Department of Integrative Physiology, National Institute for Physiological Sciences, Okazaki 444-8585, Japan
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Abstract |
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Key Words: cortex, human, serial processing, somatosensory system
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Introduction |
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In spite of many observations in favor of serial hierarchical processing, there is no study that has precisely investigated the activation timing of multiple cortical areas within the postcentral gyrus and lateral sulcus region both in animals and in humans. If the major flow of signal processing is serially organized, each cortical response should show substantial differences in latency. In the present study, we investigated the temporal relationship among cortical responses to somatosensory stimulation using magnetoencephalography (MEG). Multi-channel MEG has an advantage over single-unit or field potential recordings in that it can easily record activities from multiple cortical areas simultaneously and noninvasively.
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Materials and Methods |
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Stimulation
Transcutaneous electrical stimulations were applied to the dorsum of the left hand just on the first metacarpal bone using a conventional bipolar felt tip electrode 0.9 mm in diameter with a distance of 23 mm between the anode and cathode. The electric stimulus was a current constant square wave pulse delivered at a random interval of 13 Hz. The stimulus duration was 0.5 ms. The current intensity was three times the sensory threshold (1.0 ± 0.2 mA). Transcutaneous stimulations of the dorsum of the hand at this intensity produce well-defined tactile sensations without painful sensations and evoke clear brain potentials (Inui et al., 2002) and magnetic fields (Inui et al., 2003
) due to signals conveyed by A-beta fibers. An electrical stimulation method is suited to the time-locked averaging technique because of the constant activation time.
MEG Recording and Analysis
Somatosensory evoked magnetic fields (SEFs) were recorded using a 37-channel axial-type first-order biomagnetometer (Magnes; Biomagnetic Technologies, San Diego, CA) as described previously (Kakigi et al., 2000). The probe was centered on the C4 position as based on the International 10/20 System. This position covered the hand area of SI and SII in the hemisphere contralateral to the stimulation (Fig. 1A). The SEFs were recorded with a filter of 0.1200 Hz at a sampling rate of 2083 Hz. The analysis window was 100 ms before and 100 ms after the stimulus and the prestimulus period was used as the DC baseline. One thousand responses were collected and the average of 800900 artifact-free responses was used for the analysis.
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where Mi are recorded data values, Ti are theoretical (model) values calculated at N measuring points and %V measures the goodness-of fit of the model comparing the recorded data and the model. In the present study, we used %V for individual data at a selected latency point. We also used %RV (percentage residual variance, 100%V) as the mean value of all the data (0100 ms). For example, 20%RV indicates that the mean RV value among all sampling points (100 ms at 2083 Hz sampling rate = 208 points) is 20%.
2 is defined as
where i are the standard deviations of the noise of each sensor that are calculated from the prestimulus period. In this study, reduced
2 values were used (
2r =
2/
, where
= degrees of freedom = N-numbers of parameters). The F-ratio is defined as
where 2r1 is calculated by a model with n dipoles and
2r2 by a model with n + 1 dipoles.
2r1 and
2r2 are distributed according to
2 distributions of N 5n and N 5(n + 1) degrees of freedom, respectively. The integral probability of obtaining a F-ratio value equal or greater than the obtained value is calculated to evaluate whether a model with a larger number of dipoles represents a statistically significant improvement of the fit over a model with a smaller number of dipoles. When a P-value was <0.05, we considered the new dipole as significant. We continued to add a source to the model until the addition of a dipole did not significantly improve the fit.
Sources were superimposed on the individual magnetic resonance images (MRI; 150XT 1.5 T; Shimadzu, Kyoto, Japan). The source location was expressed using an MEG head-based coordinate system. The origin was the midpoint between the pre-auricular points. The x-axis indicated the coronal plane with a positive value in the anterior direction, the y-axis indicated the mid-sagittal plane with a positive value toward the right pre-auricular point and the z-axis indicated the transverse plane pre-auricular to the xy plane with a positive value toward the upper side.
A one-way analysis of variance (ANOVA) followed by Bonferroni/Dunns post hoc test was used for statistical comparisons of the latency among each cortical activity. The statistical significance of the source location was assessed by a discriminant analysis using x, y and z coordinates as variables. P-values < 0.05 were considered to be significant.
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Results |
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In the next step, magnetic fields due to these two sources were subtracted from the recorded data. The subtracted magnetic fields were those that remained to be explained. In the subtracted waveform (Fig. 1Bc), weak deflections around 20 and 30 ms showed a relatively clear field pattern and the best source to explain the waveform was estimated to be in the posterior crown of the precentral gyrus, corresponding to area 4. By adding the area 4 source, %V (at 21 ms) was increased from 94.7 to 99.5% (F = 12.6, P < 0.0001). In the subtracted waveform (Fig. 1Bd), which could not be explained by these three sources, isocontour maps at a latency of 60100 ms constantly showed a single dipole pattern. This source activity was estimated to occur in the upper bank of the Sylvian fissure, corresponding to SII plus adjoining areas (late SII+ source). We referred to this area as SII+ because human MT plus adjoining areas is referred to as MT+. At the peak latency of the late SII+ activity (95 ms), %V was increased from 73.7 to 96.9% (F = 8.7, P < 0.0001). At this step, the mean RV was 4.8%. The waveform of the residual magnetic fields (Fig. 1Be) had several deflections at around 30, 40 and 55 ms, but isocontour maps at these latencies showed a two-dipole pattern. One source was estimated in a region posterior and medial to the area 1 source, around the intraparietal sulcus (posterior parietal cortex, PPC source) and the other near the late SII+ source (early SII+ source: F = 3.1, P = 0.028 at 29 ms; F = 8.5, P < 0.0001 at 39 ms; F = 9.8, P < 0.0001 at 55 ms). After fitting these six sources, the mean RV (0100 ms) was 0.9% and any additional source did not significantly improve the fit. Figure 1D shows the location and orientation of each source. Figure 1C shows the time courses of each source strength and these were used for the analysis of the latency of each activity. In this case, the time course of each source activity showed a similar triphasic pattern.
Similar procedures were applied to data obtained for the remaining 12 subjects. After confirming the precise location of each source in individual MR images, activations in area 3b were identified in all 13 subjects. Sources in area 1, area 4 and PPC were found in 12, nine and eight subjects, respectively. Because two SII+ sources showed an apparently different time course of activity, we analyzed these two activities separately. Both early and late SII+ sources were identified in 10 subjects. In general, all source activities except for the late SII+ activity had two major deflections in opposite directions with a 10 ms interval. Figure 2 shows the time course of each cortical activity of all subjects. The mean onset and peak latencies are shown in Table 1. The onset latency of the area 3b source (14.4 ms) was the shortest but was not different from that of the area 4 source (14.5 ms). The onset latency of the area 3b source was significantly shorter than that of the area 1 source (18.0 ms) and, in turn, the onset latency of the area 1 source was significantly shorter than that of the PPC source (22.4 ms). The onset latency of the early SII+ source was significantly longer than that of the area 3b or area 4 source.
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Discussion |
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The source for the first activities peaking at 21 and 30 ms was located in the posterior bank of the central sulcus, corresponding to area 3b. This finding was consistent with previous somatosensory evoked potential (SEP) and SEF studies demonstrating that the earliest cortical responses to median nerve stimulation originate from area 3b in humans (Wood et al., 1985; Allison et al., 1989
) and monkeys (McCarthy et al., 1991
). The second activity in SI peaking at 25 and 34 ms was located more medial (9 mm), superior (12.7 mm) and posterior (7.2 mm) than the area 3b source, around the anterior crown of the postcentral gyrus, suggesting that this activity originated from area 1. Using intracranial SEP recordings in humans (Allison et al., 1989
) and monkeys (Allison et al., 1991
), it has been demonstrated that a 25/35 ms activity is produced by a radially oriented generator located in the anterior crown of the postcentral gyrus in area 1, in a region
10 mm medial to the region of 3b potentials peaking at 20 and 30 ms. Both the source location and the time course of the activity are consistent with the present results. The onset latency of the area 1 activity was longer by 3.6 ms than that of the area 3b activity. Therefore, our finding was congruent with the serial activations in areas 3b and 1, which is supported by the anatomical finding in monkeys that area 3 projects predominantly into area 1 (Vogt and Pandya, 1978
) and an electrophysiological study in monkeys that showed that ablations of area 3 immediately abolished cutaneous responsivity in area 1 (Garraghty et al., 1990a
). The mean distance between sources in areas 3b and 1 in this study was
17 mm. Given that the synaptic delay is 1 ms, the conduction velocity of this projection is 6.5 m/s (17 mm/2.6 ms). Since there are sparse projections from the thalamus to area 1 (Jones and Powell, 1970
; Nelson and Kaas, 1981
), there might be earlier activities in area 1 that were driven by this direct pathway. However, we could not find earlier activities in this region. As in previous MEG studies in humans, the present study did not detect activities from area 2. This seems largely due to the fact that area 2 is located in the crown of the postcentral gyrus. MEG cannot detect activities from radial dipoles such as those in the crown of gyri. The area 1 activities in this study probably originated from fissural parts of the postcentral gyrus, activities from which would create tangential magnetic components to some extent. However, there remains a possibility that our area 1 activities actually contained activities from area 2.
The third source in the postcentral gyrus was in its caudal-most part around the intraparietal sulcus, probably corresponding to area 5. Although a few previous MEG studies reported activations in this area following somatosensory stimulation at a latency of 50100 ms (Forss et al., 1994; Hoshiyama et al., 1997
), this is the first report to demonstrate the early activities in this region. The onset latency of this activity was significantly longer (4.4 ms) than that of area 1. Since area 5 receives main inputs from areas 1 and 2 (Pons and Kaas, 1986
) and, in turn, area 2 receives inputs mainly from area 1 in monkeys (Vogt and Pandya, 1978
), the responsiveness to cutaneous stimuli of area 5 appears to depend on direct relays from area 1 and area 2 and on a serial relay from area 1 to area 2 and then to area 5.
Regarding the two sources in the lateral sulcus region, we consider these two activities to come from different groups of neurons in this area, since they showed a different source orientation and time course. This notion is consistent with the fact that this region has been divided into at least two parts based on anatomical (Burton et al., 1995) and electrophysiological (Krubitzer et al., 1995
) findings in monkeys and cortical surface (Mima et al., 1997
) and intracortical (Frot and Mauguière, 1999
; Barba et al., 2002
) SEP findings in humans. We considered that our two sources in the lateral sulcus region probably corresponded to SII and PV (parietal ventral area), the regions that have been intensively studied by Krubitzer and colleagues in both animals and humans. PV is a somatosensory area first reported for squirrels (Krubitzer et al., 1986
; Krubitzer and Kaas, 1987
). Electrophysiological studies of the SII region in primates (Krubitzer and Kaas, 1990
; Krubitzer et al., 1995
; Qi et al., 2002
) demonstrated that the region historically referred to as SII is actually composed of at least two separate areas, SII and PV, each of which contains a complete representation of the body surface. In addition, distinct cortico-cortical (Disbrow et al., 2003
) and thalamocortical (Krubitzer and Kaas, 1992
; Disbrow et al., 2002
; Qi et al., 2002
) connections of SII and PV have been studied. These studies have established SII, as well as PV, as one of multiple somatosensory areas of the lateral sulcus in primates. Recently, evidence for SII and PV in humans has been provided in a functional MRI study (Disbrow et al., 2000
).
The peak latencies of the major two components of the early SII+ source were 30 and 40 ms and those of the late SII+ source were 56 and 90 ms, which were very similar to two separable components in the SII region following median nerve stimulation, N30op and N60/P90, in intracortical SEP studies in humans (Frot and Mauguière, 1999; Barba et al., 2002
). The onset latency of the early SII+ source was significantly longer than that of the area 3b source (7.3 ms), suggesting a serial mode of processing in SI and SII+. Given that signals reach the SII region via area 3b with one synaptic transmission, the estimated conduction velocity of this cortico-cortical connection is 4.3 m/s (2.7 cm/6.3 ms). Anatomical (Jones and Powell, 1970
; Friedman et al., 1980
) and electrophysiological (Pons et al., 1987
, 1992; Garraghty et al., 1990b
) studies in monkeys support a serial mode of processing through SI and SII. Findings in previous MEG studies in humans are also consistent with the present results, showing that the somatosensory region in the sylvian fissure is serially activated from SI (Hari et al., 1984
; Elbert et al., 1995
; Disbrow et al., 2001
). However, recent studies in marmosets provided evidence for hierarchical equivalence of SI and SII for tactile processing (Zhang et al., 2001a
,b). Findings in an MEG study (Karhu and Tesche, 1999
) were also in favor of parallel processing in SI and SII showing simultaneous activations in these areas. Therefore, there remains a possibility that we missed weak activities in the SII region prior to those in the present study.
The onset latency of the area 4 source was not different from that of the area 3b source, indicating that the initial activity of this source at least was independent of activities in SI, which was consistent with anatomical findings that projections from area 3b to area 4 were absent or very weak (Vogt and Pandya, 1978; Darian-Smith et al., 1993
; Burton and Fabri, 1995
). We considered that area 4 was driven by thalamic inputs (Ghosh et al., 1987
; Stepniewska et al., 2003
), although later activities of this source might come from area 1 or 2 (Ghosh et al., 1987
; Darian-Smith et al., 1993
; Burton and Fabri, 1995
). Because of the proximity of areas 3a and 4, it is possible that our area 4 activity was actually from area 3a. However, area 3a receives main inputs from deep tissues (Heath et al., 1976
) and our cutaneous stimulation method seems not to be effective at activating deep tissues. In addition, the area 4 source was located more superior (4.4 mm) than the area 3b source in the present study, which also did not support this possibility.
The present results showed that most of the source activities had polarity reversals after 10 ms, that probably corresponded to the surface positivenegative sequence of potentials recorded from the cortex of experimental animals. These positivenegative sequences have been recorded from somatosensory, visual and auditory cortex (for reviews, see Schlag, 1973; Mitzdorf, 1985
) and are often called the primary evoked response (Towe, 1966
). In general, the primary positivity is thought to reflect the initial depolarization of pyramidal cells and proximal apical dendrites, whereas the primary negativity is thought to be a surface reflection of the later depolarization of the distal apical dendrites (Landau, 1967
; Schlag, 1973
; Wood and Allison, 1981
). Under this condition, two successive dipoles with opposite directions occur. By the use of current source density analyses, many animal studies have found, regardless of species or sensory modalities, a combination of an early sink near cortical layer 4 and a corresponding source in layer 5, and a 510 ms later polarity reversed dipole with a sink in layer 2/3 and a source in layer 1 (e.g. Kossut and Singer, 1991
; Steinschneider et al., 1992
; Peterson et al., 1995
; Pearce et al., 2000
).
Although there remains a possibility that all these activations came directly from the thalamus and the different response latency was due to the different conduction velocity of the pathway between the thalamus and each cortical area, the present results together with many previous findings suggest that the main flow of somatosensory processing is serially organized in these areas. In addition, it has been shown in animals that the latency from the thalamus to a cortical cell is remarkably constant across multiple cortical areas, irrespective of the variability of traveling distance (Salami et al., 2003). The present MEG study clearly separated activities in multiple cortical areas and could show the temporal relationship among them. Although it is obvious that single-unit recording studies in conscious animals are important for understanding somatosensory processing, MEG can serve as a noninvasive method to study the timing of arrival of signals to multiple cortical areas in humans.
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Notes |
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Address correspondence to Koji Inui, Department of Integrative Physiology, National Institute for Physiological Sciences, Myodaiji, Okazaki, 444-8585, Japan. Email:inui{at}nips.ac.jp.
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References |
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