo-
ral cortices (including S2) causes impairment of tactile
object recognition in the absence of basic somesthetic dys-
function [51,52].
Spatiotemporal integration between digit representations
in anterior parietal somatosensory areas
We found that the amplitude of responses in anterior pari-
etal areas to deviant alone stimuli applied to a single digit
was significantly lower at high rate (the ISI is also 0.33s)
versus low rate (ISI: 2s) stimulation, as previous studies
[26,30-34] have shown. This decrease of amplitude result-
ing from increased rate of stimulation was much smaller
in anterior parietal areas than in S2/PV. However, the
average amplitude of early responses in anterior parietal
areas for deviant stimulation did not show a significant
decrease when the standard stimuli were interleaved
between deviants (ISI: 0.33s), though the amplitude
decrease was seen in some cases. Previous work using
non-simultaneous stimuli with long ISIs (1–4 s) also
showed similar results [26,53]. However, an interaction
between digit representations has been reported in ante-
rior parietal areas when using simultaneous [11,14,15] or
non-simultaneous stimuli with short (<100 ms) ISIs [13].
These findings are in line with the short recovery cycle
time constant (~110 ms) for neurons in anterior parietal
areas, which was estimated by fitting an exponential curve
to SEF intensities for responses to electrical stimulation of
the median nerve with different ISIs (100–500 ms) [36].
With a long ISI, the intervened standard inputs may arrive
out of the recovery period of neurons in anterior parietal
areas, with little effect on responses to deviant stimuli.
It is known that there is an inhibitory surround structure
of receptive fields in monkey area 3b [54-58]. A three-
component model has been proposed in which a lagged
inhibitory surround overlaps the excitatory center and its
one or more fixed inhibitory flankers. The fixed (as a spa-
tial filter) and lagged (as a temporal filter) surround
inhibitory components confer the spatial and temporal
selectivity of neurons in anterior parietal areas [58]. The
spatiotemporal property of inhibitory surround structure
of neural receptive fields may account for the restricted
neural receptive field and rapid recovery cycle in anterior
parietal areas observed in the present study.
Ipsilateral responses in anterior parietal areas
In the present investigation we clearly recorded early ipsi-
lateral responses with high goodness-of-fit to single finger
tactile stimulation (both right- and left-handers). Though
the amplitude of the ipsilateral response was very weak in
some cases, on average it was 2.5 times greater than the
noise level. An ipsilateral response from anterior parietal
field has also been observed in a small number of subjects
in several previous studies [59-63] using MEG or EEG to
measure responses to median nerve stimulations. A grow-
BMC Neuroscience 2007, 8:21 http://www.biomedcentral.com/1471-2202/8/21
Page 10 of 14
(page number not for citation purposes)
ing body of evidence from monkey studies [64,65] and
human fMRI studies [66,67] also report ipsilateral
responses in anterior parietal fields, suggesting that ante-
rior parietal fields receive tactile input from the ipsilateral
hand. Ipsilateral responses were relatively robust in our
study, likely due to the cutaneous mechanical stimulation
used in our experiment. Recent fMRI studies on both
monkeys and humans have shown that responses from
ipsilateral anterior parietal areas are more robust for
mechanical versus median nerve electrical stimulation
[64].
Single cell recordings from monkeys indicate that some
neurons representing multiple digits in areas 2 and 5 have
bilateral or ipsilateral receptive fields [68], and a few noci-
ceptive neurons at the junction of areas 3b and 1 have
large, bilateral receptive fields [69]. Thus the source of the
early ipsilateral response is likely not only area 3b, but
may also include input from cells in area 1, and possibly
areas 2 and 5 as well. Recent evidence from electrophysi-
ological recording in monkeys suggests that responses
from ipsilateral anterior parietal fields are elicited by feed-
back rather than feedforward afferents [64], which may be
related to the latency delay of the ipsilateral response
observed in previous SEP [62] and the current MEG study.
It has been suggested that transcallosal pathways may
mediate responses from ipsilateral anterior parietal areas
both in humans [59-61,67] and in monkeys [64,65].
However, anatomical evidence from macaque monkeys
indicates that anterior parietal areas, in particular area 3b,
have sparse or absent callosal connections for the hand
representation [1,22,25]. Callosal connections become
denser in the more caudal fields, from areas 3b to 1 and 2
[24]. Thus, transcallosal pathways mediating the early
ipsilateral responses would be through these caudal areas,
or S2/PV.
Hemispheric differences
In addition, some previous functional imaging studies
suggest functional dominance, or an increased source
amplitude, in the left versus the right hemisphere in
human primary [70-72] and secondary [73-77] somato-
sensory cortex. An expanded hand representation in left
anterior parietal fields has also been proposed [72,78].
However, morphometric and cytoarchitectonic measure-
ments show no lateralized differences in somatosensory
cortices [79]. Psychophysical tests show no differences in
spatial acuity between hands [80,81], although there does
appear to be a left-hemisphere advantage for tactile
processing of simultaneity judgment [82]. Furthermore,
as in our study, previous somatosensory evoked potential
studies show no difference in topography or response
amplitude between the two hemispheres [83,84]. Thus, it
is necessary to reassess the hemispheric asymmetry of
somatosensory cortex.
The differences between studies may be due to the differ-
ent types of stimuli used. The electrical stimulation used
in previous studies showing asymmetry is not receptor
specific, and elicits a more complex cortical activation. A
recent MEG study showed that movement might be
involved in the lateral asymmetry of somatosensory cor-
tex, and the intensity of electrical stimulation often
exceeded the motor threshold in previous studies [70-
75,77]. Passive finger movement was found to evoke lat-
erally asymmetrical responses in somatosensory cortex
[76]. Thus, the increased response in left somatosensory
cortex evoked by electric stimulation may reflect the lat-
eral asymmetry of movement rather than tactile informa-
tion processing.
Conclusion
This human MEG study revealed that the bilateral spatio-
temporal integration in S2/PV takes place over a large cor-
tical area and over a long time period. Further, the
strength of integration in this region is distance-depend-
ent. The wide overlap of digit receptive fields in S2/PV
might account for complex functions such as manual
exploration and bimanual coordination, thought to be
crucially dependent on S2/PV. In contrast, the properties
of spatiotemporal integration in anterior parietal areas
were different from those in S2/PV with significant tem-
poral integration while spatial integration was reduced,
which is consistent with the critical role of anterior pari-
etal fields in spatial discrimination. The early ipsilateral
response observed in over half of subjects suggests that
anterior parietal fields do accept tactile inputs from the
ipsilateral side of body. In addition, no tactile response
difference between hemispheres indicated functional
symmetry in human somatosensory cortex.
Methods
Subjects
SEFs were recorded in fifteen right-handed and six left-
handed healthy adult subjects (10 male and 5 female
right-handers; 2 male and 4 female left-handers; age range
22–40 years), using an Omega 2000 Whole-Cortex MEG
System (CTF Systems Inc. Port Coquitlam, Canada; 275
DC SQUID first-order axial gradiometers). All subjects
signed an informed consent as approved by the Commit-
tee on Human Research of the University of California,
San Francisco. The Edinburgh inventory [85] was used to
determine the direction and degree of handedness for
each subject. The subjects were seated comfortably and
maintained their head position during MEG testing in a
magnetically shielded room. Subjects' hands were placed
palm up on opposite armrests. The subjects closed their
eyes, wore earplugs and were asked not to pay attention to
the tactile stimulation.
BMC Neuroscience 2007, 8:21 http://www.biomedcentral.com/1471-2202/8/21
Page 11 of 14
(page number not for citation purposes)
Stimuli
Tactile stimuli were pneumatically driven pulses (~140
ms duration) applied to the tips of the digits with balloon
diaphragms. A digit oddball paradigm [9,16,30] was used
to examine the representations of the index fingers (D2,
infrequent deviant stimulus) while varying the location of
the frequent standard stimuli across adjacent (D3), non-
adjacent (D4) and contralateral (D2) digits. In this odd-
ball paradigm, infrequent deviant stimuli interspersed
with frequent standard stimuli were presented. The inten-
sity of all stimuli was well above detection threshold at 17
PSI (pounds per square inch). The location of the stand-
ard was changed between blocks and the order (including
deviant alone block) was randomized across subjects. In
each block of 600–900 trials with an ISI of 0.33s and a jit-
ter of 10 ms, standard and deviant stimuli were presented
at probabilities of 0.83 and 0.17 respectively. Deviants
were always followed by 3–7 standards to allow for an
adaptation to the standard. To compare the tactile
response to single finger stimulation in different hemi-
spheres, deviants were also presented alone at two rates:
one equal to that for deviants (mean ISI: 2 s) and the other
equal to that for the compound of deviants and standards
(mean ISI: 0.33s) in the mismatch paradigm (Figure 6).
Data recording and analysis
Data were collected at a sample rate of 1200 Hz. The filter-
ing passband for data analysis was 2–40 Hz. About 100
artifact-free trials for deviant stimuli (D2) were averaged
in each test block. Head position relative to the MEG sen-
sors was determined before and after each test block by
means of three small coils placed at landmark sites
(nasion, left and right preauricular points).
MEG data was analyzed using an equivalent current
dipole (ECD) embedded in a spherical conducting
medium. The locations of index finger representations in
somatosensory cortex were determined using a dipole fit
with contralateral index finger stimulation alone. SEFs in
somatosensory cortex peaking in the time window up to
200 ms following stimulus onset were analyzed. The early
(30–70 ms) response was analyzed for activation in ante-
rior parietal fields; and the late response (70–130 ms) was
analyzed for activation of S2/PV [11,26]. Sensors record-
ing from the hemisphere contralateral to the stimulated
index finger were chosen to determine the ECD of the
most dominant source. The position and orientation of
the ECD corresponding to the early response were first
found and fixed; then another dipole corresponding to
the late response was added with the early one fixed, then
was fitted and fixed successively. Only sources with high
goodness of fit (> 85%) were accepted. Dipoles matching
anterior parietal fields and S2/PV in each hemisphere
were identified and fixed based on contralateral index fin-
ger stimulation, and they were used for analysis of data
from other stimulation conditions. The response laten-
cies, amplitudes (root-mean-square value, RMS) of each
hemisphere and dipole moments (Q value) for all of four
dipole locations were estimated for the different stimula-
tion conditions based on peaks within the early and late
time periods.
Eight of the subjects were also scanned using a 1.5T MRI
scanner (GE Medical System, Milwaukee, WI) to acquire a
3D structural image (flip angle = 40°, TR = 27 ms, TE = 6
ms, FOV = 240 × 240 mm, 1.5 mm slice thickness, 256 ×
256 × 124 pixels). Three fiducials were placed on the sub-
ject at the same three locations as the localizing coils in
MEG. This information was used to coregister the MEG
data to the MRI image. Each subject's structural MRI was
normalized to MNI space using Neurodynamic Utility
Toolbox for MEG [86]. Then the MNI coordinates of
dipole positions were converted to Talairach coordinates,
using a non-linear transform [87].
Paired Student t-tests were used to assess significant differ-
ence between condition pairs. In cases where the number
of conditions exceeds two, repeated measures ANOVAs
were used for assessing statistical significance between
responses across different stimulation conditions. In these
cases, Bonferroni post-hoc tests were used to assess signif-
icance between specific condition pairs, whereby after cor-
rection for multiple comparisons a significance threshold
of either p < 0.01 or p < 0.05 was used. Data are presented
as mean values ± standard error of the mean throughout.
List of abbreviations
PV: parietal ventral area
MEG: magnetoencephalography
SEFs: somatosensory evoked fields
ECD: equivalent current dipole
RMS: root mean square
Q: dipole moment
LD2: left index finger
RD2: right index finger
Authors' contributions
ZZ, EAD, DJM and SSN designed the study. ZZ and EAD
drafted the manuscript. JMZ, DJM and SSN helped to draft
the manuscript. ZZ and JMZ recorded and analyzed MEG
and MRI data. All authors read and approved the final
manuscript.
BMC Neuroscience 2007, 8:21 http://www.biomedcentral.com/1471-2202/8/21
Page 12 of 14
(page number not for citation purposes)
Acknowledgements
This work was supported by NIH grant NS044590 to EAD and from the
Dana Foundation to SSN. We thank Anne Findlay and Susanne Honma for
their excellent technical help with data collection and analysis. We also
thank Sarang S. Dalal for help with data analysis using the Neurodynamic
Utility Toolbox for MEG.
References
1. Krubitzer LA, Kaas JH: The organization and connections of
somatosensory cortex in marmosets. J Neurosci 1990,
10(3):952-74.
2. Krubitzer L, Clarey J, Tweedale R, Elston G, Calford M: A redefini-
tion of somatosensory areas in the lateral sulcus of macaque
monkeys. J Neurosci 1995, 15(5 Pt 2):3821-39.
3. Disbrow E, Roberts T, Krubitzer L: Somatotopic organization of
cortical fields in the lateral sulcus of Homo sapiens: evidence
for SII and PV. J Comp Neurol 2000, 418(1):1-21.
4. Qi HX, Lyon DC, Kaas JH: Cortical and thalamic connections of
the parietal ventral somatosensory area in marmoset mon-
keys (Callithrix jacchus). J Comp Neurol 2002, 443(2):168-82.
5. Whitsel BL, Petrucelli LM, Werner G: Symmetry and connectiv-
ity in the map of the body surface in somatosensory area II
of primates. J Neurophysiol 1969, 32(2):170-83.
6. Burton H, Sinclair R: Somatosensory cortex and tactile percep-
tions. In Touch and Pain London: Academic Press; 1996.
7. Disbrow E, Litinas E, Recanzone GH, Padberg J, Krubitzer L: Cortical
connections of the second somatosensory area and the pari-
etal ventral area in macaque monkeys. J Comp Neurol 2003,
462(4):382-99.
8. Hari R, Hamalainen H, Hamalainen M, Kekoni J, Sams M, Tiihonen J:
Separate finger representations at the human second soma-
tosensory cortex. Neuroscience 1990, 37(1):245-9.
9. Forss N, Jousmaki V, Hari R: Interaction between afferent input
from fingers in human somatosensory cortex. Brain Res 1995,
685(1–2):68-76.
10. Disbrow E, Roberts T, Poeppel D, Krubitzer L: Evidence for inter-
hemispheric processing of inputs from the hands in human
S2 and PV. J Neurophysiol 2001, 85(5):2236-44.
11. Hoechstetter K, Rupp A, Stanèák A, Meinck HM, Stippich C, Berg P,
Scherg M: Interaction of tactile input in the human primary
and secondary somatosensory cortex – a magnetoencepha-
lographic study. Neuroimage 2001, 14(3):759-67.
Stimulus paradigmFigure 6
Stimulus paradigm. 1. Low rate (mean ISI; 2s) D2 stimulation (black bars) alone. 2. High rate (mean ISI: 0.33s) D2 stimula-
tion alone. 3. Ipsilateral D3; 4. ipsilateral D4; 5. contralateral D2 as the standard stimulus respectively (white bars), with D2 as
the deviant stimulus (black bars) in the digit mismatch paradigm. RD 3, 4 and LD 2 were used as standards with RD2 as devi-
ants; LD 3, 4 and RD2 were used as standards with LD2 as deviants.
BMC Neuroscience 2007, 8:21 http://www.biomedcentral.com/1471-2202/8/21
Page 13 of 14
(page number not for citation purposes)
12. Simões C, Mertens M, Forss N, Jousmäki V, Lütkenhöner B, Hari R:
Functional overlap of finger representations in human SI and
SII cortices. J Neurophysiol 2001, 86(4):1661-5.
13. Huttunen J, Ahlfors S, Hari R: Interaction of afferent impulses in
the human primary sensorimotor cortex. Electroencephalogr
Clin Neurophysiol 1992, 82(3):176-81.
14. Biermann K, Schmitz F, Witte OW, Konczak J, Freund HJ, Schnitzler
A: Interaction of finger representation in the human first
somatosensory cortex: a neuromagnetic study. Neurosci Lett
1998, 251(1):13-6.
15. Tanosaki M, Suzuki A, Takino R, Kimura T, Iguchi Y, Kurobo Y,
Haruta Y, Hoshi Y, Hashimoto I: Neural mechanisms for gener-
ation of tactile interference effects on somatosensory
evoked magnetic fields in humans. Clin Neurophysiol 2002,
113(5):672-80.
16. Hari R, Forss N: Magnetoencephalography in the study of
human somatosensorycortical processing. Philos Trans R Soc
Lond B Biol Sci 1999, 354(1387):1145-54.
17. Kakigi R, Hoshiyama M, Shimojo M, Naka D, Yamasaki H, Watanabe
S, Xiang J, Maeda K, Lam K, Itomi K, Nakamura A: The somatosen-
sory evoked magnetic fields. Prog Neurobiol 2000, 61(5):495-523.
18. Nakamura A, Yamada T, Goto A, Kato T, Ito K, Abe Y, Kachi T, Kakigi
R: Somatosensory homunculus as drawn by MEG. Neuroimage
1998, 7(4 Pt 1):377-86.
19. Maeda K, Kakigi R, Hoshiyama M, Koyama S: Topography of the
secondary somatosensory cortex in humans: a magnetoen-
cephalo-graphic study. Neuroreport 1999, 10(2):301-6.
20. Gardner EP, Costanzo RM: Spatial integration of multiple-point
stimuli in primary somatosensory cortical receptive fields of
alert monkeys. J Neurophysiol 1980, 43(2):420-43.
21. Chen LM, Friedman RM, Roe AW: Optical imaging of a tactile
illusion in area 3b of the primary somatosensory cortex. Sci-
ence 2003, 302(5646):881-5.
22. Jones EG, Powell TP: Connexions of the somatic sensory cortex
of the rhesus monkey. II. Contralateral cortical connexions.
Brain 1969, 92(4):717-30.
23. Karol EA, Pandya DN: The distribution of the corpus callosum
in the rhesus monkey. Brain 1971, 94(3):471-786.
24. Killackey HP, Gould HJ 3rd, Cusick CG, Pons TP, Kaas JH: The rela-
tion of corpus callosum connections to architectonic fields
and body surface maps in sensorimotor cortex of new and
old world monkeys. J Comp Neurol 1983, 219(4):384-419.
25. Padberg J, Disbrow E, Krubitzer L: The organization and connec-
tions of anterior and posterior parietal cortex in titi mon-
keys: do New World monkeys have an area 2? Cereb Cortex
2005, 15(12):1938-63.
26. Mertens M, Lütkenhöner B: Efficient neuromagnetic determina-
tion of landmarks in the somatosensory cortex. Clin Neuro-
physiol 2000, 111(8):1478-87.
27. Fitzgerald PJ, Lane JW, Thakur PH, Hsiao SS: Receptive field prop-
erties of the macaque second somatosensory cortex: evi-
dence for multiple functional representations. J Neurosci 2004,
24(49):11193-204.
28. Nelson RJ, Sur M, Felleman DJ, Kaas JH: Representations of the
body surface in postcentral parietal cortex of Macaca fascic-
ularis. J Comp Neurol 1980, 192(4):611-43.
29. Sripati AP, Yoshioka T, Denchev P, Hsiao SS, Johnson KO: Spatio-
temporal receptive fields of peripheral afferents and cortical
area 3b and 1 neurons in the primate somatosensory system.
J Neurosci 2006, 26(7):2101-14.
30. Kekoni J, Hämäläinen H, Saarinen M, Gröhn J, Reinikainen K, Lehtoko-
ski A, Näätänen R: Rate effect and mismatch responses in the
somatosensory system: ERP-recordings in humans. Biol Psy-
chol 1997, 46(2):125-42.
31. Tiihonen J, Hari R, Hamalainen M: Early deflections of cerebral
magnetic responses to median nerve stimulation. Electroen-
cephalogr Clin Neurophysiol 1989, 74(4):290-6.
32. Wikstrom H, Huttunen J, Korvenoja A, Virtanen J, Salonen O, Aronen
H, Ilmoniemi RJ: Effects of interstimulus interval on somato-
sensory evoked magnetic fields (SEFs): a hypothesis con-
cerning SEF generation at the primary sensorimotor cortex.
Electroencephalogr Clin Neurophysiol 1996, 100(6):479-87.
33. Mauguiere F, Merlet I, Forss N, Vanni S, Jousmaki V, Adeleine P, Hari
R: Activation of a distributed somatosensory cortical net-
work in the human brain: a dipole modelling study of mag-
netic fields evoked by median nerve stimulation. Part II:
Effects of stimulus rate, attention and stimulus detection.
Electroencephalogr Clin Neurophysiol 1997, 104(4):290-5.
34. Nagamine T, Makela J, Mima T, Mikuni N, Nishitani N, Satoh T, Ikeda
A, Shibasaki H: Serial processing of the somesthetic informa-
tion revealed by different effects of stimulus rate on the som-
atosensory-evoked potentials and magnetic fields. Brain Res
1998, 791(1–2):200-8.
35. Schnitzler A, Volkmann J, Enck P, Frieling T, Witte OW, Freund HJ:
Different cortical organization of visceral and somatic sensa-
tion in humans. Eur J Neurosci 1999, 11(1):305-15.
36. Hamada Y, Otsuka S, Okamoto T, Suzuki R: The profile of the
recovery cycle in human primary and secondary somatosen-
sory cortex: a magnetoencephalography study. Clin Neurophys-
iol 2002, 113(11):1787-93.
37. Pons TP, Garraghty PE, Friedman DP, Mishkin M: Physiological evi-
dence for serial processing in somatosensory cortex. Science
1987, 237(4813):417-20.
38. Pons TP, Garraghty PE, Mishkin M: Serial and parallel processing
of tactual information in somatosensory cortex of rhesus
monkeys. J Neurophysiol 1992, 68(2):518-27.
39. Friedman DP, Murray EA, O'Neill JB, Mishkin M: Cortical connec-
tions of the somatosensory fields of the lateral sulcus of
macaques: evidence for a corticolimbic pathway for touch. J
Comp Neurol 1986, 252(3):323-47.
40. Zhang HQ, Murray GM, Turman AB, Mackie PD, Coleman GT, Rowe
MJ: Parallel processing in cerebral cortex of the marmoset
monkey: effect of reversible SI inactivation on tactile
responses in SII. J Neurophysiol 1996, 76(6):3633-55.
41. Zhang HQ, Murray GM, Coleman GT, Turman AB, Zhang SP, Rowe
MJ: Functional characteristics of the parallel SI- and SII-pro-
jecting neurons of the thalamic ventral posterior nucleus in
the marmoset. J Neurophysiol 2001, 85(5):1805-22.
42. Zhang HQ, Zachariah MK, Coleman GT, Rowe MJ: Hierarchical
equivalence of somatosensory areas I and II for tactile
processing in the cerebral cortex of the marmoset monkey.
J Neurophysiol 2001, 85(5):1823-35.
43. Karhu J, Tesche CD: Simultaneous early processing of sensory
input in human primary (SI) and secondary (SII) somatosen-
sory cortices. J Neurophysiol 1999, 81(5):2017-25.
44. Allison T, McCarthy G, Wood CC, Williamson PD, Spencer DD:
Human cortical potentials evoked by stimulation of the
median nerve. II. Cytoarchitectonic areas generating long-
latency activity. J Neurophysiol 1989, 62(3):711-22.
45. Stancak A, Hoechstetter K, Tintera J, Vrana J, Rachmanova R, Kralik
J, Scherg M: Source activity in the human secondary somato-
sensory cortex depends on the size of corpus callosum. Brain
Res 2002, 936(1–2):47-57.
46. Inui K, Wang X, Tamura Y, Kaneoke Y, Kakigi R: Serial processing
in the human somatosensory system. Cereb Cortex 2004,
14(8):851-7.
47. Garcha HS, Ettlinger G: The effects of unilateral or bilateral
removals of the second somatosensory cortex (area SII): a
profound tactile disorder in monkeys. Cortex 1978,
14(3):319-26.
48. Garcha HS, Ettlinger G: Tactile discrimination learning in the
monkey: the effects of unilateral or bilateral removals of the
second somatosensory cortex (area SII). Cortex 1980,
16(3):397-412.
49. Mishkin M: Analogous neural models for tactual and visual
learning. Neuropsychologia 1979, 17(2):139-51.
50. Murray EA, Mishkin M: Relative contributions of SII and area 5
to tactile discrimination in monkeys. Behav Brain Res 1984,
11(1):67-83.
51. Caselli RJ: Rediscovering tactile agnosia. Mayo Clin Proc 1991,
66(2):129-42.
52. Caselli RJ: Ventrolateral and dorsomedial somatosensory
association cortex damage produces distinct somesthetic
syndromes in humans. Neurology 1993, 43(4):762-71.
53. Huttunen J, Hari R, Leinonen L: Cerebral magnetic responses to
stimulation of ulnar and median nerves. Electroencephalogr Clin
Neurophysiol 1987, 66(4):391-400.
54. Mountcastle VB, Powell TP: Neural mechanisms subserving
cutaneous sensibility, with special reference to the role of
afferent inhibition in sensory perception and discrimination.
Bull Johns Hopkins Hosp 1959, 105:201-32.
Publish with BioMed Central and every
scientist can read your work free of charge
"BioMed Central will be the most significant development for
disseminating the results of biomedical researc h in our lifetime."
Sir Paul Nurse, Cancer Research UK
Your research papers will be:
available free of charge to the entire biomedical community
peer reviewed and published immediately upon acceptance
cited in PubMed and archived on PubMed Central
yours — you keep the copyright
Submit your manuscript here:
http://www.biomedcentral.com/info/publishing_adv.asp
BioMedcentral
BMC Neuroscience 2007, 8:21 http://www.biomedcentral.com/1471-2202/8/21
Page 14 of 14
(page number not for citation purposes)
55. Iwamura Y, Tanaka M, Sakamoto M, Hikosaka O: Functional subdi-
visions representing different finger regions in area 3 of the
first somatosensory cortex of the conscious monkey. Exp
Brain Res 1983, 51:315-326.
56. DiCarlo JJ, Johnson KO, Hsiao SS: Structure of receptive fields in
area 3b of primary somatosensory cortex in the alert mon-
key. J Neurosci 1998, 18(7):2626-45.
57. DiCarlo JJ, Johnson KO: Velocity invariance of receptive field
structure in somatosensory cortical area 3b of the alert
monkey. J Neurosci 1999, 19(1):401-19.
58. DiCarlo JJ, Johnson KO: Spatial and temporal structure of
receptive fields in primate somatosensory area 3b: effects of
stimulus scanning direction and orientation. J Neurosci 2000,
20(1):495-510.
59. Schnitzler A, Salmelin R, Salenius S, Jousmaki V, Hari R: Tactile
information from the human hand reaches the ipsilateral
primary somatosensory cortex. Neurosci Lett 1995, 200(1):25-8.
60. Korvenoja A, Wikstrom H, Huttunen J, Virtanan J, Laine P, Aronen HJ,
Seppalainen AM, Ilmoniemi RJ: Activation of ipsilateral primary
sensorimotor cortex by median nerve stimulation. Neurore-
port 1995, 6(18):2589-93.
61. Korvenoja A, Huttunen J, Salli E, Pohjonen H, Martinkauppi S, Palva
JM, Lauronen L, Virtanen J, Ilmoniemi RJ, Aronen HJ: Activation of
multiple cortical areas in response to somatosensory stimu-
lation: combined magnetoencephalographic and functional
magnetic resonance imaging. Hum Brain Mapp 1999, 8(1):13-27.
62. Noachtar S, Lüders HO, Dinner DS, Klem G: Ipsilateral median
somatosensory evoked potentials recorded from human
somatosensory cortex. Electroencephalogr Clin Neurophysiol 1997,
104(3):189-98.
63. Kanno A, Nakasato N, Hatanaka K, Yoshimoto T: Ipsilateral area
3b responses to median nerve somatosensory stimulation.
Neuroimage 2003, 18(1):169-77.
64. Lipton ML, Fu K, Branch CA, Schroeder CE: Ipsilateral hand input
to area 3b revealed by converging hemodynamic and elec-
trophysiological analyses in macaque monkeys. J Neurosci
2006, 26(1):180-185.
65. Tommerdahl M, Simons SB, Chiu JS, Favorov O, Whitsel BL: Ipsilat-
eral input modifies the primary somatosensory cortex
response to contralateral skin flutter. J Neurosci 2006,
26(22):5970-7.
66. Nihashi T, Naganawa S, Sato C, Kawai H, Nakamura T, Fukatsu H, Ish-
igaki T, Aoki I: Contralateral and ipsilateral responses in pri-
mary somatosensory cortex following electrical median
nerve stimulation – an fMRI study. Clin Neurophysiol 2005,
116(4):842-8.
67. Hlushchuk Y, Hari R: Transient suppression of ipsilateral pri-
mary somatosensory cortex during tactile finger stimula-
tion. J Neurosci 2006, 26(21):5819-24.
68. Iwamura Y, Iriki A, Tanaka M: Bilateral hand representation in
the postcentral somatosensory cortex. Nature 1994,
369(6481):554-6.
69. Kenshalo DR Jr, Isensee O: Responses of primate SI cortical
neurons to noxious stimuli. J Neurophysiol 1983, 50(6):1479-96.
70. Rossini PM, Narici L, Martino G, Pasquarelli A, Peresson M, Pizzella V,
Tecchio F, Romani GL: Analysis of interhemispheric asym-
metries of somatosensory evoked magnetic fields to right
and left median nerve stimulation. Electroencephalogr Clin Neuro-
physiol 1994, 91(6):476-82.
71. Buchner H, Ludwig I, Waberski T, Wilmes K, Ferbert A: Hemi-
spheric asymmetries of early cortical somatosensory evoked
potentials revealed by topographic analysis. Electromyogr Clin
Neurophysiol 1995, 35(4):207-15.
72. Jung P, Baumgärtner U, Bauermann T, Magerl W, Gawehn J, Stoeter
P, Treede RD: Asymmetry in the human primary somatosen-
sory cortex and handedness. Neuroimage 2003, 19(3):913-23.
73. Forss N, Hari R, Salmelin R, Ahonen A, Hämäläinen M, Kajola M, Knu-
utila J, Simola J: Activation of the human posterior parietal cor-
tex by median nerve stimulation. Exp Brain Res 1994,
99(2):309-15.
74. Kany C, Treede RD: Median and tibial nerve somatosensory
evoked potentials: middle-latency components from the
vicinity of the secondary somatosensory cortex in humans.
Electroencephalogr Clin Neurophysiol 1997, 104(5):402-10.
75. Simões C, Alary F, Forss N, Hari R:
Left-hemisphere-dominant
SII activation after bilateral median nerve stimulation. Neu-
roimage 2002, 15(3):686-90.
76. Alary F, Simões C, Jousmäki V, Forss N, Hari R: Cortical activation
associated with passive movements of the human index fin-
ger: an MEG study. Neuroimage 2002, 15(3):691-6.
77. Mäkelä JP, Illman M, Jousmäki V, Numminen J, Lehecka M, Salenius S,
Forss N, Hari R: Dorsal penile nerve stimulation elicits left-
hemisphere dominant activation in the second somatosen-
sory cortex. Hum Brain Mapp 2003, 18(2):90-9.
78. Sörös P, Knecht S, Imai T, Gürtler S, Lütkenhöner B, Ringelstein EB,
Henningsen H: Cortical asymmetries of the human somato-
sensory hand representation in right- and left-handers. Neu-
rosci Lett 1999, 271(2):89-92.
79. White LE, Andrews TJ, Hulette C, Richards A, Groelle M, Paydarfar
J, Purves D: Structure of the human sensorimotor system. II:
Lateral symmetry. Cereb Cortex 1997, 7(1):31-47.
80. Sathian K, Zangaladze A: Tactile spatial acuity at the human fin-
gertip and lip: bilateral symmetry and interdigit variability.
Neurology 1996, 46(5):1464-6.
81. Vega-Bermudez F, Johnson KO: Differences in spatial acuity
between digits. Neurology 2001, 56(10):1389-91.
82. Nicholls ME, Lindell AK: A left hemisphere, but not right hem-
ispace, advantage for tactual simultaneity judgments. Percept
Psychophys 2000, 62(4):717-25.
83. Kakigi R, Shibasaki H: Effects of age, gender, and stimulus side
on scalp topography of somatosensory evoked potentials fol-
lowing median nerve stimulatiom. J Clin Neurophysiol 1991,
8(3):320-330.
84. Kakigi R, Shibasaki H: Effects of age, gender, and stimulus side
on scalp topography of somatosensory evoked potentials fol-
lowing posterior tibial nerve stimulatiom. J Clin Neurophysiol
1992, 9(3):431-440.
85. Oldfield RC: The assessment and analysis of handedness: the
Edinburgh inventory.
Neuropsychologia 1971, 9(1):97-113.
86. Dalal SS, Zumer JM, Agrawal V, Hild KE, Sekihara K, Nagarajan SS:
NUTMEG: a neuromagnetic source reconstruction toolbox.
Neurol Clin Neurophysiol 2004, 2004:52.
87. Brett M: The MNI brain and the Talairach atlas. [http://imag
ing.mrc-cbu.cam.ac.uk/imaging/MniTalairach].
