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Neurology of swallowing

Article in Clinical Neurophysiology January 2004

Impact Factor: 3.1 DOI: 10.1016/S1388-2457(03)00237-2 Source: PubMed


160 176

2 authors, including:

Cumhur Ertekin
Ege University


All in-text references underlined in blue are linked to publications on ResearchGate, Available from: Cumhur Ertekin
letting you access and read them immediately. Retrieved on: 18 July 2016
Journal of Electromyography and Kinesiology 23 (2013) 619626

Contents lists available at SciVerse ScienceDirect

Journal of Electromyography and Kinesiology

journal homepage: www.elsevier.com/locate/jelekin

An electrophysiological study of the sequential water swallowing

N. Grgr a,, S . Arc a, Tlay Kurt Incesu a, Y. Seil a, F. Tokuoglu a, C. Ertekin b
Atatrk Research and Training Hospital Department of Neurology, Yesilyurt, Izmir, Turkey
Ege University, Medical School Hospital, Department of Neurology, Turkey1

a r t i c l e i n f o a b s t r a c t

Article history: Background: Sequential water swallowing (SWS) was mostly investigated by the videouoroscopic and
Received 10 August 2012 endoscopic methods. However some physiological features of SWS was rarely evaluated by neurophysi-
Received in revised form 21 December 2012 ological techniques. Our aim was to investigate some neural and muscular changes on sequences of SWS
Accepted 21 December 2012
using electromyography (EMG) methods.
Methods: Fifty-eight normal adults were investigated. SWS was initiated voluntarily with 50 ml and
100 ml water volumes from a cup. Submental EMG, respiratory signals, heart rate, and sympathetic skin
Sequential water swallowing
responses (SSR) were measured during SWS.
Respiration Key results: All parameters were increased signicantly during the 100 ml SWS. During swallowing apnea
Aging period, compensatory respiration cycles occurred in 24% and 48% of participants in the 50 ml and 100 ml
Dysphagia SWS, respectively. Heart rate increased during swallowing apnea. SSR were evoked just before and just
Heart rate after the SWS in more than halves of participants. A foreburst EMG in SM muscles at the initiation of
Sympathetic skin responses SWS was recorded in 86% of normal participants. Older age was associated with a prolonged duration
Swallowing apnea of the apnea period.
Conclusions: All parameters of the SWS could be recorded numerically and objectively using electrphys-
iological methods. These are similar to those obtained by videouoroscopic and similar methods. The
foreburst activity of the initiation of SWS may represents preparatory activity from the activation of
the fast cortical descending motor pathway. Increasing heart rate and the prolonged apnea urged that
older people and patients could be carefully tested for respiratory and cardiac rhythm disorders.
2012 Elsevier Ltd. All rights reserved.

1. Introduction et al., 1990). It should be expected that after the rst swallow in
SWS, subsequent swallows could be primarily initiated at the
Continuous sequential cup/straw swallowing or sequential hypopharynx in normal subjects; these would be most prone to
water swallowing (SWS) in humans has recently been recognized produce laryngeal penetration (Daniels et al., 2004; Daniels and
as a more logical approach to evaluate the physiology of degluti- Foundas, 2001).
tion and to diagnosis dysphagia (Chi-Fishman and Sonies, 2000; When the water volume is increased for SWS, laryngeal pene-
Daniels et al., 2004; Daniels and Foundas, 2001). SWS is a common tration or aspiration frequently occurs (Dosier et al., 2006; Lederle
daily occurrence characterized by multiple, successive, rapid swal- et al., 2011; Martin et al., 1994) There are also reports of an effect
lows (Chi-Fishman and Sonies, 2000; Lederle et al., 2011). of aging on SWS with laryngeal penetration occurring more fre-
During SWS, there are rhythmic or pseudorhythmic swallow se- quently in older adults (Daniels et al., 2004; Mcculloch et al., 2007).
quences without pause, as SWS requires breath-holding resulting Most studies of SWS in normal humans have used videouoros-
in a swallowing apnea period. However, SWS may have longer copy or similar techniques. However, the relationship between res-
interswallow intervals especially at the end of last swallows; this piration and swallowing and other physiological events during
is compensated for by the inspiration/expiration respiratory cycle SWS has never rarely studied by electrophysiological methods.
(Daniels et al., 2004) Breathing can also be interspersed between In this study we applied electrophysiological methods to evalu-
swallows at the midpoint of SWS even in normal subjects (Chi- ate along with SWS and to try some relation with central nervous
Fishman and Sonies, 2000; Chi-Fishman et al., 1998; Cruccu system. We proposed that the onset of SWS is induced by volun-
tary control while subsequent swallows and other autonomic
Corresponding author. and respiratory activity are somewhat related either by the swal-
E-mail addresses: nevin.gurgor@gmail.com, nevin@dr.com (N. Grgr), cumhur- lowing induced factors circulating at the brainstem; or the result
ertekin@gmail.com (C. Ertekin). of central nervous activities; or both.

1050-6411/$ - see front matter 2012 Elsevier Ltd. All rights reserved.
620 N. Grgr et al. / Journal of Electromyography and Kinesiology 23 (2013) 619626

2. Materials and methods 2.3. Electrocardiogram and heart rate

Fifty-eight normal healthy adults without any swallowing com- We simultaneously recorded electrocardiogram (ECG) data in a
plaints were investigated (21 male, 37 female) exclusion criteria third channel of the EMG using silversilver chloride cup elec-
were muscle, nerve and brain disorders; mean age was 48.4 years trodes. One of the electrodes was placed on the second left inter-
(range, 2083 years). All participants were voluntary and included costal space and a second was placed on the dorsum of the hand.
hospital staff and patients relatives. The ethics committee of our Hearth rate was measured before and during SWS. ECG signals
hospital approved the study and all participants provided informed were ltered (band pass 0.230 Hz) and amplied.
consent. During the examination, the seated participant was in-
structed to hold their head in neutral upright position. All examin- 2.4. Sympathetic skin response (SSR) measurements
ations were performed in the afternoon at least 2 h after lunch.
In order to understand the aging effects on SWS, we divided The SSR was recorded from the skin of the left hand. The skin
part of participants into two groups. The young group had the surface was cleaned and silversilver chloride electrodes were
mean age of 31.8 years (range, 2039 years) and included 17 par- placed on the skin of the palm and dorsum of the hand using elec-
ticipants (10 female, 7 male). The older group had a mean age of trogel (Lome EEG paste) The low frequency lter was 0.2 Hz and
69.2 years (range, 6083 years) and included 14 participants (9 fe- the high frequency lter was 100 Hz. Spontaneous electrodermal
male, 5 male). activity (EDA) or background uctuations of EDA were rst re-
corded for 20 s with the subjects at rest. During the 50 ml and
100 ml SWS tests, the rst SSR was evoked after the examiners
2.1. Sequential water swallowing (SWS) command to swallow. The rst SSR was related to attention
and is called the arousal SSR for the sake of brevity. SSR and heart
Liquid swallows of tap water were initiated voluntarily with 50 rate changes during SWS were evaluated and reviewed in detail
and 100 ml water in a disposable cup positioned in between the elsewhere.
lips before the any command was given. Water temperature was
approximately 2325 C. Swallowing signals were recorded from 2.5. Order of experiments
submental/suprahyoid EMG. The submental EMG (SM-EMG) was
recorded using bilateral silversilver chloride (AgAgCl) EEG elec- We rst recorded basal respiration and heart rate. Afterwards,
trodes taped under the chin over the submental muscle complex the SWS test was conducted three times with 50 ml water followed
(mylohyoid, geniohyoid, and anterior digastric muscles). The skin by three times with 100 ml water. There were intervals (1
overlying the submental complex was cleaned and the electrogel 5 min) between each experiment. If participants needed additional
(Lome EEG paste) was also used with the EMG surface electrodes interval time, this was also permitted in order to create a more re-
placed for submental recordings. Signals were ltered (band pass laxed environment. His or her head was stabilized by one of the
10010 kHz), amplied, rectied, and integrated. Total analysis examiners hand from the top of head during all experiments.
time was adjusted to 20 s for each set of SWS.
Baseline EMG activity were initiated for several seconds prior to 2.6. Statistical methods
onset of SWS; afterward the instruction to swallow was given by
the examiner. Subjects were asked to drink water continuously The mean and standard deviation (SD) and standard error of
as they do in their daily life just before they were asked to start mean (SEM) of all measured quantities were calculated and
drinking. The SWS test was repeated three times with 50 and paired-t test was applied for comparisons. Chi-square analyses
100 ml water drinking in all subjects. The third SWS traces for each were used to test for differences in percentage of respiratory pat-
subjects were selected for the individual measurement. The third tern between 50 and 100 ml SWS. Signicance was tested at the
trial was of SWS found to be the most sophisticated and reliable 0.5% level. Statistical analysis was conducted using the SPSS statis-
measurement comparing previous two SWSs. The number of swal- tical package.
lows were recorded and counted according to the periodic move-
ments on SM-EMG. Total duration of SWS was calculated from
3. Results
the onset of the rst EMG burst to the end of the last swallow on
the SM-EMG traces in a SWS epoch. Four channel-EMG apparatus
3.1. Effect of bolus volume in SWS
were used (Nicolet-Viking V.11.0).
After the command to swallow, normal adult subjects could
perform swallowing movements recorded from SM muscles that
2.2. Swallowing apnea measurement during SWS were quite rhythmic (Fig. 1). Table 1 reports swallowing measure-
ments and other parameters. As expected, the number of swallows
The swallowing apnea period of respiration was studied in all and the duration of SWS increased signicantly with 100 ml SWS
participants. For this purpose, an additional EMG channel was used (p < 0.0001). This means that when the amount of water is in-
simultaneously. The respiratory signal was obtained via a nasal creased, the number of swallows and subsequently the duration
cannula (Sleep Sense) and placed at the entry of the nostrils of SWS are proportionally increased. However, there were two
and connected to the EMG machine. Airow direction was re- ndings that were not usually expected in normal subjects: the
corded as a negative polarity representative of inspiration and a rst SM-EMG bursts showed some interesting features that can
positive polarity representative of expiration. The SM-EMG and be called foreburst of SWS. These occurred after the command
phase of respiration were simultaneously recorded to detect swal- of swallow by examiner; however they almost always appeared
lowing apnea and respiratory phase pattern before, during, and just before or during the last respiratory cycles and before swal-
after 50 or 100 ml of SWS. Respiratory signals were also recorded lowing apnea. They were often smaller in amplitude than the sub-
at rest. A plateau in the respiratory signal along the baseline indi- sequent swallow bursts and sometimes longer in duration as
cated an apneic period. EMG lters for the respiratory channel swallowing continued (Figs. 1 and 2). However, the foreburst of
were adjusted with a band pass of 0.230 Hz. SWS could not be found in 10 of 58 participants; they were seen
N. Grgr et al. / Journal of Electromyography and Kinesiology 23 (2013) 619626 621

Fig. 1. Sequential water swallowing (100 ml). First channel: SM-EMG (The
foreburst is lined). Second channel: respiration (Resp) (nasal cannula). Third
channel: ECG. Fourth channel: electrodermal activity and rst SSR. Note: the
foreburst occurs with the last respiratory cycle, before the apnea interval.

Table 1
Statistical results* of SM-EMG, respiration and heart rate changes after 50 ml and
100 ml water swallowing (SWS). Fig. 2. The initiation of 100 ml SWS. First channel: SM-EMG. Second channel:
respiration (nasal cannula). Third channel: sympathetic skin response (SSR). Note:
50 ml SWS* 100 ml P the typical foreburst and SSR just after instruction from the examiner.
1. Number of swallows 4.7 1.3 0.1 6.4 1.6 0.2 <0.0001
37 411 than those of the non-swallowing period. They mostly appeared
2. SWS duration (s) 6.3 2.0 0.2 7.8 2.0 0.2 <0.0001 with long inter-swallow intervals.
310.5 414 We compared participants with and without compensatory res-
3. Swallowing apnea (s) 6.1 1.9 0.2 7.0 2.1 0.2 <0.0003 piration during swallowing apnea during the 50 ml and 100 ml
2.510 312 SWS. In the 50 ml SWS, subjects with compensatory respiration
4. Heart rate (basal)/(min) 76.4 11.6 76.4 11.6 NS during swallowing apnea showed increased number of swallows
1.5 1.5 (p = 0.0004), SWS duration (p = 0.0002), and apnea interval
5. Heart rate (during swallowing 88.4 12.3 88.5 12.2 NS (p = 0.03) compared to participant without compensatory respira-
apnea)/min 1.1 1.6 tion. Results were similar for the 100 ml SWS, although the num-
P < 0.0001** P < 0.0001** ber of swallows and swallowing apnea were not signicantly
Mean SD, SEM, Range. different between the two groups. The increase in water volume
p Values obtained from the comparison of the basal and SWS conditions for from 50 ml to 100 ml may produce more risk but this was probably
heart rate. compensated by the increase number of extraneous respiratory cy-
cles from 24% to 48%.
Table 1 reports changes in heart rate during SWS. In basal con-
in 86% during the 50 ml SWS. Similarly, the foreburst was found in ditions before swallowing, mean heart rate was 76/min. During
approximately 86% of participants during the 100 ml SWS. Thus swallowing (either 50 or 100 ml SWS), heart rate was increased
there is no difference in the appearance of a foreburst of SWS to approximately 88 beats/min (p = 0.001) (Fig. 4). This is the
in 50 ml versus 100 ml SWS (Table 2). well-known swallowing tachycardia described more than a cen-
A second important observation during SWS is that there were tury ago by Meltzer (Sheroziya et al., 2003). All heart rate changes
compensatory respiration cycles (inspiration/expiration) during occurred during the apnea interval. After the apnea interval the
the swallowing apnea period while participants were sequentially heart rate dropped to basal values. Arousal SSR could be evoked
swallowing (Fig. 3). During the 50 ml SWS, 14 participants demon- in approximately 52% of participants; at the end of SWS, second
strated such compensatory respiratory cycles within the swallow- SSR was found in nearly the same number of cases.
ing apnea period (approximately 24%). However, during the 100 ml
SWS the compensatory respiratory cycles were signicantly more 3.2. Age effects on SWS
common, being found in 28 subjects (approximately 48%). It was
not uncommon to observe the compensatory respiratory cycle be- Table 3 and Fig. 5 shows the effect of age on SWS values. There
tween the last interswallow interval of SWS. Indeed the last swal- were no signicant differences between the two age groups with
lows during SWS had slightly longer intervals compared to the rst the exception of swallowing apnea, which was prolonged in the
swallows (Fig. 3). However, the compensatory respiration could older age group on the 50 ml SWS (p < 0.042) (Fig. 5). Although
also be recorded in the midst of SWS during swallowing apnea. the mean duration of the 50 and 100 ml SWS were increased in
The most striking feature of the respiratory cycles or compensatory the older age group, this did not reach statistical signicance.
respiration was found during the inter swallow intervals. A second The rate of compensatory respiratory cycles was similar be-
feature was that the onset was mostly inspiration and immediately tween age groups. In the 50 ml SWS, 29% of both groups showed
continued with expiration. Their amplitudes were often higher compensatory respiration cycles. In the 100 ml SWS, 47% and
622 N. Grgr et al. / Journal of Electromyography and Kinesiology 23 (2013) 619626

Table 2
Electrophysiological features of the foreburst activity in 50 ml and 100 ml SWS.

Number of Foreburst activity recorded from Mean Mean _

Interval between the peak of foreburst
cases number of cases M SD SEM amplitde (mV) duration (s) and the peak of rst swallow (s)
50 ml SWS 58 50 (86%) 71.5 34 1.9 0.7 1.5 0.8
4.8 0.1 0.1
100 ml SWS 58 50 (86%) 68.5 26.8 1.8 0.7 1.5 1.4
3.8 0.1 0.2

There were no statistical signicant value in between 50 and 100 ml SWS.

Table 3
Statistical summary of SWS study for young and old normal participant.

Parameters Young Signicants Old

people*n = 17 people*n = 14
Number of swallows 4.7 1.3 (0.3) NS 4.8 1.5 (0.4)
50 ml SWS 37 49
100 ml SWS 6.8 1.6 (0.4) 6.5 1.5 (0.4)
410 49
Duration of swallows (s) 5.9 2.1 (0.5) 6.8 2.6 (0.7)
50 ml SWS 3.010.0 NS 3.010.5
100 ml SWS 7.7 2.0(0.4) 8.6 2.2(0.6)
Fig. 3. Sequential water swallowing (100 ml). First channel: SM-EMG. Second 512 514
channel: respiration and swallowing apnea, Note: compensatory respiratory cycle
Swallowing apnea (s) 5.3 1.9 (0.4) 7.1 2.3 (0.6)
in between last swallows during the apnea period (arrow).
50 ml SWS 2.510 0.042 3.510.5
100 ml SWS 6.9 2.1(0.5) 7.8 2.6(0.6)
Heart rate basal/(min) 81 13.6(3.3) NS 74 10.27 (2.8)
50 ml SWS 60111 5793
100 ml SWS 81 13.63(3.3) NS 74 10.27(2.8)

60111 5793
Heart rate apnea/(min) 97.7 11.5(2.8) 83.4 9.6 (2.6)
50 ml SWS 68114 0.001** 68112
100 ml SWS 96.4 14.4(3.5) 0.003** 83.3 8.1(2.2)

60118 68112
Heart rate increase during 15.0 7.6 (1.8) NS 9.5 7.11 (1.9)
SWS apnea 3.033 0.021
50 ml SWS 13.7 6.9(1.6) 8.2 6.2(1.6)
100 ml SWS NS
026 0.021

mean SD, SEM, Range.
They were compared by the basal values of ECG.

conclude there was again no difference between young and old

participants (Table 4). One variation was that the initiation and
end of swallowing apnea was completed much more frequently
with expiration in the older age group (71.4%) compared to the
younger group (64%).

3.3. Initiation and termination of SWS

Fig. 4. Comparison of ECG between baseline and during swallowing apnea
interval. Each line denotes a case investigated. Vertical line is heart beats per Some specic features were recognized at the initiation of SWS.
minute. In the apnea interval, there is clear-cut tachycardia. As shown in Fig. 2, the examiners order to swallow rst pro-
duced the foreburst on SM-EMG, which was elicited even before
or mostly during the last cycle of respiration in 87% of participants.
50% of young and older participants showed compensatory respira- During or just after the rst respiration cycle, an arousal SSR was
tion cycles, respectively. The 50 ml SWS was safer than the 100 ml evoked in approximately 52%. Some participants showed another
SWS irrespective of age. If the expiration or inspiration relationship SSR just after the end of the sequential swallowing and apnea period,
resulted in the initiation and termination of swallowing apnea; we unrelated to water volume. However, this second SSR was not re-
N. Grgr et al. / Journal of Electromyography and Kinesiology 23 (2013) 619626 623

Fig. 5. Young and older healthy participants, 50 ml SWS with SM-EMG (upper) and respiration (respiration, lower trace). Note: increase of swallowing apnea interval and
compensatory respiratory cycle during the apnea period in older participants.

Table 4 described. The foreburst began immediately after the examiners

The onset and end of SWS apnea. instruction. It does not seem to be a deection of the initial swal-
Young peoples Old peoples n = 14
low. We think this for several reasons. First, the foreburst is lower
n = 17 in amplitude and longer in duration than the subsequent swallow
50 ml SWS
deexions. It is also the rst event in the SWS procedure. It was al-
Expiration/expiration n = 11 64.70% n = 10 71.43% ways formed just before the onset of swallowing apnea. It appears
Expiration/inspiration n=5 29.42% n=4 28.57% within the regular respiratory movements and can even overlap
Inspiration/expiration n=1 5.88% the last respiratory cycle before the swallowing apnea period
(Figs. 1 and 2 and Table 2). It is probably either a type of startle re-
100 ml SWS sponse or, more likely, it may present a preparatory EMG signal
Expiration/expiration n=9 52.94% n = 11 78.57%
produced by the descending motor pathway(s) to the suprahyoid
Expiration/inspiration n=6 35.30% n=3 21.43%
Inspiration/expiration n=1 5.88% muscles.
Inspiration/inspiration n=1 5.88% During sequential swallowing, the rst cortical input is thought
to descend to the brainstem neural network or swallowing central
pattern generator (CPG) based on experimental studies (Martin
corded in approximately half of participants (Fig. 6). During termina- and Sesle, 1993; Miller, 1982; Narita et al., 1999). During such a
tion of SWS, the last swallow often showed longer intervals than the voluntarily-induced swallow (Ertekin, 2011), the regions of the
previous interswallow intervals (see Figs. 1 and 3). The interswallow cortex and subcortical areas involved with swallowing serve
interval could be compensated by a respiratory cycle, either expira- mainly to trigger deglutition and to control the beginning of the
tion to inspiration or vice versa. In most participants the swallowing motor sequences, after triggering of SWS and during the sequential
was completed without compensatory respiratory cycles. Swallowing deglutition (Ertekin and Aydogdu, 2003; Jean and Car, 1979; Lang,
tachycardia was particularly apparent during the latter parts of swal- 2009; Nishino, 1993; Thexton et al., 2007). On the other hand, the
lowing apnea. After the end of swallowing, heart rate immediately most consistent cortical activation is seen in the primary motor
decreased to the basal level. (see Figs. 1 and 4). and primary sensory cortices (Hamdy et al., 1999; Martin et al.,
2004; Mossier et al., 1999; Suzuki et al., 2003). It has been demon-
4. Discussion strated that motor planning of voluntary swallow or sensory stim-
ulation of the oropharynx may activate the supplementary motor
SWS can be subdivided into three parts for analysis: initiation, area, insula, cingulated cortex, premotor cortex, basal ganglia,
swallowing apnea period and termination, by means of EMG and cerebellum without any signicant act of swallowing (Abe
methods. et al., 2004; Lowell et al., 2008; Sros et al., 2008). Thus our fore-
burst is an activation related to the preparation of SWS just before
4.1. Initiation of SWS its onset, with a duration of approximately 14 s, similar to reports
mentioned above. When the instruction of the examiner was heard
The initiation of SWS was voluntary. The foreburst of SWS in the fast auditive afferent pathways should be activated to stimu-
one of the most important phenomenon, and it has not yet been late the M1 cortex and cingulated cortex. As a result, the prepara-
624 N. Grgr et al. / Journal of Electromyography and Kinesiology 23 (2013) 619626

Fig. 6. Termination of SWS. First channel: SM-EMG. Second channel: respiration (Resp). Third channel: EDA and SSR. Note; compensatory respiration during the apnea
interval (underlined) and the second SSR around the termination of SWS (arrow).

tory SWS can be elicited by means of the very fast cortico-bulbar (Daniels and Foundas, 2001; Dosier et al., 2006; Lederle et al.,
pathways with onset latencies of less than 1015 ms to the perio- 2011). It was also reported that a tendency to inspire during and
ral muscles, as determined by transcranial magnetic stimulation after the SWS suggest that there might be an increased drive to
(TMS)Cruccu et al., 1990; Liscic et al., 1998; Meyer et al., 1994; breath during sequential swallowing (Lederle et al., 2011; Dosier
Yldz et al., 2005. et al., 2006). During the swallowing apnea period, the most impor-
It is well known that the SSR can be evoked by any kind of arou- tant swallowing stage is the pharyngeal phase from the standpoint
sal stimuli (Dawson et al., 2000; Vetrugno et al., 2003). In order for of respiration control, because swallowing and respiration share
our instruction to produce this kind of arousal, the SSR must be the pharynx as a common pathway during the pharyngeal phase
evoked by cortico-subcortical processes. The onset of arousal SSR of swallowing (Thexton et al., 2007). Swallowing itself is also ac-
is later than the onset of foreburst but before swallowing apnea. cepted as a protective reex for the upper airway, while respiration
This may suggest that the arousal SSR could be initiated by the is also a reliable system to control the rhythmicity and regularity of
sound-induced cortico-subcortical mechanisms. The anterior cin- SWS. Experimental studies demonstrated that the CPG of breathing
gulate cortex or thalamo-cortical limbic circuits and lower brain- and swallowing may anatomically overlap but the grouping of the
stem structures including nucleus tractus solitarii (NTS)were medullary interneurons may have more than one function, or the
demonstrated to positively correlate with neural activity in sub- two system of respiration and swallowing are coordinated during
jects experiencing auditory and arousal stimuli with SSR (Frederik- SWS (Jean, 2001; Jean and Dallaporta, 2006; Kessler and Jean,
sen et al., 1998; Korpelainen et al., 1993; Pron et al., 1995). The 1985; Martin, 2006). It is conceivable that the very rst swallows
arousal SSR could be evoked in about half of the participants. This should be under voluntary control (Aydogdu et al., 2011) but in
may suggest that they have somewhat different central sources. subsequent swallow sequences are inuenced some automated
Probably, the SSR is related to concentration or attention of partic- or reexive process. Later swallows and their interswallow inter-
ipants. Fast habitiation may also cause the absence of SSR in some vals might be regulated by the swallowing CPG in the brainstem
participants. When the presence of both SSR and foreburst activity network, and the NTS may be important for this regulation (Jean,
may strongly demonstrated that the initial part of SWS is related 2001; Car and Amri, 1987). An inherent feature of the generator
with cortical voluntary preparation process of deglutition. neurons at the dorsal swallowing group (DSG) in and around the
NTS is to re a sequential or rhythmic pattern parallel to the motor
4.2. The swallowing apnea period pattern of oropharyngeal swallowing (Bariotay et al., 2008; Felix
et al., 2006; German et al., 2009; Jean, 2001; Jean and Dallaporta,
The swallowing apnea period during the 50 ml or 100 ml SWS 2006). The bulbar CPG and the NTS could also functionally impor-
can be controlled voluntarily, spontaneously, or both. However, tant in controlling the rhythmicity of SWS in humans; rhythmicity
the last two swallows often had longer inter-swallow interval than of SWS is disturbed in patients with amyotrophic lateral sclerosis
other swallows in the same set, and the longer inter swallow inter- (ALS) especially in bulbar and pseudobulbar types (Aydogdu
val observed in the last two swallows was sometime compensated et al., 2011).
by a high volume respiratory cycle beginning with inspiration (see In our 50 and 100 ml SWS, heart rate signicantly increased
Fig. 3). Compensatory respirations were usually more frequent in during swallowing apnea (p = 0.001). Swallowing tachycardia is
the 100 ml than the 50 ml SWS. The 100 ml SWS also showed long- one characteristic of the SWS apnea period. This has been previ-
er swallowing apnea periods, greater number of swallows, and ously investigated, usually by discrete swallows; drinking water
longer duration of swallowing. This kind of compensatory swallow was shown to cause a transient increase in sympathetic activity,
during the apnea period was reported in previous SWS studies mean arterial pressure, and heart rate immediately after drinking
N. Grgr et al. / Journal of Electromyography and Kinesiology 23 (2013) 619626 625

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626 N. Grgr et al. / Journal of Electromyography and Kinesiology 23 (2013) 619626

Meyer BU, Werhahn K, Rothwell JC, Roericht S, Fauth C. Functional organisation of Tlay Kurt Incesu was born at 1967 in Samsun. She
corticonuclear pathways to motoneurones of lower facial muscles in man. Exp graduated from Gazi University Medical School, Ankara
Brain Res 1994;101:46572. in 1990. During 19941998 period, she completed her
Miller AJ. Deglution. Phys Rev 1982;62:12984. education at Neurology Department of Pamukkale Uni-
Mossier K, Patel R, Liu WC, Kalnin A, Maldjian J, Baredes S. Cortical representation of versity Medical School Hospital in Denizli and she
swallowing in normal adults: functional implications. Laryngoscope became Neurologist. Then, she worked as assistant
1999;109:141723. professor at the same hospital. She worked in EMG
Narita N, Yamamura K, Yao O, Martin RE, Sessle BJ. Effects of functional disruption laboratory of Clinical Neurophysiology Department of
of lateral pericentral cerebral cortex on primate swallowing. Brain Res Ege University Medical School for 6 months in 2000. She
has been working as an associate professor at Neurology
Nishino T. Swallowing as a protective reex for the upper respiratory tract.
Department of Medical School, Katip Celebi University
Anesthesiology 1993;79:588601. _
Nitta E, Iwasa Y, Sugita M, Hirono C, Shiba Y. Role of mastication and swallowing in in Izmir since 2011. She is a member of Turkish Society
the control of autonomic nervous activity for heart rate in different postures. J of Neurology and Turkish Society of Clinical Neurophysiology EEG-EMG. Her
Oral Rehab 2003;30:120015. research interest focus on clinical neurophysiology and movement disorders.
Pron Y, Aubertin P, Guihneuc P. Prognostic signicance of electrophysiological
investigations in stroke patients: somatosensory and motor evoked potentials
and sympathetic skin response. Neurophysiol Clin/Clin Neurophysiol Yaprak Seil was born at 1971 in Sakarya. She gradu-
1995;29:14051. ated from Istanbul University Cerrahpasa Medical
Sheroziya OP, Ermishkin VV, Lukoshkova EV, Mazygula EP, Rybyakova VB, School (English Department) in 1995. She completed
Chepetova TV. Changes in swallowing related tachycardia and respiratory her education at Neurology Department of Ege Univer-
arrhythmia induced by modulation of tonic parasympathetic inuences. sity Medical School Hospital in Izmir and she became
Neurophysiology 2003;35:434444. Neurologist in 2001. Then, she worked as volunteer
Sros P, LaLone P, Simith R, Stevens T, Theurer JJ, Menon RS, et al. Functional MRI of neurologist for one year in EMG laboratory of Clinical
oropharyngeal air-pulse stimulation. Neuroscience 2008;153:13008.
Neurophysiology Department at the same hospital. She
Suzuki M, Asada Y, Ito J, Hayashi K, Inove H, Kitano H. Activation of cerebellum and
has gained Young Scientist Award from Turkish Acad-
basal ganglia on volitional swallowing detected by functional magnetic
emy of Sciences in January 2002. Also, she and swal-
resonance imaging. Dyshagia 2003;18:717.
Thexton AJ, Crompton A, German RZ. Electromyographic activity during the reex lowing group of Clinical Neurophysiology Department
pharyngeal swallow in the pig: Doty and Bosma (1956) revisited. J Appl Physiol of Ege University had Sedat Simavi Medical Sciences
2007;102:587600. Award in 2003. She has been working at Neurology Department of Atatrk Edu-
Vetrugno R, Liquori R, Cortelli P, Montagna P. Sympathetic skin response: basic _
cation and Research Hospital in Izmir since 2002, after 2007 she has been associate
mechanisms and clinical applications. Clin Auton Res 2003;13:25670. proffessor at the same department. She is a member of Turkish Society of Neurology
Yldz N, Ertekin C, zdemirkran T, Yldz SK, Aydogdu I, _ Uludag B, et al. and Turkish Society of Clinical Neurophysiology EEGEMG. Her research interest
Corticonuclear innervation to facial muscles in normal controls and in focus on clinical neurophysiology, neurourology-sexual disorders in females and
patients with central facial paresis. J Neurol 2005;4:42935. neuromuscular disorders.

Nevin Grgr was born at 1965 in Izmir. She graduated Figen Tokucoglu graduated from Aegen University
from Ege University Medical School in 1989. During Medical School in 1989. She completed her residency on
19931996 period, she completed her education at neurology in 1995, had master degree on elctrodiag-
Neurology Department of Atatrk Research and Train- nostic neurology. Her area of interests are clinical
ing Hospital in Izmir. Then, she worked as Neurologist at electrophysiology, movement disorders and multiple
the same hospital. She worked in EMG laboratory of sclerosis.
Clinical Neurophysiology Department of Ege University
Medical School for 6 months in 2000. She has been
working as neurologist at Neurology Department of
Atatrk Research and Training Hospital in Izmir since
2000. She is a member and Turkish Society of Clinical
Neurophysiology EEG-EMG. Her research interests focus
on epilepsia and clinical neurophysiology.

ehnaz Arc was born at 1973 in Antalya. She gradu- Cumhur Ertekin is a professor in neurology and clinical
ated from Akdeniz University Medical School in 1996. neurophysiology. He was a chair in clinical neurology at
Ege University in Izmir, Turkey. He was founder of
She completed her education at Neurology Department
of Ege University Medical School Hospital in Izmir and Turkish Society of Clinical Neurophysiology EEGEMG.
she became Neurologist in 2003. She has been working He was retired from University.
as neurologist at Neurology Department of Atatrk
Research and Training Hospital in Izmir since 2003. She
is a member of Turkish Society of Neurology and Turk-
ish Society of Clinical Neurophysiology EEGEMG. Her
research interests focus on epilepsia and clinical neu-