| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
RESEARCH REPORT |
1 Dental Division, Miyagi National Hospital, Miyagi, Japan;
2 MEG Laboratory, Kohnan Hospital, 4-20-1 Nagamachi-Minami, Taihaku-ku, Sendai 982-8523, Japan;
3 Division of Stomatognathic Physiology and Prosthodontics, Tohoku University Graduate School of Dentistry, Sendai, Japan;
4 Department of Applied Physics, Okayama University of Science, Okayama, Japan; and
5 Department of Neurosurgery, Tohoku University Graduate School of Medicine, Sendai, Japan;
* corresponding author, nak{at}kohnan-sendai.or.jp
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
|---|
KEY WORDS: magnetoencephalography • somatosensory evoked potential • gingiva • lip • tongue
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Functional brain-imaging techniques—such as positron emission tomography (PET) and functional magnetic resonance (fMR) imaging—have identified the sensorimotor areas corresponding to the oral organs (Petersen et al., 1988; Grafton et al., 1991; Wildgruber et al., 1996; Corfield et al., 1999; Lotze et al., 2000; Fox et al., 2001). However, PET or fMR imaging indicates that the activated areas include multiple and extended parts of the brain. In addition, the limited temporal resolution of these techniques cannot separate the pure SI area from the secondary somatosensory cortex, higher sensory cortices, or even the motor cortex.
The somatotopy of the oral SI cortex has been demonstrated by direct cortical stimulation during awake craniectomy surgery (Penfield and Boldrey, 1937; Picard and Olivier, 1983). For example, the face, upper lip, lower lip, tongue tip, and back of the tongue areas are located from superior to inferior in the SI cortex (Penfield and Boldrey, 1937). However, oral SI somatotopy is variable in individuals (Penfield and Boldrey, 1937; Picard and Olivier, 1983). SI somatotopy can also be studied by intracranial recording of somatosensory-evoked potentials (SEPs) (Baumgartner et al., 1992; McCarthy et al., 1993). SEP recording showed general agreement in the medial-to-lateral (superior-to-inferior) representation in the somatosensory cortex of the hand, chin, upper lip, lower lip, tongue, and palate (McCarthy et al., 1993). However, the oral somatotopy was variable and overlapping, and polarity inversion of potentials across the sulcus was a less reliable criterion for trigeminal SEPs. For example, the palatal SI cortex was spatially separated or distributed, as well as variable among subjects. Moreover, these intracranial methods can be used only during brain surgery, and not for normal subjects or patients with oral diseases.
Magnetoencephalography (MEG) is a non-invasive method whereby brain functions can be localized. MEG measures the weak magnetic fields produced by neuronal currents. MEG has excellent temporal resolution (milliseconds) similar to that achieved with electroencephalography (EEG). Moreover, the spatial resolution of MEG is higher than that of scalp EEG, because little distortion is caused by inhomogeneous head conductivity. Somatosensory-evoked magnetic fields (SEFs) for hand and foot stimuli are now well-established and are applied clinically (Sutherling et al., 1988; Baumgartner et al., 1991; Gallen et al., 1993; Kakigi, 1994; Nakasato et al., 1996; Ohtomo et al., 1996; Kawamura et al., 1996; Nakasato and Yoshimoto, 2000; Kumabe et al., 2000; Iwasaki et al., 2001). SEFs for oral organs have been studied only for limited stimulation points, such as the tongue (Karhu et al., 1991; Hari et al., 1993; Yamashita et al., 1999), lip (Hari et al., 1993; Mogilner et al., 1994; Hoshiyama et al., 1996, 1997; Schnitzler et al., 1999; Yamashita et al., 1999; Nagamatsu et al., 2001), and buccal mucosa (Yamashita et al., 1999). The SI somatotopy remains little known (Hari et al., 1993; Mogilner et al., 1994; Hoshiyama et al., 1996; Yamashita et al., 1999).
The present study measured SEFs for the lip, gingiva, and tongue. Stimulation points for each organ were systematically selected to include left vs. right, upper vs. lower, and anterior vs. posterior parts of each organ. The neural source was estimated at the peak latency for each response according to a single equivalent current dipole (ECD) model, which assumes that the measured magnetic field can be most appropriately explained by a single current at one point in the brain. Latency, ECD moments, and ECD location of the SEFs were statistically compared between the stimulation points for evaluation of the functional organization of the oral SI cortex in time and space.
|
MATERIALS & METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
|---|
We induced SEFs by electrical stimulation of the lip, gingiva, and tongue at a total of 24 points using our homemade clip electrode (Fig. 1A
). The points were defined as left or right, upper or lower, and anterior (near the central to lateral incisors) or posterior (near the second premolar to the first molar locations) of the lip mucosa, the lingual side of the gingiva (Fig. 1B), and the tongue. The clip electrode, with a 5-mm inter-electrode distance, was attached to the lip mucosa facing the teeth crowns with the mouth closed, the gingival mucosa at 5 to 10 mm from the gingival edge, and the tongue mucosa at 5 to 10 mm from the lingual edge. Electric stimuli were constant-current biphasic pulses lasting 0.2 ms, delivered at 0.7 Hz, with a tolerable intensity of 2–10 times the sensory threshold. Median nerve SEFs were measured for comparison with the use of an electrical square wave lasting 0.3 ms delivered transcutaneously at 2.8 Hz to the unilateral median nerve (Nagamatsu et al., 2001).
|
) consisting of an array of 102 identical sensor elements distributed over the whole head except the lower face and immersed in liquid helium (Vector View; Neuromag Ltd., Helsinki, Finland). Each sensor element was comprised of two orthogonal planar-type first-order gradiometers with a 13-mm baseline. The MEG measurements were performed in a magnetically shielded room. The subjects lay supine, and we determined the exact location of the head, with respect to the sensor elements, with 3 fiduciary markers by measuring magnetic signals produced by indicator currents passed through coils placed at known locations on the scalp. The positions of the coils with respect to the outer landmarks of the head were obtained by a three-dimensional digitizer. Three-dimensional magnetic resonance (MR) images (Signa Horizon LX ver 8.2; GE Medical Systems, Milwaukee, WI, USA) were obtained in all subjects, with 3 fiduciary markers formed by small oil-containing capsules placed at the same locations on the scalp. The MEG signals were recorded from 50 ms before to 300 ms after the trigger point, filtered from 0.1 to 300 Hz, and digitized at about 1000 Hz. The resulting data were averaged based on recordings from 200 stimuli for the lip, gingiva, tongue, and median nerve.
Bilateral SEF waveforms were recorded, and the contralateral response at the peak latency of 30–100 ms with posterior orientation was used for further analysis. A single dipole model for the SEF data in the contralateral hemisphere to the stimulus side was used for evaluation of the source moment and position. We also used sequential ECD analysis, from -5 ms to +5 ms around the peak at 1-ms intervals, to verify stable ECD estimation within 1-mm distance for each session. The position of the ECD was superimposed on the MR images for correlation with the central sulcus. The relative angles of ECDs were calculated between the oral SEFs and median nerve N20m in the coronal plane of the best-fitting sphere for each subject. This study accepted only ECDs accounting for > 90% of the field variance and with confidence volume < 1 cm3. The single-ECD assumption is well-known to account for peak signals in previous MEG studies of SI response (Karhu et al., 1991; Gallen et al., 1993; Hari et al., 1993; Kakigi, 1994; Kawamura et al., 1996; Nakasato et al., 1996; Ohtomo et al., 1996; Iwasaki et al., 2001; Nagamatsu et al., 2001). Therefore, we used the single-ECD model for the hemispheric data contralateral to the stimulus side.
Two statistical analyses were performed. The latency, ECD moments, and relative ECD angles of all subjects were compared among the anterior-upper, anterior-lower, posterior-upper, and posterior-lower stimulus points for each organ. The dipole parameters were averaged over 8 stimulus points, and the overall averages of dipole parameters were compared among the lip, gingiva, and tongue. The paired t test was used, and data were considered significant at P < 0.01.
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
|---|
. All ECD dipoles were estimated to be located on the central sulcus, based on the MR images of individual subjects.
|
). Significant differences were found as follows: The latency of the gingival SEFs was shorter than the latencies for the tongue and lip; the dipole moment of the gingival SEFs was smaller than that of the lip; the ECD position of the lip SEFs was superior to those of the tongue and gingiva; and the ECD position for the anterior upper stimulus of the tongue was lower than those of the anterior lower and posterior lower stimuli.
|
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
|---|
The first SI response of the lip SEF, cN15m, has an anterior-oriented current with a peak latency around 15 ms (Nagamatsu et al., 2001). The cN15m has small amplitude, so previous studies of trigeminal SEFs have focused on the later components with posterior currents and peak latencies of 20 to 60 ms (Karhu et al., 1991; Hari et al., 1993; Mogilner et al., 1994; Hoshiyama et al., 1996). The present study also used cP55m for comparison, since the cN15m was not observed among the gingival SEFs. The latency of the gingival cP55m was significantly shorter than those of the lip or tongue cP55m. Latency differences in these trigeminal SEFs can be explained by the peripheral conduction time, including transmission time, at the peripheral mechanoreceptors; the central conduction time from the pons to the SI cortex; and the central processing time within the cortex, i.e., the inter-peak latency between cN15m and cP55m. The peripheral conduction time in lip SEFs was estimated at about 2.1 ms, which cannot explain the shorter latency (about 6 ms) of the gingival cP55m (Nagamatsu et al., 2001). Central conduction time from the pons to the SI cortex must be the same for all trigeminal systems. Therefore, we believe that the central processing time must be shorter for gingival SEFs than for lip or tongue SEFs. In addition, our subjects, including the two dentists among the authors (HN and SM), felt a tooth-tap sensation during stimulus of the gingiva, suggesting that both the mucosa and the periodontium were stimulated. Somatosensory information from the gingiva or periodontium may undergo rapid processing within the SI cortex in humans.
The dipole moment of the gingival cP55m was significantly smaller than that of the tongue cP55m. The small moment of the gingival SEFs may indicate that only a small number of neurons is excited. However, the cortical representation was unexpectedly large for the palatal gum stimulus compared with the lip or tongue stimulus in humans (McCarthy et al., 1993). This observation and our present results suggest a lower density of excited neurons over the widely distributed gingival SI cortex.
All cP55m dipoles for the gingiva, lip, and tongue were localized on the central sulcus. The lip dipole was significantly superior to the gingival and tongue dipoles, whereas the gingival and tongue dipoles were very close. Differences in ECD positions were negligible between anterior and posterior stimuli, and between upper and lower stimuli within the same organ, except that the ECD for the anterior upper tongue stimulus was significantly lower than the ECD for the lower tongue stimulus.
The somatotopy of the oral SI cortex is generally agreed to locate the lip SI superior and medial to the tongue SI cortex (Penfield and Boldrey, 1937; Hari et al., 1993; McCarthy et al., 1993; Yamashita et al., 1999). However, the findings of the somatotopy differ for the other oral organs as well as the different parts of each organ. The well-known "homunculus" map of the SI cortex shows that the upper lip area is drawn superior to the lower lip area (Penfield and Boldrey, 1937). However, the relative functional anatomy between the upper and lower lip areas was not described. Moreover, the original mapping of the cortical stimulation points (Penfield and Boldrey, 1937) shows variable and wide distribution of the oral sensory responses. Previous SEF studies (Mogilner et al., 1994; Hoshiyama et al., 1996, 1997; Yamashita et al., 1999) have suggested that the upper lip SI is superior to the lower lip SI. However, these studies provided no statistical evidence. Our present results, together with those from a previous study (Hari et al., 1993), indicate that there is no fixed organization of the oral SI somatotopy except for general agreement for the lip and tongue areas.
The present study shows that MEG provides a non-invasive method for the investigation of function in human intra-oral structures, including the gingiva, with high spatial and temporal resolutions.
|
ACKNOWLEDGMENTS |
|---|
Received August 6, 2003; Last revision January 22, 2004; Accepted January 22, 2004
|
REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Baumgartner C, Barth DS, Levesque MF, Sutherling WW (1992). Human hand and lip sensorimotor cortex as studied on electrocorticography. Electroencephalogr Clin Neurophysiol 84:115–126.[ISI][Medline]
Corfield DR, Murphy K, Josephs O, Fink GR, Frackowiak RS, Guz A, et al. (1999). Cortical and subcortical control of tongue movement in humans: a functional neuroimaging study using fMRI. J Appl Physiol 86:1468–1477.
Fox PT, Huang A, Parsons LM, Xiong JH, Zamarippa F, Rainey L, et al. (2001). Location-probability profiles for the mouth region of human primary motor-sensory cortex: model and validation. Neuroimage 13:196–209.[ISI][Medline]
Gallen CC, Sobel DF, Waltz T, Aung M, Copeland B, Schwartz BJ, et al. (1993). Noninvasive presurgical neuromagnetic mapping of somatosensory cortex. Neurosurgery 33:260–268.[ISI][Medline]
Grafton ST, Woods RP, Mazziotta JC, Phelps ME (1991). Somatotopic mapping of the primary motor cortex in humans: activation studies with cerebral blood flow and positron emission tomography. J Neurophysiol 66:735–743.
Hari R, Karhu J, Hamalainen M, Knuutila J, Salonen O, Sams M, et al. (1993). Functional organization of the human first and second somatosensory cortices: a neuromagnetic study. Eur J Neurosci 5:724–734.[ISI][Medline]
Hoshiyama M, Kakigi R, Koyama S, Kitamura Y, Shimojo M, Watanabe S (1996). Somatosensory evoked magnetic fields following stimulation of the lip in humans. Electroencephalogr Clin Neurophysiol 100:96–104.[Medline]
Hoshiyama M, Kakigi R, Koyama S, Watanabe S, Shimojo M (1997). Activity in posterior parietal cortex following somatosensory stimulation in man: magnetoencephalographic study using spatio-temporal source analysis. Brain Topogr 10:23–30.[ISI][Medline]
Iwasaki M, Nakasato N, Kanno A, Hatanaka K, Nagamatsu K, Nagamine Y, et al. (2001). Somatosensory evoked fields in comatose survivors after severe traumatic brain injury. Clin Neurophysiol 112:205–211.[ISI][Medline]
Kakigi R (1994). Somatosensory evoked magnetic fields following median nerve stimulation. Neurosci Res 20:165–174.[ISI][Medline]
Karhu J, Hari R, Lu ST, Paetau R, Rif J (1991). Cerebral magnetic fields to lingual stimulation. Electroencephalogr Clin Neurophysiol 80:459–468.
Kawamura T, Nakasato N, Seki K, Kanno A, Fujita S, Fujiwara S, et al. (1996). Neuromagnetic evidence of pre- and post-central cortical sources of somatosensory evoked responses. Electroencephalogr Clin Neurophysiol 100:44–50.[Medline]
Kumabe T, Nakasato N, Inoue T, Yoshimoto T (2000). Primary thumb sensory cortex located at the lateral shoulder of the inverted omega-shape on the axial images of the central sulcus. Neurol Med Chir (Tokyo) 40:393–403.
Lotze M, Seggewies G, Erb M, Grodd W, Birbaumer N (2000). The representation of articulation in the primary sensorimotor cortex. Neuroreport 11:2985–2989.[ISI][Medline]
McCarthy G, Allison T, Spencer DD (1993). Localization of the face area of human sensorimotor cortex by intracranial recording of somatosensory evoked potentials. J Neurosurg 79:874–884.[ISI][Medline]
Mogilner A, Nomura M, Ribary U, Jagow R, Lado F, Rusinek H, et al. (1994). Neuromagnetic studies of the lip area of primary somatosensory cortex in humans: evidence for an oscillotopic organization. Exp Brain Res 99:137–147.[ISI][Medline]
Nagamatsu K, Nakasato N, Hatanaka K, Kanno A, Iwasaki M, Yoshimoto T (2001). Neuromagnetic localization of N15, the initial cortical response to lip stimulus. Neuroreport 12:1–5.[ISI][Medline]
Nakasato N, Yoshimoto T (2000). Somatosensory, auditory, and visual evoked magnetic fields in patients with brain diseases. J Clin Neurophysiol 17:201–211.[ISI][Medline]
Nakasato N, Seki K, Kawamura T, Fujita S, Kanno A, Fujiwara S, et al. (1996). Functional brain mapping using an MRI-linked whole head magnetoencephalography (MEG) system. Electroencephalogr Clin Neurophysiol 46(Suppl):119–126.
Ohtomo S, Nakasato N, Kawamura T, Kanno A, Seki K, Fujita S, et al. (1996). Correspondence of anatomy and function in the human digit sensory cortex revealed by an MRI-linked whole-head MEG system. Electroencephalogr Clin Neurophysiol 47(Suppl):91–95.
Penfield W, Boldrey E (1937). Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain 60:389–443.
Petersen SE, Fox PT, Posner MI, Mintun M, Raichle ME (1988). Positron emission tomographic studies of the cortical anatomy of single-word processing. Nature 331:585–589.[Medline]
Picard C, Olivier A (1983). Sensory cortical tongue representation in man. J Neurosurg 59:781–789.[ISI][Medline]
Schnitzler A, Volkmann J, Enck P, Frieling T, Witte OW, Freund HJ (1999). Different cortical organization of visceral and somatic sensation in humans. Eur J Neurosci 11:305–315.[ISI][Medline]
Sutherling WW, Crandall PH, Darcey TM, Becker DP, Levesque MF, Barth DS (1988). The magnetic and electric fields agree with intracranial localizations of somatosensory cortex. Neurology 38:1705–1714.
Wildgruber D, Ackermann H, Klose U, Kardatzki B, Grodd W (1996). Functional lateralization of speech production at primary motor cortex: a fMRI study. Neuroreport 7:2791–2795.[ISI][Medline]
Yamashita H, Kumamoto Y, Nakashima T, Yamamoto T, Inokuchi A, Komiyama S (1999). Magnetic sensory cortical responses evoked by tactile stimulations of the human face, oral cavity and flap reconstructions of the tongue. Eur Arch Otorhinolaryngol 256(Suppl 1):S42–S46.
This article has been cited by other articles:
|
|
 |
|
  K. Kubo, Y. Shibukawa, M. Shintani, T. Suzuki, T. Ichinohe, and Y. Kaneko Cortical Representation Area of Human Dental Pulp J. Dent. Res., April 1, 2008; 87(4): 358 - 362. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Bessho, Y. Shibukawa, M. Shintani, Y. Yajima, T. Suzuki, and T. Shibahara Localization of Palatal Area in Human Somatosensory Cortex J. Dent. Res., March 1, 2007; 86(3): 265 - 270. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. J. Miyamoto, M. Honda, D. N. Saito, T. Okada, T. Ono, K. Ohyama, and N. Sadato The Representation of the Human Oral Area in the Somatosensory Cortex: a Functional MRI Study Cereb Cortex, May 1, 2006; 16(5): 669 - 675. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| IADR Journals | Advances in Dental Research ® |
| Journal of Dental Research ® | Critical Reviews (1990-2004) |
