Oral structure representation in human somatosensory cortex

Abstract

To clarify the topography of the areas representing whole intraoral structures and elucidate bilateral neuronal projection to those areas in the primary somatosensory (S1) cortex, we recorded somatosensory-evoked magnetic fields (SEFs), which reflect the earliest cortical responses to pure tactile stimulation, using magnetoencephalography and a piezo-driven tactile stimulation device. Subjects consisted of 10 healthy male adults. Following tactile stimulation of 6 sites on the oral mucosa (inferior/superior buccal mucosa, posterior/anterior tongue mucosa, and upper/lower lip mucosa), SEFs with a peak latency of 15 ms (1M) were identified bilaterally. In contrast, SEFs with a peak latency of 30 ms following right index finger tactile stimulation were identified only in the contralateral hemisphere. Equivalent current dipoles (ECDs) generating 15 ms components were found along the posterior wall of the central sulcus, bilaterally. The ECD locations for oral mucosa-representing areas were located inferiorly to those for the index finger, with the following pattern of organization from top to bottom along the central sulcus: index finger, upper or lower lip, anterior or posterior tongue and superior or inferior buccal mucosa, with a wide distribution, covering 30% of the S1 cortex. Source strength for 1M in the ipsilateral hemisphere was weaker than that in the contralateral hemisphere. These results clearly indicate that sensory afferents innervating the intraoral region project to both the contralateral and ipsilateral 3b areas via the trigeminothalamic tract, where contralateral projection is predominant. The results clarify the intraoral structure-representing areas in the S1 cortex, adding those areas to the classical “sensory homunculus”.

Introduction

Functional mapping of the primary somatosensory (S1) cortex in human was first reported by Penfield and Boldrey (1937). The S1 cortex includes area 3b, known as the “somatosensory homunculus”. The foot-, hand-, and trunk-, as well as orofacial- and intraoral-representing areas in the S1 cortex, receive input from peripheral sensory neurons. The results of two earlier studies indicated that cortical representation of orofacial sensation in human was widely distributed over the primary somatosensory cortex, and that this distribution was located more laterally and inferiorly than that for any other body area (Penfield and Boldrey, 1937, Penfield and Rasmussen, 1950).

Using a variety of non-invasive neuroimaging tools such as electroencephalography (EEG), functional-magnetic resonance (functional-MR) imaging and magnetoencephalography (MEG), many authors have reported locations in the S1 cortex for intraoral structures, including the lip (Shöhr and Petruch, 1979, Baumgartner et al., 1992, McCarthy et al., 1993, Hashimoto, 1988, Hoshiyama et al., 1996 Nakamura et al., 1998, Nagamatsu et al., 2000, Disbrow et al., 2003, Nakahara et al., 2004, Murayama et al., 2005, Nevalainen et al., 2006), tongue (Picard and Olivier, 1983, Karhu et al., 1991, McCarthy et al., 1993, Nakamura et al., 1998, Disbrow et al., 2003, Nakahara et al., 2004, Murayama et al., 2005), hard palate (McCarthy et al., 1993, Bessho et al., 2007), teeth (dental pulp) (Kubo et al., 2008), and gingiva (Nakahara et al., 2004, Murayama et al., 2005). However, due to electrical noise contamination and/or small amplitudes in EEG/MEG waveforms, these studies were unable to detect early components, which reflect initial cortical neuronal response, excepting studies on the lip (Nagamatsu et al., 2000) and hard palate (Bessho et al., 2007). Initial cortical responses have been identified at around 10–15 ms following stimulation of various orofacial areas in earlier EEG and MEG studies (Shöhr and Petruch, 1979, Hashimoto, 1988 Baumgartner et al., 1992, McCarthy et al., 1993). In MEG studies, initial cortical responses were generated by anterior–superior-oriented current (Nagamatsu et al., 2000, Bessho et al., 2007).

Somatosensory stimulation of the trigeminal nerve caused bilateral neural activation of the S1 cortex (Nevalainen et al., 2006). The unilateral somatosensory cortex of the facial area can be resected with no serious facial sensory deficit (Penfield and Rasmussen, 1950, Lehman et al., 1994). In addition, bilateral tongue sensation following unilateral direct cortical S1 stimulation in human has been reported (Penfield and Boldrey, 1937, Penfield and Rasmussen, 1950). Although the ascending pathway, from the trigeminothalamic tract to the ipsilateral cortical representation area, for orofacial and intraoral regions from peripheral sensory neurons is not yet fully understood, two possible projection pathways have been proposed: 1) projection from contralateral cortical activity via the corpus callosum, and 2) direct ipsilateral projection via uncrossed ascending fibers. In monkey studies (Jones et al., 1986, Rausell and Jones, 1991a, Rausell and Jones, 1991b, Manger et al., 1996), it has been reported that ipsilateral cortical representation reflects input from the ipsilateral thalamic ventral posteromedial nucleus innervated by the ipsilateral trigeminal nuclei (Manger et al., 1996). Ipsilateral representation occupied 40% of area 3b trigeminal representation, and 40% of the ventral posteromedial nucleus of the thalamus was devoted to representation of ipsilateral intraoral structures (Manger et al., 1996). Bilateral somatosensory-evoked magnetic field (SEF) responses in human S1 cortex following lip and tongue stimulation have been described (Karhu et al., 1991, Hoshiyama et al., 1996, Disbrow et al., 2003, Nevalainen et al., 2006). These showed peak latencies of approximately 30 to 60 ms, with inferior–posterior orientation of equivalent current dipoles (ECDs) in the bilateral S1 cortices (Karhu et al., 1991, Hoshiyama et al., 1996, Nevalainen et al., 2006). This indicates that these responses were not derived from initial direct cortical activity in the ipsilateral hemisphere, as the initial magnetic component would have shown a shorter latency and anteriorly-oriented currents. In an EEG study, bilateral initial cortical responses of somatosensory-evoked potentials (SEPs) following lip tactile stimulation showed a peak latency of approximately 15 ms in both hemispheres, with no significant differences in latencies (Hashimoto, 1988). However, scalp EEG recordings have low spatial resolution of the current source. In addition, functional-MR imaging technique does not have high enough temporal resolution to distinguish initial neuronal activity in the cortex.

Therefore, the aim of the present study was to clarify the functional topography of the areas representing whole intraoral structures, and elucidate bilateral neuronal projection to those areas in the S1 cortex. For this purpose, we recorded SEFs by MEG, which can localize dynamic sources not only with high spatial resolution, but also with very high temporal resolution (Yamamoto et al., 1988, Ribary et al., 1989, Suk et al., 1991, Mogilner et al., 1994).