1Brain Research Unit,
Karhu, J. and
C. D. Tesche.
Simultaneous early processing of sensory input in human primary (SI)
and secondary (SII) somatosensory cortices. The anatomic connectivity of the somatosensory system supports the simultaneous participation of widely separated cortical areas in the early processing of sensory input. We recorded evoked neuromagnetic responses
noninvasively from human primary (SI) and secondary (SII) somatosensory
cortices to unilateral median nerve stimulation. Brief current pulses
were applied repetitively to the median nerve at the wrist at 2 Hz for
800-1,500 trials. A single pulse was omitted from the train at random
intervals (15% of omissions). We observed synchronized neuronal
population activity in contralateral SII area 20-30 ms after
stimulation, coincident in time with the first responses generated in
SI. Both contra- and ipsilateral SII areas showed prominent activity at
50-60 ms with an average delay of 13 ms for ipsilateral compared with
contralateral responses. The refractory behavior of the early SII
responses to the omissions differed from those observed at ~100 ms,
indicative of distinct neuronal assemblies responding at each latency.
These results indicate that SII and/or associated cortices in parietal
operculum, often viewed as higher-order processing areas for
somatosensory perception, are coactivated with SI during the early
processing of intermittent somatosensory input.
A widely held view of cortical somatosensory
organization is that the sensory scene is completed by serial,
hierarchical processing of gradually more complex stimulus features.
Anatomically, this view is supported by the presence of large,
somatotopically organized primary receiving cortices with converging
projections to smaller association areas. Primary somatosensory cortex
SI contains, from anterior to posterior, four cytoarchitectonic areas
3a, 3b, 1, and 2 (Brodmann 1909 In addition to PPC, further processing of tactile information occurs in
second somatosensory cortex (SII) and neighboring cortical areas that
are located in the parietal operculum posterior to the face
representation in SI and medial to the primary auditory areas (for a
review, see Burton 1986 Extensive anatomic and physiological studies have confirmed that SII
obtains bilateral input (Robinson and Burton 1980a The cortico-cortical and thalamocortical connectivity of SII and
adjacent cortices provides a substrate for both early participation in
the initial processing of somatosensory input and in higher-order processing, which includes input from SI. Functionally, SII has been
associated with processing of the temporal features of somatic sensation (Burton and Sinclair 1991 Subjects and stimuli
We report results from six healthy volunteers (age 25-50 yr).
Informed consent was obtained from all subjects. Unilateral median
nerve stimulation was delivered through transcutaneous electrodes at
the wrist in the form of a train of brief constant current pulses
(rectangular shape, 0.3-ms duration) at 2 Hz (interstimulus intervals
of 0.5 s). Individual pulses in the train were omitted randomly
(15% omissions) to investigate possible responses to a brief
interruption of the temporal pattern of the stimuli (Fig. 1C). The pulse amplitudes
(4-6 mA) were adjusted individually to be completely painless but
strong enough to cause a muscle twitch in the hand muscles innervated
by the median nerve. Between 800 and 1,500 pulses were delivered to
each stimulated nerve.
ABSTRACT
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
INTRODUCTION
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
; Economo
1929
). In monkey, each area is occupied by a complete body map
(Nelson et al. 1980
; Pons et al. 1985
, 1987b
) with the largest cortical representations of peripheral sites like fingers or face corresponding to the largest somatosensory receptor density. The somatosensory association areas of posterior parietal cortex (PPC) are located posterior to primary somatosensory cortex (SI) (Powell and Mountcastle 1959
). Areas 3a and
3b receive the densest thalamocortical afferentation and project to
areas 1 and 2. Only the latter are connected anteriorly to the motor areas and to posterior association areas (Jones 1986
).
The anatomically hierarchical corticocortical projections between the
subdivisions of SI and association cortices are taken to advocate
functional hierarchy in somatosensory processing.
). Originally, Woolsey and Fairman (1946)
demonstrated that this "second"
somatosensory area exists in a variety of animals and has separate
representations for different parts of the body. The activation of this
area to somatosensory stimulation first was observed in man by
intraoperative cortical recordings in epileptic patients
(Penfield and Jasper 1954
) and noninvasively with
magnetoencephalographic (MEG) recordings (Hari et al. 1984
,
1993
) and with positron-emission tomography (Burton et al. 1993
, 1997a
; Ledberg et al.
1995
). Recent anatomic and physiological studies in monkeys
have clarified the borders of the region that traditionally was
designated as SII, the neighboring parietal ventral area (PV)
(Krubitzer et al. 1995
) and insular cortex, which
includes retroinsular area (Ri) and granular insula (Ig) (Burton
et al. 1995
). Interestingly, at least two of these opercular
regions seem to have relatively complete body maps with enlarged
representation of the hand area similar to that observed in SI
(Burton et al. 1995
; Krubitzer et al.
1995
). The more anterior region is connected more strongly with
the area 3b in SI and is possibly more responsive to cutaneous
stimulation than the posterior one (Burton et al. 1995
;
Robinson and Burton 1980b
).
;
Whitsel et al. 1969
; for a review, see Burton
1986
). All cytoarchitectonic areas of SI are connected
reciprocally with the ipsilateral SII; however, the main source of
reciprocal callosal fibers between SI and contralateral SII may be in
area 2 (Manzoni et al. 1986
). Area 3b has callosal
connections also with PV, and SII is interconnected densely with both
ipsi- and contralateral PV (Krubitzer and Kaas 1990
).
The callosal connections between SI and SII are organized somatotopically (Manzoni et al. 1986
), and this
topographic organization appears to duplicate that of the association
connections between SI and SII in the ipsilateral hemisphere
(Jones and Powell 1969
). The cortico-cortical
association input from SI may have a significant role in defining the
response properties of neurons in SII and neighboring areas to
peripheral stimuli, and, subsequently, SII may contribute via
corticolimbic pathways to tactile learning and memory (Friedman
et al. 1986
; Mishkin 1979
; Murray and
Mishkin 1984
; Suzuki and Amaral 1994
).
; Ferrington
and Rowe 1980
), with sensorimotor integration (Huttunen
et al. 1996
), with tactile attention (Mima
1998
), and with tactile learning and intermanual transfer
(Ridley and Ettlinger 1976
). SII, together with other parietal regions (Iwamura et al. 1994
), may integrate
somatosensory information from both sides of the body (Manzoni
et al. 1986
; Ridley and Ettlinger 1976
). These
observations indicate that SII has the capacity to perform several
functions depending on the overall demands of somatosensory processing.
However, the timing of neuronal activity in SII and parietal operculum
with respect to the other somatosensory areas has remained somewhat
evasive. In this study, we used intermittent median nerve stimulation
and whole-scalp magnetoencephalography to obtain functional evidence for timing of initial activation of neuronal assemblies in human primary and secondary somatosensory cortical areas.
METHODS
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Fig. 1.
A and B: magnetoencephalographic (MEG)
signal detection illustrated with simulated data. magnetic resonance
(MR) images of the subject N1 show the locations
( ) of dipolar current sources in primary (SI;
A) and secondary (SII; B) somatosensory
cortices. Tails indicate the directions of the current flow at each
location. Corresponding MEG signals are shown on the
right. Each of the 61 squares in the array contain 2 superconducting sensors that measure, respectively, the gradients
Bn/
x and
Bn/
y of the magnetic
field component Bn perpendicular to the x-y plane
determined by the detector substrates.
, amplitudes and orientations
of the local magnetic field gradients. MEG signals are strongest in
those sensors that are located directly over the dipolar sources.
C: experimental design showing the temporal pattern of
the stimuli. Repetitive electrical stimulation of the median nerve at
the wrist at 2 Hz was interrupted by infrequent omissions of single
stimuli. Sequence of occurrence of the expected but omitted stimuli
(O), the 1st stimuli after an omission (F), and all the subsequent
stimuli (S) was randomized.
Data acquisition
Neurophysiologic responses to median nerve stimulation were
recorded with a magnetoencephalographic (MEG) array. Subjects were
seated underneath a cryogenic dewar containing a helmet-shaped array of
122 superconducting quantum interference detectors (SQUIDs) (Ahonen et al. 1993). The SQUID sensors were mounted in
pairs on planar substrates at 61 sites over the scalp. Each sensor was configured to sample the temporal variation of the local magnetic field
gradient created by changes in current flow in the brain. Figure 1,
A and B, shows the distribution of the sensors
across the array and results of a simulation of MEG signals
corresponding to idealized sources of current in SI and in SII.
Measurements were performed inside a magnetically shielded room. Three small coils were located on the subject's scalp before entering the room. A 3-D digitizer (Polhemus Navigation Science, Colchester, VT) was used to record the locations of the coils with respect to nasion and left and right preauricular points. During the measurement session, each coil was energized individually with current immediately before recording a block of data. The position of the head with respect to the array was determined from measurements of the magnetic field patterns generated by these test currents. This allowed the alignment of a coordinate system for the MEG data with magnetic resonance images for each subject (1-T Siemens Magnetom system with a MPR3D sequence).
Data recorded by the array were band-pass filtered at 0.03-330 Hz and sampled at 1 kHz. Average evoked MEG responses were calculated on-line time-locked to the presentation of stimuli S and of stimuli F over 600-ms epochs (c.f. Fig. 1C). In a separate calculation, responses were averaged over 1,100-ms epochs time-locked to the anticipated but omitted stimuli (an omission is indicated by the letter O in Fig. 1C). These epochs also included responses to the subsequent first stimulus after an omission (stimuli F in Fig. 1C). Averaged evoked MEG responses for epochs containing all stimuli except those following immediately after an omitted stimulus (stimuli S in Fig. 1C) were calculated subsequently off-line. A vertical electrooculogram was used to reject trials contaminated by eye movements and blinks (rejection limits ±150 µV).
Signal analysis
An equivalent current dipole (ECD) model was used to
characterize neuronal population activity in superficial fissural
cortex. An ECD is a short segment of current flow used to approximate a
fairly well-localized (~cm) region of activity (Williamson and Kaufman 1981; for a review, see
Hämäläinen et al. 1993
). MEG responses
for these sources were computed using a spherical head model with
parameters fixed by an approximation of the local curvature of the
sphere to the configuration of the skull directly over the presumed
source location.
Individual ECD locations and orientations were determined for sources in SI, SII, and associated cortical areas from a least-squares fit of the predicted signals to the data. Signals were used for subsets of 34 channels located over central (SI and parietal sources) and temporal (SII and parietal opercular sources) areas, respectively. SQUID sensors detect relative changes in the signal strength as a function of time, necessitating a choice of baseline for the measured responses. The baseline for the epochs containing responses to the omitted stimuli and to the first stimuli after omission was the average of the sensor readings from 100 to 5 ms preceding the omission. The baseline for the evoked responses to the subsequent stimuli was the average of the sensor readings from 100 to 5 ms before the corresponding stimulation.
A quantitative measure of the overlap of two patterns of MEG signal
strengths and orientations, such as those shown in Fig. 1, A
and B, can be determined directly from the data
(Ilmoniemi and Williamson 1987; Uusitalo and
Ilmoniemi 1997
). The degree of overlap is characterized by a
single parameter, the signal-space (SSP) angle. Current distributions
in the brain that generate identical patterns of signals in the MEG
array are not distinguishable: the corresponding SSP angle is 0°.
Signal patterns that are completely orthogonal determine an SSP angle
of 90°. All ECDs used in the present analysis, including those of SI
and SII, had pairwise SSP angles in excess of 30° and consequently
could be adequately distinguished by the 122-channel MEG array.
The random omissions of individual stimuli elicited responses that
appeared as more complex and widespread patterns of activity across the
array. Characterization of these responses by ECD sources was not
attempted. The complex omission responses were characterized at
specific latencies directly as the patterns of signals recorded in the
MEG array. Waveforms were determined simultaneously for all of the ECD
sources and the omission-related responses from a multicomponent
analysis of the MEG data (Tesche et al. 1995). These
waveforms are referred to in the text as SSP waveforms.
The measured data contained contributions from neuronal population
activity within the human brain and also contributions from various
external noise sources. These noise sources, referred to collectively
as "system noise," were uncorrelated with the brain signals. The
effective system noise for each SSP component was determined from data
recorded for the same number of trials and sampling frequency/filter
settings with no subject under the array (Tesche et al.
1995). Only features such as repeatable peaks in evoked
response waveforms that had amplitudes exceeding the corresponding
system noise by
2.5 SD were accepted for further analysis. The
statistical significance of source strength differences between all the
averaged responses except the first ones after omissions (responses to
the S stimuli in Fig. 1C) and the responses to the first
stimuli after omissions (responses to the F stimuli in Fig.
1C) was tested by Student's paired two-tailed
t-test.
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RESULTS |
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Figure 2 shows the locations and
orientations for sources in SI and SII (subject N1). The
averaged SSP waveforms indicate time-locked neuronal population
activity in contralateral SI and in bilateral SII cortices to right
median nerve stimulation. During the first 200 ms after the omitted
stimuli, the waveforms for SI and SII are on the order of system noise.
In contrast, the activation of SI to the first and subsequent median
nerve stimulations after omissions begins with brisk, prominent
responses at ~20 ms after the stimulation. In general, SI waveforms
display a characteristic, well-known pattern of neuromagnetic responses
at 35, 45, 60-80, and ~100 ms (Hari et al. 1984,
1993
; Mauguière et al. 1997a
,b
).
|
Surprisingly, SII contralateral to stimulation also shows initial activity at ~20 ms after the stimulation with prominent bilateral responses occurring first at 40-60 ms. Because the SSP angles between SI and SII for all recordings were on average 66 ± 13°, (complete dissimilarity 90°), disentanglement of their respective signals in the present analysis is highly likely. In contrast, activation of separate neuronal populations within SII would correspond to almost identical patterns of signals in the MEG array. Thus the SII SSP waveforms shown here may contain at each latency contributions from slightly different locations and orientations of the underlying sources within SII and immediately adjacent areas in parietal operculum.
Figure 3 shows SSP waveforms for contralateral SI and bilateral SII sources for both hemispheres in all subjects. The responses to the first stimuli after omissions and the responses to all the other stimuli are depicted separately. In SI, the initial 20-ms responses were evident in all studied hemispheres. In contralateral SII, the 20-ms activity was detected in 7 of 12 studied hemispheres (subjects N1, N2, N3, N5, and N6) and the 40-60-ms activity in 9 of 12 studied hemispheres (subjects N1, N2, N3, N4, and N5). The first response of SII preceded the first response of SI in four hemispheres (subjects N1, N3, and N5). The 100-ms responses were observed in all studied hemispheres. In SII ipsilateral to stimulation, SII responses could be recognized at around 50 ms in 8 of 12 studied hemispheres and at 100 ms in all studied hemispheres. Ipsilateral 50- and 100-ms SII activity peaked significantly later than the corresponding activity of contralateral SII (cf. Table 1).
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|
Figure 4 shows the SII responses to contralateral median nerve stimulation in all subjects with a larger amplification than in Fig. 3. The identification of the latencies of the P1, P2, and P3 peaks are indicated on the figure. The amplitudes of these early SII responses for each subject and hemisphere are shown in Table 2. The earliest P1 response in SII (mean latency 20.9 ± 2.9 ms) coincides in time with N20 response in SI (20.8 ± 1.4 ms). P1 was followed by an opposite deflection (N1; 29.2 ± 4.4 ms) in seven hemispheres and subsequent activation (P2; 40.7 ± 4.0 ms) was followed by an opposite deflection (N2; 54.3 ± 7.3 ms) in six hemispheres. The most prominent SII activity started at ~80 ms (mean latency 83.8 ± 10.3 ms).
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Preceding omissions did not have any significant effects on SI responses, whereas they clearly enhanced the 100-ms, but not earlier, responses in SII. The enhanced responses to omissions during the 100-ms response are shown in Fig. 4 as the difference area between the SSP waveforms for the first responses after omissions and the SSP waveforms for responses to subsequent stimuli. The group-averaged difference area to stimuli immediately after an omission is 7.1 ± 5.5 nAm, whereas the difference area to all the other stimuli is 2.1 ± 1.2 nAm (P < 0.01).
Figure 5 displays the relationship between the latency of the earliest SI response and the body length, between the earliest SII response and the body length, and between the earliest SI and SII responses. There is a clear dependence between the latencies of early SI and SII responses and the body length. All correlations are linear with the explained proportions of variance 84% (SI vs. body length), 78% (SII vs. body length), and 89% (SII vs. SI).
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DISCUSSION |
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Early neuronal population activity in SII
In this study, noninvasively recorded evoked neuromagnetic
responses revealed early synchronized neuronal population activity in
human SI and in parietal operculum, most likely in SII or adjacent somatosensory cortex. This activity started 20-30 ms after
intermittent median nerve stimulation in contralateral SII and
coincided in time with the first neuromagnetic activity in the primary
receiving cortex SI (representing the initial thalamocortical volley to area 3b). In four hemispheres, the peak activity in SII areas preceded
the activity in SI. There was also a clear dependence between the
latencies of initial SI and SII responses and the body length. Body
length is not a direct measure of the distance from the stimulation
site to cortex along the peripheral conducting nerve fibers. However,
it is very closely correlated with the latency of the initial
somatosensory evoked responses in SI as shown by normative studies for
intersubject comparisons of somatosensory evoked potentials (for
example, Chiappa 1990). The similar dependence between
the latency of early SII responses and the body length strongly
suggests a quite direct anatomic route to SII areas.
The initial activity in contralateral SII areas was followed by an
~40-ms evoked responses. Corresponding responses emerged in
ipsilateral SII areas slightly later, at 50-60 ms. This 10- to 20-ms
delay suggests callosal transmission of input from the contralateral
hemisphere (cf. Burton 1986; Manzoni et al.
1986
). The 40- to 60-ms time frame is significantly shorter
than that determined previously by the 100-180 ms bilateral SII
responses to regular stimuli (Hari et al. 1984
, 1993
;
Hämäläinen et al. 1990
). This first
sign of bilateral activity is an indicator of the time required for the
initiation of interhemispheric somatosensory processing of intermittent
stimuli in parietal operculum.
To our knowledge, early evoked responses in the 40-ms latency range
have been observed twice before in contralateral human SII by
intracranial recordings. In these two series of epileptic patients,
small SII responses were observed in 1 of 20 (Woolsey et al.
1979) and in 1 of 25 studied subjects (Lüders et
al. 1985
). These sparse observations are consistent with the
primary findings by Penfield and Rasmussen (1954), who
could define an SII area in only 8 of 350 cases of stimulation of the
sensorimotor cortex during brain surgery. The much higher prevalence of
SII responses in this study may be in part due to the different
sensitivity of used methods to neuronal currents. Human SII resides in
the depth of sylvian fissure, which is not reached by intracranial grid
electrodes but which is readily accessible to MEG recordings (Hari et al. 1984
).
Parallel anatomic routes to SI and SII
Simultaneous 20-ms neuronal population activity of primary
receiving cortex SI and SII clearly requires an anatomic substrate for
the conduction of peripheral input to receiving neurons. The thalamocortical connectivity of SII and neighboring areas in parietal operculum obey, in primates, a general principle that is different from
the connectivity of SI. SI receives the great majority of input via a
single (caudal ventral posterior lateral; VPLc) relay nucleus, whereas
the somatic cortical fields of parietal operculum each receive inputs
from an assembly of thalamic nuclei and the individual thalamic
somatosensory nuclei each project to more than one cortical field
(Burton 1984; Burton et al. 1990
;
Friedman and Murray 1986
; Krubitzer and Kaas
1992
; Manzoni et al. 1986
; Stevens et al.
1993
). The anatomic routes that mediate touch, pressure, and
position from peripheral nerve endings to SI via VPL of thalamus are
characterized by a strict organization according to the submodalities
of somatic sensation. Separate sets of thalamic relay cells project to
specific areas in SI. Signals from muscle afferents project to area 3a
(Phillips et al. 1971
) and from slowly and rapidly
adapting mechanoreceptors project mainly to areas 3b and 1, correspondingly (Kaas et al. 1979
). Signals from joints, muscles, and other "deep" structures project to area 2 (Burchfield and Duffy 1972
; Iwamura et al.
1993
; Pons et al. 1985
).
The ventroposterior inferior thalamic nucleus (VPi) appears to be the
main source of afferentation to the area traditionally designated as
SII (Burton et al. 1990; Friedman and Murray
1986
; Krubitzer and Kaas 1992
; Stevens et
al. 1993
). It is distinct from VPLc even if some thalamic relay
cells in VPLc may convey information to both SI and SII. VPi includes
also finger-like protrusions of neuron groups that extend to the region
of ventroposterior nucleus (VP). Neurons in all parts of VPi project
preferentially to SII rather than to SI, and PV in parietal operculum
receives the majority of its thalamic input via VPi (Krubitzer
and Kaas 1992
). Another substantial source of afferentation
resides in dorsal part of posterior nucleus (Po) (Burton et al.
1990
; Friedman and Murray 1986
), centrolateral
nucleus (CL) (Stevens et al. 1993
), and possibly also in
anterior pulvinar (Burton et al. 1990
). The insular and
retroinsular regions receive their input from a variety of nuclei
(including VPi) located at the posteroventral border of thalamus
(Friedman and Murray 1986
). A number of subcortical somatosensory afferent pathways to SII and neighboring cortices are
dissociated from those to SI.
Functional interaction between SI and SII
Neuronal activity in SII may depend on the integrity of processing
in SI or may even receive the majority of the low-frequency sensory
input via SI in primates (Garraghty et al. 1990;
Mountcastle et al. 1969
; Pons et al.
1987b
). The functional consequences of ablations or
inactivations of SI cortical areas in monkeys originally supported the
view of hierarchical processing of somatosensory input. Removal of SI
or even area 3a or 3b alone seriously impaired further processing of
tactile information (Garraghty et al. 1990
; Pons
et al. 1987a
). Furthermore, total removal of the hand
representation in SI left the corresponding area in SII initially
unresponsive, but after 6-8 wk this area was occupied by foot
representation (Pons et al. 1988
). This observation
contradicted the notion of any functionally significant direct thalamic
input from hand nerve endings to SII. However, deactivation of SI in
cats and prosimians did not have a clear effect on the responsiveness
of SII to cutaneous stimuli (Burton and Robinson 1987
;
Garraghty et al. 1991
; Turman et al.
1992
) and recent investigations in marmosets using reversible inactivations of SI (Rowe et al. 1996
; Turman et
al. 1995
; Zhang et al. 1996
) suggest that SI and
SII receive independent input in these species.
One possible hypothesis to account for the results of lesion studies
would be an ability of the somatosensory system to provoke subthreshold
excitatory postsynaptic effects on SII via callosal and/or ipsilateral
reciprocal connections between SI and SII (Manzoni et al.
1986). This kind of functional network could modulate the reactivity of different cortical regions and be also responsive to the
overall attentional or anticipatory state of the somatosensory system.
A recent study in marmosets provided evidence that reduction in SII
responsiveness in association with cooling of SI was attributable to
the loss of background facilitatory influence rather than a blockage of
peripheral input via a putative serial pathway from SI (Zhang et
al. 1996
). In another study, trained monkeys lost the ability
to discriminate somatosensory frequencies after lesions restricted to
SI but could relearn the tasks at higher thresholds with SII intact
(LaMotte and Mountcastle 1979
).
SII activation depends on stimulus intervals and attention
SII is capable of responding to temporal information over a wide
variety of time scales from milliseconds to several seconds. In
addition to high-frequency input, "vibration," (>100 Hz)
(Burton and Sinclair 1991;
Hämäläinen et al. 1990
),
low-frequency "flutter" (1-50 Hz) activates SII neurons strongly
in primates. Indeed, in some recent studies the majority of activated
SII neurons produce high-fidelity responses to very low-frequency input
at 1-10 Hz (Burton and Sinclair 1991
). At the level of
neuronal assemblies, similar responsiveness to the slow temporal
features of input is supported by previous neuromagnetic studies, which
have revealed very consistently the sensitivity of the 100-ms SII
response to regular interstimulus intervals (ISIs)
10-20 s
(Hari et al. 1984
, 1993
; Mauguière et al.
1997a
,b
). In contrast, early SI neuronal population responses
are suppressed due to repetitive stimulation only at ISIs <150-120 ms
(Huttunen et al. 1992
).
The early coactivation of contralateral SI and parietal operculum
during regularly presented stimuli interspersed with omissions has not
been reported in the earlier studies in man which used uninterrupted
trains of stimuli (Forss et al. 1996; Hari et al. 1984
, 1993
). Quite recently intermittent stimulation studies
with random omissions and slightly longer ISIs of 1.2 s also
failed to evoke 20- to 60-ms activity in SII and surrounding areas
(Mauguière et al. 1997b
). Because many aspects of
the measurement techniques were roughly comparable for the previous and
present MEG studies, we conclude that the neuronal populations in
parietal operculum that respond at short latencies to intermittent
somatosensory input may not have been effectively activated by the
regular stimulation or by intermittent stimulation with 1.2-s ISI to
the level of detection in the previous studies. The large number of
averaged responses used in the present study (800-1,500) served to
enhance the signal-to-noise ratio and thus the detectability of fairly low-amplitude responses in parietal operculum.
Random omissions of robust somatosensory stimuli may draw attention
involuntarily to the stimulation and modulate the neuronal response of
cortical areas. Poranen and Hyvärinen (1982)
suggested that activity of individual neurons in SII can be altered by
attentional effects. Neurophysiological studies in monkeys have
revealed increased firing rates in SI and both increased and decreased
firing in SII during a selective spatial attention task (Hsiao
et al. 1993
). Very recently, a selective attention study using
vibrotactile stimuli showed predominantly suppressed firing rates in
SII during the anticipation of a stimulus and relatively enhanced
activity during and after the attended stimulus (Burton et al.
1997b
). In two studies of somatosensory attention,
directed attention increased the magnitude of neuromagnetic 100-ms SII
activity to some extent (Mauguière et al. 1997a
,b
;
Mima et al. 1998
), but there were no signs of
attentional enhancement of SII activity at 20-60 ms.
We may use the previous results to suggest a consistent interpretation of the data presented here. In the present study, the early SII responses at 20 and 40-60 ms showed no enhancement to the stimuli immediately after the omission, whereas the responses at ~100 ms enhanced significantly. We did not experiment directly on the ISIs in this study. However, given the lack of change of the amplitude of the shortest latency responses in SII to a preceding stimulus omission, which in effect doubles the ISI from 0.5 to 1 s, one might not expect to see any major ISI dependence for this response.
In contrast, the enhancement of 100-ms responses agrees nicely with the
previously reported long recovery cycle 10-20 s for SII responses at
this latency range to both median nerve (Hari et al. 1984
,
1993
) and cutaneous (Hari et al. 1990
) hand
stimulation. The contrasting refractory behavior between the early and
late SII responses reported here suggests activation of separate
underlying neuronal assemblies during intermittent stimulation.
Interestingly, similar stimulus dependence and slow recovery of
population responses are taken in the auditory modality to represent
the duration of sensory memory traces (Lü et al.
1992
). The interpretation of 100 ms responses in Sll as an
indicator of sensory memory would be consistent with the observed
impairments in frequency discrimination and tactile learning after
lesions of SII cortex (LaMotte and Mountcastle 1979
;
Ridley and Ettlinger 1976
).
Conclusions
The data reported here are indicative of separate somatosensory
pathways contributing to early contralateral SI and SII responses. In
addition, the data support activation of two functionally separate neuronal assemblies in SII or adjacent cortical areas underlying the
early and late SII responses. Results from anatomic and PET studies are
consistent with the contribution of multiple neuronal populations to
simultaneous synchronous activity in SII and surrounding areas
(Burton et al. 1995, 1997a
; Krubitzer et al.
1995
). In the present study, some of the early contralateral
SII responses appear to emerge even before those in SI. However, even
very short delays of responses, on the order of 2-3 ms, would allow
for a synapse in SI and subsequent signal transmission via SI to SII.
Thus on the basis of the present evoked response data, it cannot be
concluded that the early SII activity was mediated exclusively by
separate thalamocortical connections or by additional cortical
afferents from SI. However, the data do demonstrate the coactivation of SII and/or associated cortices in parietal operculum with SI during the
early processing of the intermittent somatosensory input.
The timing of somatosensory input appears to be crucial for the
activation of neuronal populations in SII and/or adjacent cortical
areas. Interestingly, recent MEG results showed very early (16-20 ms)
neuronal responses to an identical median nerve stimulation in human
cerebellum (Tesche and Karhu 1997). This result,
together with that of the present study, suggests that early
coactivation may span both cerebral and cerebellar neuronal assemblies
in somatosensory networks during intermittent somatosensory stimuli.
The main factor separating these studies from earlier ones is the
relatively rapid somatosensory stimulation interspersed by randomly
timed omissions with a predictable duration. In a recent PET study,
anticipated somatosensory stimuli produced a substantial suppression of
blood flow in SII (Drevets et al. 1995
). We may
speculate that if SII areas are deeply involved in the detection of
temporal features of somatosensory input, the early responses may
reflect an enhancement of the fast, direct processing of anticipated
stimuli in SII. In this case, somatosensory networks which are
associated with the analysis of the timing of stimuli may modulate the
function of pathways to SII or of the receiving SII neurons.
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ACKNOWLEDGMENTS |
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This study was supported by National Institute of Neurological Disorders and Stroke Grant NS-34533.
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FOOTNOTES |
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Address reprint requests to C. D. Tesche.
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 10 August 1998; accepted in final form 17 December 1998.
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REFERENCES |
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