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. 2007 Nov 2;30(1):92–100. doi: 10.1002/hbm.20488

Time‐dependent hemispheric shift of the cortical control of volitional swallowing

Inga K Teismann 1,2,†,✉, Rainer Dziewas 2,†, Olaf Steinstraeter 1, Christo Pantev 1
PMCID: PMC6870608  PMID: 17979116

Abstract

An important part of the cortical processing of swallowing takes place in the sensorimotor cortex, predominantly in the left hemisphere. However, until now, only deglutition related brain activation with low time resolution exceeding a time interval of 1 s has been reported. In this study, we have examined the chronological sequence of cortical swallowing processing in humans by means of high temporal resolution magnetoencephalography (MEG). The cortical MEG activity was recorded during self‐paced volitional swallowing in 10 healthy subjects. Data were analyzed using synthetic aperture magnetometry and the group analysis was performed using a permutation test. Swallowing‐related muscle activity was recorded by electromyography. Within the time interval of 1 s of the most pronounced muscular swallowing execution, the MEG analysis revealed neural activation in the primary sensorimotor cortex. During the first 600 ms, only left hemispheric activation was found, bihemispheric activation during the next 200 ms and a right hemispheric activation during the last 200 ms. Thus, our results demonstrate a time‐dependent shift of neural activation from left to right sensorimotor cortex during deglutition with left hemispheric dominance in the early stage of volitional swallowing and right hemispheric dominance during its later part. Hum Brain Mapp 2009. © 2007 Wiley‐Liss, Inc.

Keywords: lateralization, swallowing, somatosensory cortex, MEG, synthetic aperture magnetometry, time‐dependence

INTRODUCTION

Various functional and structural asymmetries in the human cerebral cortex are known [Geschwind and Galaburda, 1985]. Likely one of the best‐known asymmetries is the lateralization of language function to the left hemisphere for the majority of right‐handed subjects. Hemispheric differences were also found for other higher cognitive functions [Federmeier and Benjamin, 2005; Natale et al., 1983] and in the motor system [Yan et al., 2006]. Most of these studies described lateralization in terms of amplitude differences in electroencephalography (EEG) and magnetoencephalography (MEG) experiments or different extents of cortical activation using PET or functional MRI without discussing latency differences.

Swallowing is a complex action involving 5 cranial nerves and 50 different smooth and skeletal muscles. Both the brainstem and cortical areas are involved in the central coordination of swallowing. In the last few years, an increasing number of studies have examined cortical activation related to human swallowing by means of different neuroimaging methods (MEG, fMRI, PET, TMS, and EEG). Across studies, a bilateral activation of the precentral and postcentral gyrus has been consistently found [Dziewas et al., 2003; Hamdy, et al., 1996, 1999; Hartnick et al., 2001; Zald and Pardo, 1999]. Majority of these studies also found hemispheric asymmetries, suggesting different roles of the two hemispheres in distinct phases of deglutition [Daniels et al., 1996, 2006; Hamdy et al., 1996; Robbins et al., 1993]. None of these studies, however, focused on the chronological sequence of cortical processing of human swallowing, but rather principally on its localization.

A major problem in investigating the cortical processing of swallowing with EEG or MEG is caused by the fact that swallowing does not result in evoked cortical potentials due to the intraindividual and interindividual variable duration of swallowing phases. Instead, swallowing like other voluntary movements, results in circumscribed frequency changes. These types of changes are time‐locked to the event but not phased‐locked and thus cannot be extracted by simple linear methods, such as averaging, but may be detected by time‐frequency analysis [Pfurtscheller and Lopes da Silva, 1999]. This might be due to a decrease or increase in synchrony of the underlying neuronal populations, otherwise known as event‐related desynchronization (ERD) [Pfurtscheller, 1977, 1992; Pfurtscheller and Aranibar, 1977] or synchronization (ERS) [Pfurtscheller, 1992].

In MEG synthetic aperture magnetometry (SAM) is used to analyze the frequency changes. SAM is a minimum‐variance beamformer with an integrated step for the estimation of dipole orientation [Robinson and Vrba, 1999]. In contrast to other MEG source localization methods, beamforming does not rely on averaging and therefore allows the analysis of evoked and induced brain activity. Like fMRI, SAM calculates volumetric maps of brain activation and allows the application of similar paradigms. While fMRI monitors changes in blood flow with the BOLD effect MEG directly measures neuronal activity. The same cortical areas were active comparing MEG studies analyzed with SAM and fMRI studies using the same stimulation paradigm [Hirata et al., 2002; Taniguchi et al., 2000].

Voluntary movement is known to result in desynchronizations in the upper alpha and lower beta band, localized close to sensorimotor areas [Derambure et al., 1993; Pfurtscheller and Aranibar, 1979; Pfurtscheller and Berghold, 1989; Stancak and Pfurtscheller, 1996]. These ERDs have also been reported in different swallowing studies before [Dziewas et al., 2003; Furlong et al., 2004; Teismann et al., 2007].

In this study we investigated the temporal characteristics of human swallowing in healthy subjects by means of whole‐head MEG and SAM. We focused on the chronological sequence of its cortical processing.

SUBJECTS AND METHODS

Subjects

Ten healthy right‐handed volunteers (8 males and 2 females, age range 22–60 years, mean 35.9 years) served as subjects. The local ethics committee approved the protocol of the study and informed consent was obtained from each subject after the nature of the study was explained in accordance to the principles of the Declaration of Helsinki.

Intra‐Oral Infusion

To facilitate volitional swallowing during MEG recording, water was infused into the oral cavity via a flexible plastic tube 4.7 mm in diameter attached to a fluid reservoir. The reservoir bag was positioned about 1 m above the mouth of each subject when seated. The tip of the tube was placed in the corner of the mouth between the buccal part of the teeth and the cheek. The tube was gently fixed to the skin with tape. The side chosen for tube placement was alternated between subjects. The infusion flow was individually adjusted to the subject's request and ranged between 8 and 12 ml/min. The aim was to establish a swallowing frequency of 4–6 times per minute.

MEG Recording

During 15 min of MEG recording, the subject swallowed in a self‐paced manner, without external cueing. Swallowing acts were recorded and identified by electromyographic recording. MEG data were collected using a whole head 275‐channel SQUID sensor array (Omega 275, CTF Systems) housed in a magnetically shielded room. Magnetic fields were recorded with a sample frequency of 600 Hz. The data were filtered during acquisition using a 150 Hz low‐pass filter. Recordings were performed while subjects were seated in a comfortable upright position and watching a silent movie of their choice.

Electromyography Recording

Surface electromyography (EMG) was measured with two pairs of bipolar skin electrodes (Ag‐Ag‐Cl) placed on the submental muscle groups [Vaiman et al., 2004]. The electrodes were connected to a bipolar amplifier (DSQ 2017E EOG/EMG system, CTF Systems, Canada) and the nominal gain was set at 1.

Anatomical MRI

MRI data were acquired on a 3.0 T Scanner (Gyroscan Intera, Philips Medical Systems, Best, The Netherlands) with a standard head coil. The 3D isotropic T1w dataset of the whole head had a measured voxel size of 1.0 mm edge length. A Turbo Field‐echo‐technique in sagittal slice orientation with 3D acquisition was used, i.e., phase encoding in two directions (ap and slice encoding direction lr); FOV 256 mm × 205 mm × 160 mm (frequency encoding × phase encoding × slice encoding in fh/ap/lr direction), measured matrix 256 × 205 × 160, reconstructed after zero filling to 512 × 410 × 320, i.e., reconstructed edge length 0.5 mm; contrast was defined by TR = 7.4 mm, TE = 3.4 ms, FA= 9°, an inversion recovery pre‐pulse every 805 ms = every 102 acquisitions, one saturation slab caudal to the acquired volume. Acquisition bandwidth per pixel was 217.1Hz, total bandwidth 55.578 kHz, with two signal averages total acquisition time was 11:01 min.

Data Analysis

Each individual's EMG signal was used to mark the beginning of main muscle activation (M 1) and the end of the task‐specific muscle activity (M 2) for every single swallow. The beginning of the main muscle activation was defined as an enduring >100% increase in amplitude or frequency of the EMG signal after an initial increase of more than 50% of EMG activity defining the onset of swallowing preparation. The end of task‐specific muscle activity was defined as a decrease in amplitude or frequency of the EMG signal greater than 50%. To estimate the maximal null distribution (see below), a third marker was set to distinguish background activity from the onset of swallowing preparation (M 0). For analysis of the whole swallowing execution, phase time intervals were defined as follows (see Fig. 1):

  • 1

    1 s Execution stage: −0.4 to 0.6 s in reference to M 1.

  • 2

    1 s Resting stage: 0 to 1 s in reference to M 2.

  • 3

    1 s Background active: −2 to −1 s in reference to M 0.

  • 4

    1 s Background control: −1 to 0 s in reference to M 0.

Figure 1.

Figure 1

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Definition of the swallowing execution and resting stage of swallowing‐related muscle activity. The EMG recording of one swallowing act is shown (surface electrodes, recording from the submental muscles). For the 1 s analysis of the whole swallowing phase with SAM, the beginning (M 1) and the end (M 2) of main muscle activation were marked. The swallowing execution phase and the corresponding resting phase were defined. To estimate the maximal null distribution a third marker (M 0) at the beginning of task‐specific muscle activity was set and two background phases were defined (Methods). [Color figure can be viewed in the online issue, which is available at www.interscience.wiley.com.]

To examine the chronological sequence of brain activation, the execution stage was divided into five parts, each lasting 200 ms. Time intervals for the subsequent analysis were defined as follows (see Fig. 2):

  • 1

    200 ms Execution stage 1 (E1): −0.4 to −0.2 s in reference to M 1.

  • 2

    200 ms Execution stage 2 (E2): −0.2 to 0.0 s in reference to M 1.

  • 3

    200 ms Execution stage 3 (E3): 0.0 to 0.2 s in reference to M 1.

  • 4

    200 ms Execution stage 4 (E4): 0.2 to 0.4 s in reference to M 1.

  • 5

    200 ms Execution stage 5 (E5): 0.4 to 0.6 s in reference to M 1.

  • 6

    200 ms Resting stage (R): 0 to 0.2 s in reference to M 2.

  • 7

    200 ms Background active (B1): −0.4 to −0.2 s in reference to M 0.

  • 8

    200 ms Background control (B2): −0.2 to 0 s in reference to M 0.

Figure 2.

Figure 2

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To analyze the cortical activation within the early and later stages of the execution phase, this 1 second interval is divided into five successive 200 ms time intervals (E1–E5). The corresponding resting stage (R) and two background stages (B1 and B2) are also shortened to 200 ms (Methods). [Color figure can be viewed in the online issue, which is available at www.interscience.wiley.com.]

MEG data were filtered at five different frequency bands: theta (4–8 Hz), alpha (8–13 Hz), beta (13–30 Hz), low gamma, (30–60 Hz), and high gamma (60–80 Hz). From the filtered MEG data, SAM was used to generate a 20 × 20 × 14 cm3 volumetric pseudo‐t images [Vrba and Robinson, 2001] with 3 mm voxel resolution for all five frequency bands. A pseudo‐t value cancels the common‐mode brain activity by subtracting the source power found in a defined control stage from the source power in the active stage. To account for uncorrelated sensor noise, this difference is normalized by the mapped noise power [Vrba and Robinson, 2001]. Data from the execution stages described earlier were used to analyze cortical activity during the different time intervals. The corresponding resting stage served as a control. The required similarity between the resting stage and the two background stages Group analyses were performed in the manner previously published by [Chau et al., 2004]. Briefly, the individual MRIs were first normalized by transforming them into a common anatomical space using SPM2. Then, spatially normalized activation maps were obtained by applying this transformation to the individual SAM volumes.

For analysis of single conditions, the significance of activated brain regions was assessed by the permutation test method described by Chau et al. [2004]. The maximal null distribution was estimated by comparing Background stage 1 (active) and 2 (control) [Chau et al., 2004; Nichols and Holmes, 2002]. For the comparison of conditions to each other, a standard permutation test for paired samples was performed [Nichols and Holmes, 2002]. Hemispheric lateralization concerning the five different time intervals of swallowing related activation was quantified using a lateralization index (LI), which was calculated as (L − R)/(L + R), where L and R are the cumulative pseudo‐t activation in the somatosensory cortex (BA 3, 1, and 2, according to the Talairach atlas) of the left and right hemisphere, respectively. A positive LI indicates left hemispheric lateralization, while a negative LI indicates stronger right hemispheric activation. Ratios around 0 represent indeterminate dominance, 1, respectively −1 are indicating unilateral activation [Dziewas et al., 2003; Yetkin et al., 1995].

To confirm the chosen frequency band and to emphasize our SAM results wavelet analysis of the active areas during execution stage and resting stage were performed. These time‐frequency plots of parieto‐frontal channels were determined for both hemispheres and averaged across all 10 subjects.

RESULTS

No coughing or signs of aspiration occurred during MEG measurements. EMG recordings showed swallowing‐related muscle activity. A sufficient number of swallows were recorded in all 10 subjects, ranging from 37 to 101 within the 15 min of MEG recording. Less than 4% of the trials were rejected due to overlap between the “1 s Execution stage” and the “1 s Resting stage” or between the “1 s Background control” and the “1 s Execution stage” of the subsequent swallow (see Table I).

Table I.

Characteristics of subjects and the number of swallows before and after rejection are shown

Subject Age Sex Swallows After rejection
1 34 M 93 93
2 56 M 39 38
3 34 M 46 44
4 24 M 67 62
5 60 M 58 53
6 47 M 71 70
7 36 M 61 58
8 23 W 37 37
9 23 W 62 58
10 22 M 101 99
Mean 35.9 63.5 61.2
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Swallows were recorded with the help of EMG. Less then 4% of the trials had to be rejected due to an overlap between different intervals (Methods).

In the analysis of the whole swallowing execution phase, all subjects showed ERDs in the beta frequency band in the primary sensorimotor cortex. In the other frequency bands and other cortical areas, no systematic ERDs or ERSs were observed. Comparison of the “1 s Resting stage” and the “1 s Background control” showed no significant event‐related changes. In the following ERD and activation are going to be used synonymously.

Group analysis of the whole swallowing execution phase (1 s) revealed significant ERDs of rhythmic brain activity (P < 0.05) in the beta frequency band bilaterally in Brodman areas (BA) 4, 3, 1, and 2, with a slight left hemispheric lateralization (pseudo‐t value in the right hemisphere: −0.343, in the left hemisphere: −0.412) (see Fig. 3). The other frequency bands (alpha, high and low gamma, and theta) showed no significant event‐related cortical activations during the swallowing execution phase.

Figure 3.

Figure 3

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Event‐related desynchronizations in the beta frequency band (13–30 Hz) during the 1 s execution phase of volitional swallowing. Significant activation in the group analysis is shown (P < 0.05). The color bar represents the t‐value.

Separate calculations of the SAM results for each 200 ms interval resulted in ERDs of rhythmic brain activity in sensorimotor cortex for all individuals and intervals. No systematic activation was found in any other cortical area or frequency band.

Group analysis of the 200 ms intervals revealed significant ERDs in the beta frequency band in the sensorimotor cortex in all five time intervals (P < 0.05). A strong left hemispheric lateralization of activation was found during the first three movement stage intervals (0–600 ms). This effect was quite small within the first 200 ms (LI: 0.38). It increased in the second 200 ms interval and even more in the third interval (LI: 1). In the fourth movement stage interval (600–800 ms), bihemispheric activation of the sensorimotor cortex was found (LI: −0.07) and a right hemispheric lateralization is seen in the last 200 ms of the swallowing execution phase (800–1000 ms; LI: −0.49) (see Fig. 4, Table II).

Figure 4.

Figure 4

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Event‐related desynchronizations in the beta frequency band during the five successive 200 ms time intervals of the swallowing execution phase. Significant activation in the group analysis is shown (P < 0.05). The color bar represents the t‐value.

Table II.

Demonstration of the hemispheric shift of activation over time

Time window E1 E2 E3 E4 E5
Sum of significant pseudo‐t values right hemisphere −2.6494 0 0 −55.1507 −9.4685
Sum of significant pseudo‐t values left hemisphere −5.8861 −1.9097 −18.8312 −50.7963 −3.2234
Lateralization index of pseudo‐t activation 0.3792 1 1 −0.0411 −0.4921
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The group results of cumulative significant pseudo‐t activation are shown for all five time intervals and in both hemispheres. The first three time windows (E1–E3) reveal left hemispheric lateralization. In E2 and E3 even no significant ERD was found in the right hemisphere. This results in a lateralization index of 1. The time interval E4 shows bilateral activation with slight right hemispheric lateralization that accelerates in the last observed time interval (E5).

Time‐frequency wavelet plots calculated for the active parieto‐frontal cortical areas in all 10 subjects revealed a strong beta ERD during swallowing execution in both hemispheres compared with resting stage. While the strongest reduction of beta activation emerged in E3 in the left hemisphere, the corresponding decrease was found later (E4, E5) in the right hemisphere (see Fig. 5).

Figure 5.

Figure 5

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Time‐frequency wavelet plots were derived from the parieto‐frontal channels of both hemispheres. Averaged time‐frequency plots of each subject were then averaged across the group to provide a group mean time‐frequency plot. Time 0 on the x‐axis corresponds to the individually set markers (M 1 for the execution stage, M 2 for the resting stage). Please note that the time scale is differing between the execution stage and the resting stage. Colors represent the level of frequency power, with lower numbers (blue) indicating a decrease in power (ERD) and higher numbers (red) an increase in power (ERS).

According to the time‐frequency plot results showing the strongest changes in the higher alpha and lower beta band, additional SAM calculations (10–20 Hz and 13–20 Hz) were performed. Here again ERDs in somatosensory areas were found. The localization of group as well as single results did not differ between these additionally analyzed frequency ranges and the initial beta band results, with a slightly reduced maximum ERD in the newly calculated frequencies.

DISCUSSION

This study is, to our knowledge, the first to show a time‐dependent shift of cortical activation from the left to right hemisphere during volitional swallowing in humans. Thus, while only left hemispheric ERDs were seen during the first 600 ms of swallowing, the activation began to shift thereafter to the right somatosensory cortex leading to bilateral activation between 600 and 800 ms after swallowing‐onset and ending in a strongly right lateralized activation. Concordant results were found in time‐frequency wavelet plots and SAM analysis.

Functional and anatomical hemispheric asymmetry is a frequent observation in human brain research. In the somatosensory system, hemispheric asymmetry has been shown with use of such techniques as MEG [Soros et al., 1999], SEP [Jung et al., 2003] and near‐infrared diffusing‐wave spectroscopy [Li et al., 2005]. Asymmetries have been observed in both localization [Wikstrom et al., 1997] and source strength [Rossini et al., 1994] for somatosensory evoked fields. An fMRI study demonstrated a predominant role of the left supplementary motor area in right‐handed subjects in the control of voluntary movements [Babiloni et al., 2003]. All of these studies focused on asymmetries in the extent of cortical activation or interhemispheric amplitude differences but little has been reported thus far concerning the temporal dynamics in human brain asymmetries. In one of the rare studies about latency differences, Suzuki et al. [1997] and Kanno et al. [1996] found faster right hemispheric processing for pure tones compared to the left hemisphere in subjects with left as well as right hemispheric language dominance [Kanno et al., 1996; Suzuki et al., 1997]. In other studies, faster processing in the left hemisphere has been shown for complex visual stimuli [Okubo and Nicholls, 2005] while there was no interhemispheric difference in the latency of visual evoked potentials like the N100 [Abe and Kuroiwa, 1990]. In the somatosensory system, evoked magnetic responses to median nerve stimulation did not show hemispheric asymmetries as a function of latency (20, 30, 50, 70, 90, and 150) [Theuvenet et al., 2005].

In what concerns human swallowing, several studies found hemispheric asymmetries related to the extent of activation which suggested different roles for the hemispheres [Hamdy et al., 1996]. Several studies found a left hemispheric dominance [Dziewas et al., 2003; Martin et al., 2004; Mosier et al., 1999] while others support the hypothesis of a handedness‐independent lateralization [Hamdy et al., 1996, 1999; Martin et al., 2007].

To date, only one study has described the temporal characteristics of cortical activation during human swallowing. In an MEG study, Furlong et al. [2004] examined the temporal patterns of swallowing activation through time‐frequency plots using wavelet analysis and showed ERD bilaterally in the sensorimotor cortex in the beta frequency band during human swallowing with a marked reduction of the ERD at the beginning of the volitional swallowing phase [Furlong et al., 2004]. Unlike our study, Furlong et al., instructed their subjects to swallow in response to a visual stimulus and no EMG was recorded to precisely monitor swallowing related‐muscle activity. In spite of these differences in experimental design, which make a comparison with our own findings rather difficult, the disappearance of ERD in the left somatosensory cortex about 2 s after onset of the visual stimulus is consistent with the activation shift from the left to right hemisphere reported in our study.

In the interpretation of such a clear left hemispheric lateralization in early swallowing processing, a link to language lateralization seems likely. It is evident that several of the skeletal muscles used for language production are also used for volitional swallowing [Clark, 2003]. These are the same groups of muscles affected in patients with dysarthria and dysphagia and both syndromes often occur together in stroke patients [Mann et al., 1999].

Another explanation of our results is suggested by studies showing that the left hemisphere plays a major role in the oral phase (volitional) component of the swallowing act, while the right hemisphere dominantly coordinates the pharyngeal stage [Daniels et al., 2006]. Left hemispheric stroke often results in buccofacial, speech, and swallowing apraxia [Robbins and Levin, 1988] leading to extended oral transfer times [Robbins et al., 1993]. Therefore the coordination of labial, lingual and mandibular musculature during bolus transfer seems to be aligned by the left hemisphere [Daniels, 2000]. This is supported by an MEG brain imaging study finding a left hemispheric specialization of mirror neurons regarding movements of the temporomandibular joint. Healthy subjects showed left lateralized activation in the inferior parietal cortex, the anterior part of the inferior‐lateral precentral gyrus and the occipitotemporal region during movement observation of symmetrical jaw‐opening [Shibukawa et al., 2007]. The same group found no hemispheric specialization in jaw movement preparation [Shibukawa et al., 2004]. Less is know about movement specialization of the right hemisphere. It is supposed to be predominant in movement planning [Barthelemy and Boulinguez, 2001, 2002] and shows faster reaction times [Sturm et al., 1989]. Patients with right hemispheric cortical strokes of the middle cerebral artery showed a longer pharyngeal stage duration and higher incidence of laryngeal penetration and aspiration than patients with left hemispheric stroke [Robbins et al., 1993]. Corroborating these findings, another study showed that right hemispheric damage led to dysfunction and dysmotility in the pharyngeal stage of deglutition [Daniels et al., 1996]. All these results are in line with our findings showing a left hemispheric lateralization in the early stage of volitional swallowing and a distinct right hemispheric lateralization in cortical processing in the later part of deglutition corresponding. We suppose that the early left hemispheric activation might reflect the cortical activation during the oral swallowing phase while the later right hemispheric activation corresponds to the pharyngeal phase. The reason for this hemispheric specialization of different phases of deglutition is unknown. Anyhow, this knowledge might help to prognosticate the course of dysphagia after stroke and to adjust swallowing therapy.

Taken together, our results show a time‐dependent shift of cortical activation from left to right sensorimotor cortex during volitional swallowing. These findings support the hypothesis that the hemispheres play different roles in the coordination of deglutition.

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