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A Motor Grammar of Swallowing12

© Norbert Rüffer, 2012

Korrespondenzadresse: Dr. Norbert Rüffer, Fuchsweg 10, 65719 Hofheim,

mail@norbert-rueffer.de

Abstract

Swallowing is characterised by a sequence of motor events in the oral, pharyngeal and

oesophageal space. This sequence is controlled by a complex motor system that includes

the Central Pattern Generator for Swallowing (CPGS), located in the ponto-medullary region

of the brain stem. In this paper we will discuss some facts that challenge the assumption that

neural control systems for iterative movements, such as swimming, walking or breathing

(iterative CPGs), can serve as a model for the CPGS (iterative CPGS hypothesis).

In contrast to the iterative CPGS hypothesis, we propose a processing model of motor

planning and control for swallowing that is based on two fundamental principles that are not

specific to swallowing: motor coordination and motor learning. Motor coordination is a

combinatory planning process generating sequentially and hierarchically organised motor-

temporal structures or motor plans. Being free within biomechanical and functional

constraints, motor coordination enables a range of more or less fixed motor-temporal

relations within the pharyngeal swallowing sequence and between bolus transit and

swallowing motor events, depending in part on bolus features.

Automaticity of swallowing is based on motor learning, that is, improvement of motor

coordination with respect to bolus transit and airway protection, long-term storage of the

resulting motor-temporal patterns and activation of these structures. The CPGS is not an

iterative CPG but plays the role of the motor memory for the swallowing system.

The current work does not present new data but rather provides a new interpretation of data

recently published by Kendall, Mendell, Logemann, Martin-Harris and others on the motor-

temporal structure of the pharyngeal motor sequence.

1 This paper is based partly on presentations at the 6th World Congress for NeuroRehabilitation (WCNR), March 21–25, 2010, in Vienna, Austria, and at an expert meeting on ‘Motor Grammar and Presbyphagia’ at the University of Bielefeld, April 16, 2011. 2 I want to thank Andrea Hofmayer and Sönke Stanschus for important comments.

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Eine motorische Grammatik des Schluckens

Schlucken ist durch eine Sequenz motorischer Aktionen im oralen, pharyngealen und

ösophagealen Raum charakterisiert, die durch ein komplexes motorisches System

kontrolliert wird, das den in der ponto-medullären Region des Hirnstamms lokalisierten

Central Pattern Generator des Schluckens (CPGS) einschließt. Wir diskutieren Fakten, die

die Annahme in Frage stellen, dass neuronale Kontrollsysteme für iterative Bewegungen wie

schwimmen, laufen oder atmen (iterative CPGs) ein geeignetes Modell für den CPGS

darstellen (iterative CPGs-Hypothese).

Als Alternative zur iterativen CPGs-Hypothese wird ein Verarbeitungsmodell der motorischen

Planung und Kontrolle des Schluckens vorgeschlagen, das auf zwei fundamentalen

Prinzipien basiert, die nicht schluckspezifisch sind: motorische Koordination und motorisches

Lernen. Motorische Koordination ist ein kombinatorischer Planungsprozess, der sequentiell

und hierarchisch organisierte motorisch-zeitliche Strukturen oder Motorpläne generiert. Die

auf motorischer Koordination basierende motorische Planung ist im Rahmen

biomechanischer und funktionaler Outputbedingungen variabel und ermöglichen ein

Spektrum von mehr oder weniger fixierten, zum Teil von Boluseigenschaften abhängigen

motorisch-zeitlichen Relationen innerhalb der pharyngealen Schlucksequenz und zwischen

Bolustransit und Schluckmotorik.

Die Automatizität des Schluckens basiert auf motorischem Lernen, d.h. einer Optimierung

der schluckmotorischen Koordination im Hinblick auf den Bolustransport und die

Atemwegsprotektion, der Speicherung dieser optimierten motorisch-zeitlicher Strukturen

sowie deren Aktivierung. Der CPGS ist kein iterativer Mustergenerator, sondern fungiert als

motorischer Speicher des Schlucksystems.

Die vorliegende Arbeit präsentiert keine neuen Daten, sondern re-interpretiert aktuelle Daten

von Kendall, Mendell, Logemann, Martin-Harris und anderen zur motorisch-zeitlichen

Struktur der pharyngealen Schlucksequenz.

Keywords: Central Pattern Generator for Swallowing (CPGS), processing model of

swallowing, motor planning of swallowing, motor coordination, motor learning, biomechanical

and functional constraints of swallowing

Schlüsselwörter: Central Pattern Generator des Schluckens (CPGS), Verarbeitungsmodell

des Schluckens, motorische Planung des Schluckens, motorische Koordination, motorisches

Lernen, biomechanische und funktionale Beschränkungen des Schluckens

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The Central Pattern Generator for Swallowing

Swallowing is characterised by a sequence of motor events in the oral, pharyngeal and

oesophageal space that is controlled by a complex motor system, which includes cortical,

subcortical und brain stem areas. Kendall and colleagues proposed the following pharyngeal

swallowing sequence based on videofluoroscopy data (Kendall et al., 2000):

Spstart>Aestart>H1>SPmax>Aeclose>PESop>H2>PESmax>HL>H3>Pamax>PEScl

SPstart=soft palate begins to elevate; Aestart=aryepiglottic folds begin to elevate; H1=hyoid bone begins to elevate;

Spmax=soft palate has reached maximal elevation; Aeclose=aryepiglottic folds contact the epiglottis;

PESop=pharyngoesophageal sphincter (PES) begins to open; H2=hyoid bone has reached maximal elevation; PESmax=PES

reaches maximum distension; HL=larynx approximates the hyoid bone; H3=hyoid begins to descend; Pamax=maximum

pharyngeal constriction; PEScl=PES closes

According to this sequence, pharyngeal swallowing starts with the motor events soft palate

and aryepiglottic folds elevation (SPstart, Aestart), moves through hyoid and laryngeal

elevation (H1-3, HL) in association with laryngeal closure at the epiglottis level and

pharyngeal contraction (Pamax), and terminates in pharyngoesophageal sphincter

relaxation, opening and finally closure (PESop, PESmax, PEScl) after the bolus has reached

the oesophagus.

The Central Pattern Generator for Swallowing (CPGS), which is located in the ponto-

medullary region of the brain stem, plays an important role in neural control of swallowing.

While neural control of swallowing is not restricted to the CPGS, it is nevertheless based to a

large extent on the CPGS network. It is assumed that the CPGS generates a basic motor

plan for pharyngeal swallowing which can be modulated by superior levels of the swallowing

motor system (see Daniels&Huckabee, 2008, p. 19ff for an overview).

Although there has been no attempt to clarify the concept of the CPGS ‘basic motor plan’ to

date, there is a prominent few in dysphagia research, suggesting that the CPGS output can

be identified with a rhythmic pattern that serves as a frame for the motor-temporal structure

of swallowing. The following statement by Lang is typical in this respect (Lang, 2009, p. 340,

underlines added):

‘Electrophysiologic studies have found that neurons of the brain stem contain the timing pattern-

generating circuitry that governs the oral, pharyngeal, and esophageal phases of swallowing.

One can find neurons that respond at a time delay and duration that corresponds to the expected

timing of rhythmical movements of the jaw or peristalsis of the pharynx or esophagus. These neural

events are not caused by feedback from periphery, e.g., propagating peristalsis, because this pattern

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persists even in paralyzed animals. Therefore, these neural events found in premotor neurons must

control the timing of these phases of swallowing...

Swallowing is initiated by a voluntary act but much of this process is composed of stereotyped motor

activity that is controlled by brain stem central pattern generators.’

According to Lang, the CPGS is a ‘timing pattern-generating circuitry’ that generates a

‘rhythmical’ and ‘stereotyped motor activity’ without being ‘caused by feedback from

periphery’. The CPGS function is viewed as being similar to Central Pattern Generators in

the sense of neural control systems for rhythmic and repetitive movements such as

swimming, walking or breathing. We will call Central Pattern Generators in this sense

iterative CPGs.

What are iterative CPGs? Iterative CPGs are neural networks that function as a biological

oscillator generating a rhythmical pattern. They may differ in neural architecture and rhythmic

pattern output as shown by the examples of the leech heartbeat CPG and the lobster pyloric

CPG in Hooper (2001):

Fig. 1. Neural network and rhythmic pattern output of central pattern generators; Hooper, 2001, p. 3, Fig. 1 Permission for reprint by John Wiley & Sons Ltd.

Iterative CPGs are related to motor systems and the CPG-generated rhythmic pattern serves

as a frame for the temporal relations of the motor activity output of the respective motor

system. Sensory integration may modify the CPG rhythmic pattern, which in turn would lead

to temporal modification of the correlated motor activity. An example is the locust flying CPG,

in which sensory feedback of wing elevation affects cycle period and burst duration of the

generated rhythmic pattern, which in turn affects the flying behaviour of the locust (Hooper,

2001).

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Although the role of iterative CPGs within motor systems has only been partly explored, the

available data seem to support the following modular model. Motor systems generate motor

activities by selecting a set of muscles and activating this set in a particular temporal order:

Fig. 2. Motor-temporal control of iterative CPGs embedded in motor systems

Within the resulting motor-temporal sequence, the rhythmic pattern of an associated iterative

CPG translates into a frequency pattern related to shorter or longer intervals between

designated time points of the motor-temporal structure. Iterative CPGs control the intervals

between onset times of distinct muscles of the sequence, intervals between onset and offset

times of identical muscles (activation lengths) and define the onset and offset time of an

iteration cycle (motor-temporal loop). Iterative CPGs temporally modify motor activities but do

not change them in a qualitative way, since the effects of iterative CPGs are limited to

particular selection of a set of muscles and their activation sequence. Qualitative change of

motor activity is based on a different selection of muscles and their activation at the motor

system level.

Lateral turns in lampreys provide an example. In lampreys the swimming CPG is located in

the spinal cord and is neuroanatomically arranged as a sequence of spinal segments, which

each control a set of muscles called a myotome. Swimming results from laterally coordinated

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waves of myotomal contractions along both sides of the fish’s body. Fagerstedt & Ullén

(2001) have shown that if the lamprey executes a lateral turn in response to a stimulus on

one side of the fish, this motor activity is the result of a lateral change in the swimming motor

sequence caused by longer cycle duration together with increasing burst duration, burst

proportion (within the movement cycle) and burst intensity. Apart from the change in burst

intensity, lateral turns in lampreys can be described as connected to a change in frequency:

cycle duration, burst duration and burst proportion are related to the intervals between onset

times and to activation lengths. That there is also an effect on burst intensity, that is, motor

force, does not contradict the assumption that iterative CPGs primarily modify the temporal

structure of motor activities, since temporal motor features and motor force are closely

related for biomechanical reasons. An increase in the frequency of iterative movements

normally requires an increase in the motor force.

Although the assumption that swallowing is controlled by an iterative CPG – which we will

call the iterative CPGS hypothesis – seems at first sight to have certain plausibility because

both iterative motor sequences and the pharyngeal swallowing sequence show a high

degree of automaticity, the facts contradict this assumption. If the CPGS neural control of

swallowing were similar to iterative CPG motor control, we would expect a similar structure

for neural control in both cases. For swallowing this would imply that swallowing should have

an iterative motor-temporal structure and that motor-temporal changes due to sensory

integration of bolus properties should be related to a change in frequency, that is, change in

the intervals within a certain selection and activation order of motor events.

Five problems with the iterative CPGS hypothesis

In the following, some facts will be discussed that challenge the assumption that iterative

CPGs are an appropriate model for the swallowing CPG. There are five main problems with

the iterative CPGS hypothesis:

Table 1. Iterative CPGs vs. CPGS

Iterative CPGs Five problems with

the iterative CPGS hypothesis

Generate iterative cycles (motor-temporal

loops)

1. The swallowing sequence has – with the

exception of mastication – no iterative

structure

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Relate sensory integration to frequency in

the sense of shorter or longer intervals

between designated time points in a motor

sequence including onset times, activation

length and iterative cycle

2. Sensory integration of bolus properties is

only in part linked to change in frequency

Control the temporal structure of motor

activities within a certain activation sequence

3. The activation order of the swallowing

sequence is only partly fixed

4. It varies with bolus properties

5. It varies with bolus position

Problem no. 1: The pharyngeal swallowing sequence does not have an iterative motor-

temporal structure

As the pharyngeal swallowing sequence of Kendall et al. (2000) shows, swallowing is

composed of distinct motor events (swallowing gestures) that are activated in a particular

sequence with no repetition and therefore has no iterative structure:

Spstart>Aestart>H1>SPmax>Aeclose>PESop>H2>PESmax>HL>H3>Pamax>PEScl

SPstart=soft palate begins to elevate; Aestart=aryepiglottic folds begin to elevate; H1=hyoid bone begins to elevate;

Spmax=soft palate has reached maximal elevation; Aeclose=aryepiglottic folds contact the epiglottis;

PESop=pharyngoesophageal sphincter (PES) begins to open; H2=hyoid bone has reached maximal elevation; PESmax=PES

reaches maximum distension; HL=larynx approximates the hyoid bone; H3=hyoid begins to descend; Pamax=maximum

pharyngeal constriction; PEScl=PES closes

Of the swallowing motor events only mastication is iterative but since mastication is subject

to a greater degree of voluntary control, it seems to be a questionable example of

neurological control by the CPGS.

Problem no. 2: Sensory integration of bolus properties is only in part linked to change in

frequency

With the assumption that sensory integration of bolus properties (volume,

viscosity/consistency) is linked to a modification of frequency, we would expect bolus

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properties to temporally affect onset times and activation lengths of the pharyngeal motor

events within a certain activation order.

The data in Kendall et al. (2000) partly support this expectation:

Fig. 3. Swallowing gesture timing related to increasing bolus volume: 1-ml liquid vs. 20-ml liquid; Kendall et al. 2000, adapted from Fig. 5, p. 81 B1=the first movement of the bolus from a stable or “hold” position that passes the posterior nasal spine, Spstart=soft palate begins to elevate, Aestart=aryepiglottic folds begin to elevate, H1=hyoid bone begins to elevate, Spmax=soft palate has reached maximal elevation, Aeclose=aryepiglottic folds contact the epiglottis, PESop=PES begins to open, H2=hyoid bone has reached maximal elevation, PESmax=PES reaches maximum distension, H3=hyoid begins to descend, PAmax=maximum pharyngeal constriction, PEScl=PES closes

Most of the expected motor events show simultaneously earlier onset, target and reset times

with increasing bolus volume related to faster oropharyngeal bolus transit (relative to the

bolus head).

However, a closer look at the data reveals that

some motor events differ with respect to the degree of temporal change caused by

increasing bolus volume (e.g., SPstart vs. PESop), and

some show no temporal change at all (H1)

The data show that subsequences of the pharyngeal swallowing sequence may behave

differently with respect to sensory integration of bolus properties. This is an unexpected fact

if it is assumed that sensory integration is linked to frequency change since frequency

change should affect the pharyngeal swallowing sequence in a continuous way.

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Problem no. 3: The activation order of the swallowing sequence is only partly fixed.

In a subsequent study, Kendall et al. (2003) presented data that show sequential variability in

the pharyngeal motor sequence. Only some subsequences of the swallowing sequence and

some relations between the bolus position and motor events of the swallowing sequence are

fixed. The following table shows the fixed relations:

Table 2. Constant motor-temporal relations

Constant motor-temporal relations:

Onset of arytenoid cartilage elevation (AE1) > onset of UES opening (UES1)

AE1 > UES1

Onset of UES opening (UES1) >= bolus head arrives at UES (BP-UES)

UES1 > BP-UES

Onset of UES opening (UES1) > maximum larynx-to-hyoid approximation (LA2)

UES1 > LA2

Maximal distension of the UES (UES2) > maximum pharyngeal constriction (PC2)

UES2 > PC2

Kendall et al. 2003, adapted from Table 4, 6, 9, 12, p. 88-89 (1-ml, 3-ml, and 20-ml liquid bolus)

However, according to data from Kendall et al. (2003), most of the motor-temporal relations

of the pharyngeal swallowing sequence are partly or even totally free:

Table 3. Variable motor-temporal relations

Variable motor-temporal relations: (second percentage=reverse order)

1-ml liquid 2-ml liquid 20-ml liquid

Maximum aryepiglottic fold elevation (to the point of supraglottic closure) > maximum hyoid elevation

AE2 > HE2 85% vs. 15% 88% vs. 12% 100% vs. 0%

Onset of the UES opening > maximum hyoid elevation

UES1 > HE2 51% vs. 49% 70% vs. 30% 97% vs. 3%

Maximum aryepiglottic fold elevation (to the point of supraglottic closure) > onset of the UES opening

AE2 > UES1 78% vs. 22% 88% vs. 12% 84% vs. 16%

Maximum aryepiglottic fold elevation (to the point of supraglottic closure) > the head of the bolus arrives at the UES

AE2 > BP-UES 93% vs. 7% 90% vs. 12% 86% vs. 14%

Maximum aryepiglottic fold elevation (to the point of supraglottic closure) > maximum larynx to hyoid approximation

AE2 > LE2 98% vs. 2% 96% vs. 4% 100% vs. 0%

Upper oesophageal sphincter reached its widest opening > maximum larynx to hyoid approximation

UES2 > LE2 74% vs. 26% 79% vs. 21% 90% vs. 10%

Maximum hyoid elevation > UES reached its widest opening

HE2 > UES2 93% vs. 7% 90% vs. 10% 68% vs. 32%

Maximum hyoid elevation > maximum pharyngeal constriction

HE2 > PC2 84% vs. 16% 86% vs. 14% 88% vs. 12%

Kendall et al., 2003, adapted from Table 2,3,5,7,8,10,11,13, p. 88–90

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In the table the second percentage shows the reverse order of the respective subsequence.

The data demonstrate a range of different degrees of sequential variability, from relatively

fixed to relatively or even completely free. In most cases variability was greater with small

bolus volumes.

There was no constant complete pharyngeal motor sequence with all swallows and all bolus

volumes. The most common sequence of a certain length

AE2>UES1>HE2>UES2>LE2>PC2

was associated with only 25% of the observed swallows.

Variability in the pharyngeal motor sequence cannot be expected under the iterative CPGS

hypothesis, because iterative CPGs control the temporal structure of motor events within a

certain activation sequence generated by the connected motor system.

Problem no. 4: The activation order of the swallowing sequence varies with bolus properties.

Comparable to the data of Kendall et al. (2003), Mendell & Logemann (2007) found a partly

variable and, with respect to order, bolus-dependent pharyngeal swallowing sequence:

Table 4. Frequency of temporal sequences observed for each bolus type

Sequence 3-ml liquid 10-ml liquid 1-3-ml paste

LE-HE-BOT-LC 24 8 20

HE-LE-BOT-LC 23 12 42

LE-HE-LC-BOT 17 38 2

HE-LE-LC-BOT 14 25 7

(HE=LE)-BOT-LC 13 2 23

Each cell represents the number of participants who followed this pattern (n=100). LE=onset of laryngeal elevation, defined as the first displacement in movement at the area of the posterior vocal folds and arytenoid area, HE=onset of hyoid elevation, BOT=onset of tongue base movement toward the posterior pharyngeal wall, LC=first frame showing complete laryngeal closure; Mendell & Logemann, 2007, adapted from Table 4, p. 1264

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The table shows variable subsequences between the onsets of hyoid elevation, tongue base

retraction and laryngeal elevation, which was identified by arytenoid movement, as well as

complete laryngeal closure. The sequential order was rather free with low bolus volume and

viscosity and shows a more fixed order with increasing bolus volume and viscosity.

Of particular interest was the activation order of tongue base retraction, laryngeal closure

and UES opening:

Fig. 4. Fronting of laryngeal closure and UES opening with increasing bolus volume. HE=onset of hyoid elevation, BOT=onset of tongue base movement toward the posterior pharyngeal wall, LC=first frame showing complete laryngeal closure, UES=onset of upper esophageal sphincter (UES) opening; Mendell & Logemann, 2007, adapted from Table 4+5, p. 1264 (3-ml liquid, 10-ml liquid, 1-3-ml paste)

With low bolus volume the activation order of these motor events corresponds to the order of

swallow phases and the sequence was mostly initiated by oral tongue base retraction and

terminated by pharyngeal UES opening. If the bolus volume increases, however, the Mendel

& Logemann data show that this may speed up the motor response by means of motor-

temporal fronting of UES opening (UES) and laryngeal closure (LC) before the onset of

tongue base retraction (BOT). Such structures do respond to high bolus volumes causing

accelerated bolus transit with a combination of earlier airway protection and earlier UES-

opening. Motor-temporal transformations cannot be expected with the iterative CPGS

hypothesis, since they change the activation order of a motor sequence beyond modification

of internal time intervals. Fronting of UES opening and laryngeal closure generates a

qualitatively different pharyngeal sequence, which is specialised with respect to high bolus

volume and fast bolus transit.

Problem no. 5: The activation order of the swallowing sequence varies with the bolus

position.

Unlike the widespread concept of ‘delayed pharyngeal swallow’, the swallow onset,

identifiable by the onset of hyoid movement, is not invariably synchronised with trigger areas

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in the posterior oral space. Up to 80% of normal subjects swallow late, that is, with

pharyngeal bolus positions at swallow onset but without subsequent decrease in airway

protection (Martin-Harris et al., 2007). Pharyngeal bolus positions at swallow onset are a

normal feature of non-instructed spontaneous swallows (Dua et al., 1997), of swallows with

bolus accumulation in the valleculae during mastication (Hiiemae & Palmer, 1999), of

sequential swallows (Daniels & Foundas, 2001) and of swallows of healthy elderly (Leonard

& MCKenzie, 2006). Therefore, it is necessary to distinguish between late swallows with

pharyngeal bolus positions at swallow onset and sufficient airway protection and delayed

swallows with pharyngeal bolus positions at swallow onset and reduced airway protection.

Late swallows without reduced airway protection are possible because there is an early level

of airway protection that is independent of epiglottic closure (Rüffer, 2012):

Fig. 5. Early airway protection in case of late swallows; Rüffer, 2012, adapted from Fig. 9, p. 52

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This early level of airway protection is based on several factors:

Anatomy: Spaces within the pharynx (valleculae, lateral pharyngeal channels, pyriform sinuses) are able to contain bolus material that has reached the pharynx before swallow onset thereby reducing the probability of penetration.

Dwell time: There is a time slot between the time point where bolus material enters the pharynx before swallow onset and decrease of airway protection (Dua et al., 1997).

Arytenoid movement: Early onset of arytenoid adduction and elevation reconfigures the laryngeal vestibule and its surroundings and increases airway protection at the biomechanical level (Dua et al., 1997).

Swallow-related apnoea: Early onset of swallow-related apnoea prevents aspiration of bolus material (Martin-Harris et al., 2007).

Of particular interest with respect to the connection between the bolus position and the

activation order of the swallowing sequence is arytenoid movement. While full arytenoid

adduction and elevation is localised after the onset of hyoid elevation and results in glottic

closure as well as arytenoid to epiglottic closure, the onset of arytenoid adduction and

elevation is shifted before the onset of hyoid elevation in case of late swallows.3 This early

movement leads to modification of the laryngeal vestibule and its surroundings by widening

the lateral pharyngeal channels, closing the interarytenoid space and heightening the barrier

of the aryepiglottic folds. It contributes to airway protection at the biomechanical level

because it reduces the probability that liquid boluses entering the hypopharynx before

swallow onset will overflow into the laryngeal vestibule. Together with the other factors in

early airway protection, fronting of arytenoid movement enables late swallows with sufficient

airway protection.

As late swallows demonstrate, the activation order of the pharyngeal swallowing sequence

may vary with bolus position. Both bolus properties and bolus position may induce motor-

temporal change of the pharyngeal swallowing sequence which goes beyond modification of

temporal distances within a certain activation order, a fact that is not expected under the

iterative CPGS hypothesis.

The data from Kendall, Mendell & Logemann and others challenge the assumption that the

CPGS is similar to iterative CPGs. The motor-temporal structure of swallowing has features

that are not expected with the assumption of iterative CPG control. The pharyngeal 3 Data from Mendell & Logemann (2007) provide evidence of a variable activation order for the onsets of arytenoid elevation and hyoid elevation in case of small bolus volume (see Table 4). We hypothesize that – apart from the influence of bolus volume – this variable order of the onsets of arytenoid movement and hyoid elevation is a feature of early swallows. It can be assumed that Mendell & Logemann saw early swallows mainly because they observed instructed swallows in a videofluoroscopy setting.

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swallowing sequence does not include iterative loops, is in part variable, and bolus properties

as well as bolus position may induce motor-temporal transformations of the sequence. The

data show that the motor-temporal structure of swallowing is much more variable and

context-sensitive than one would expect with the assumption of the iterative CPGS

hypothesis. Since variability and context sensitivity are features of voluntary movement,

pharyngeal swallowing seems to be closer to voluntary movement than usually expected. It is

voluntary movement and not reflexes or iterative movements that provide an adequate

blueprint for the pharyngeal swallow.

Elements of a new model for motor processing of swallowing

Let me focus on the question of how to explain the facts challenging the iterative CPGS

hypothesis. Unlike the iterative CPG model, we want to propose a model of motor planning of

swallowing that is based on two fundamental principles of motor processing which are not

specific to swallowing, namely motor coordination and motor learning:

Principles of motor processing

1. motor coordination

2. motor learning

We assume that there is no difference between swallowing and other motor activities with

respect to the basic principles of motor processing, which we identify with motor coordination

and motor learning. As the following assumptions show, the combined effects of motor

coordination und motor learning can explain the data that are problematic for the iterative

CPGS hypothesis:

1. Motor coordination

The neurological control of swallowing is based on a combinatory motor planning

process that coordinates muscle activities in a sequential and hierarchical way and

thus generates more complex muscle activities.

This can explain why sensory factors (bolus properties) may be correlated to

subsequences of the pharyngeal sequence (Kendall et al., 2000). Pharyngeal

subsequences correspond to intermediate levels of motor coordination.

2. Selective conditions for motor coordination

Swallowing motor coordination is free within selective conditions, leaving a range of

possible variations (voluntary movement as blueprint).

This can explain why the pharyngeal swallowing sequence is only fixed in part and

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may be subject to motor-temporal transformations (Kendall et al., 2003;

Mendell&Logemann, 2007).

3. Motor learning

Automaticity of swallowing is the result of motor learning.

This can explain why the pharyngeal swallow is reflexive without assuming that it is

controlled by an iterative CPG.

A closer look at 1–3 may clarify the concepts behind the proposed model for motor planning

of swallowing:

1. Motor coordination

Motor activities of a certain complexity are based on motor planning. Motor planning means

that a motor activity is not simply a response to a particular stimulus but that it is mediated by

some kind of computational process which integrates perception but does not map it directly

to motor activity. Elementary motor systems like reflexes are characterised by direct

stimulus-response mapping without motor planning. Possible evidence for motor planning

derives from the computational complexity and flexibility of a motor activity, although even

unspectacular motor activities such as pointing, for example, are presumably rather complex

(Shadmehr&Wise, 2005). We do not believe that motor planning presupposes voluntary

control. Speaking is an example of a motor activity that is certainly planned but nevertheless

not voluntarily controlled, at least under normal circumstances. Apart from the complexity

and flexibility of a motor activity, motor planning is also indicated by the ability of a motor

system to control and correct its output, which presupposes something like a comparison of a

motor plan with an actual motor output. Examples are preservation of function despite

developmental or age-related change in the biomechanical, neuromotor or sensory features

of a motor system (for example, change in biomechanical context due to growth). Further

possible evidence in support of motor planning is found in motor planning errors, that is,

apraxia. In the case of speech apraxia, speech movements are affected at the motor-

temporal planning level whereas the muscle level of speech is, in contrast to dysarthria,

intact (Ziegler & Cramon, 1986). Although we do not believe that motor planning is restricted

to cortical processing, if it can be demonstrated using an imaging technique – for example,

fMRI – that a motor activity relies on cortical processing, this could also be interpreted as

evidence of motor planning. This is particularly true if cortical processing precedes a

connected motor activity, which can be demonstrated with EEG data showing a pre-motor

potential (readiness potential (RP), Kornhuber & Deecke, 1965). Pre-activation is not a

requisite feature of motor planning, however, since motor planning can be nearly

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simultaneous with motor output as is true in the case of language planning and execution of

speaking (‘incremental production’, Levelt, 1989, pp 24–27). The swallowing motor system

has all the hallmarks of motor planning. It is able to flexibly synchronise its motor output with

bolus properties; it can control and correct its motor output, preserving its functionality even if

the biomechanical and neuromotor environment undergoes change, which is true both in the

development (Weckmueller et al., 2010) and ageing of the swallowing system

(Wilmskötter&Stanschus, 2012); it can be affected by motor planning errors (Huckabee &

Kelly, 2006); and it is at least in part controlled by cortical processing (Hamdy et al., 1999).

There is also some evidence that pre-activation is relevant for swallowing, at least for

volitional swallowing (Huckabee et al., 2003).

We assume that motor planning of swallowing (as well as motor planning in general) is

localised within a processing system that includes a motor grammar, which generates motor-

temporal structures or motor plans and that the swallowing motor response is the result of

mapping a motor plan into muscle activity:

Fig. 6. Motor processing

The planning level of a complex motor activity like swallowing must at least represent a

selection of a set of muscles along with temporal specification of the activation of each

muscle within the set. Motor planning is primarily a temporal process since what makes

muscles interact is their being simultaneously active. We therefore assume a syntactic rule

coordinate, generating motor plans by linking motor events with the same time feature:

17

Coordinate4

Coordinate two motor events X and Y to a complex motor event ME={t,{X,Y}}, where t is a

time feature

Motor-temporal structures based on the rule Coordinate can be seen as tree structures with

a hierarchy of temporally defined motor ‘constituents’:

Fig. 7. Motor tree

At the lowest coordination level, such structures – which we will call ‘motor trees’ – represent

activations of muscles or muscle fibres at a certain time point and at the next coordination or

time level the result of the first level coordination is coordinated in turn with further muscles

or muscle fibres and so on. The set-theoretical representations generated by Coordinate are

equivalent to motor trees as long as the hierarchical and not the serial order of motor trees is

identified with the activation order (sequence of onsets).

The term ‘motor event’ in Coordinate refers to muscle activities at different levels of motor

coordination. It differs from the term ‘swallowing gesture’ in that it is not restricted to motor

activities of intermediate complexity but includes also more elementary motor activities at the

level of single muscles or muscle fibres as well as more complex motor activities, such as the

anterior movement of the hyoid or the complete pharyngeal swallowing sequence.

Although Coordinate does not mention motor force, motor force is captured by Coordinate.

Within the proposed concept of motor coordination, differences in motor force simply relate to

differences in parallel coordination of muscle fibres at the same coordination or time level.

Hyoid movement is an example of motor coordination. Data from Pearson et al. (2010) reveal

that, at two time levels, the motor tree of hyoid movement coordinates the mylohyoid muscle

4 Coordinate is similar to the rule Merge of the minimalist syntax theory (Chomsky, 1995, p. 226). A main difference between Merge and Coordinate is that motor trees generated by Coordinate cannot be recursive since they do not include heads (like V in VP, for example).

18

of the suprahyoid muscle group, which seems to be primarily responsible for the superior

movement of the hyoid, with the geniohyoid muscle of the suprahyoid muscle group, on

which the anterior movement of the hyoid seems to be primarily based:

Fig. 8. Motor tree of hyoid movement

2. Conditions for motor coordination

We assume that motor coordination of swallowing at the planning level is free within certain

constraints. Constraints on swallowing motor coordination serve as output conditions that

filter out motor-temporal structures if they are lacking obligatory motor features. There are

two types of conditions for motor coordination: biomechanical and functional.

Biomechanical conditions for swallowing motor coordination

Motor systems are embedded into biomechanical systems or, to use Rodney Brooks’ term

from robotics, motor systems are ‘embodied’ (Brooks, 2002, p. 51). This embodiment has far-

reaching consequences for motor systems, because it makes both the output of motor

systems and motor coordination at the planning level depend on biomechanical features:

Fig. 9. Biomechanical effects on motor output and motor coordination

Laryngeal closure at the epiglottic level may illustrate the dependence of the output of the

swallowing system on biomechanics. Epiglottic closure is a complex biomechanical process

19

depending on the biomechanical features of the hyoid, larynx and epiglottis but at the muscle

level it is initiated simply by contraction of the suprahyoid musculature.

The effects of embodiment are not restricted to the output of the swallowing system however

because they also affect motor coordination at the planning level. The reason is that

biomechanical hardware and neuromotor control of motor systems must be adjusted. If there

is no adjustment between the biomechanical hardware and neuromotor control of a motor

system, there will be a decrease in motor optimality at least, if not a decrease in function.

Motor optimality is an important concept in the field of sports science (training theory) and

robotics that is also important for swallowing but has not yet been systematically applied to

swallowing (see Todorov, 2006 for an overview). Optimal movements – or ‘physiological

movements’ – are characterised by maximising temporal synchronisation and minimising

motor force. An example of the effects of embodiment on swallowing motor coordination is

that the onset of hyoid movement must take into account the biomechanically caused

temporal costs of the laryngeal movement. The activation order of the pharyngeal motor

sequence is also in part dependent on biomechanics:

Biomechanical conditions for swallowing coordination are evident with motor events

that are biomechanically dependent in a direct way. Hyoid elevation (HE) should

therefore precede laryngeal elevation (LE), epiglottic closure (EC) and UES opening

(UES): HE > LE > EC/UES

Other biomechanical conditions for swallowing coordination are related to the space

within which swallowing muscles must act. Epiglottic closure (EC) should therefore

precede pharyngeal constriction (PC), since early pharyngeal constriction would

biomechanically obstruct epiglottic closure: EC > PC

There are also biomechanical conditions related to pressure. Soft palate closure

(SPC) should therefore precede tongue base retraction (BOT) to enable tongue base

retraction generating enough pressure for bolus transit: SPC > BOT

Functional conditions for swallowing motor coordination

Although it is difficult to draw a sharp line between biomechanical and functional conditions

on swallowing motor coordination because biomechanical conditions also contribute to

swallowing functionality, it makes sense to differentiate between conditions for swallowing

that depend on the embodiment of the swallowing motor system and conditions that do not.

Biomechanically independent functional conditions for swallowing motor coordination are

related to synchronisation of bolus transit with the sequence of swallowing motor events.

20

This synchronisation should at least link bolus arrival at the laryngeal vestibule with laryngeal

closure at some level (airway protection) and bolus arrival at the UES with UES opening

(bolus transport). We assume hypothetically that this minimal requirement fulfils swallowing

functionality:

Fig. 10. Selective synchronisation Selective synchronisation implies a clustering of temporally fixed motor temporal relations

around the synchronisation points of laryngeal closure and UES opening and enables more

free motor coordination elsewhere. Martin-Harris et al. (2003) were the first to discover

motor-temporal clustering of the pharyngeal swallowing sequence with respect to related

respiratory events. Selective synchronisation should lead to further clustering with respect to

bolus transit.

Selective synchronisation enables sensory integration of bolus properties by transforming the

pharyngeal swallowing sequence. Fronting of UES opening and laryngeal closure in case of

high volume in the data of Mendell & Logemann (2007) is an example of this (see Fig. 4).

The swallowing system can respond to a change in bolus transit by varying bolus properties

with transformations of the pharyngeal swallowing sequence to preserve selective

synchronisation of laryngeal closure and UES opening with the bolus transit.

Selective synchronisation allows variable bolus positions at swallow onset as long as airway

protection is preserved (‘larynx closure at some level’). Although in conflict with the common

assumption in dysphagia research that swallows with pharyngeal bolus positions are always

delayed, this implication of selective synchronisation is supported by data showing that late

swallows with pharyngeal bolus positions and sufficient airway protection are a common

feature of normal swallowing (Martin-Harris et al., 2007; Dua et al., 1997; Hiiemae&Palmer,

1999; Daniels&Foundas, 2001; Leonard&McKenzie, 2006). As we have seen, late swallows

21

with sufficient airway protection are possible because there is an early level of airway

protection independent of epiglottic closure which is based in part on fronting of arytenoid

movement (see Fig. 5).

The fixed relations of the Kendall et al. (2003) data can be explained by the proposed

functionality of selective synchronisation of bolus transit with laryngeal closure and UES

opening together with biomechanical conditions:

Constant motor-temporal relations (Kendall et al., 2003)

Explanation in terms of conditions for motor coordination

Onset of arytenoid cartilage elevation (AE1) > onset of UES opening (UES1)

AE1 > UES1

Functional condition: Since the bolus reaches the laryngeal vestibule before UES for anatomical reasons, laryngeal closure – particularly at the arytenoid level – should precede UES opening to fulfil swallowing functionality with respect to airway protection

Onset of UES opening (UES1) >= bolus head arrives at UES (BP-UES)

UES1 >= BP-UES

Functional condition: the arrival of the bolus at the UES should be synchronised with UES opening to fulfil swallowing functionality with respect to bolus transport

Onset of UES opening (UES1) > maximum larynx-to-hyoid approximation (LA2)

UES1 > LA2

Biomechanical condition: UES should relax before maximal laryngeal elevation to enable laryngeal elevation to dilate the UES in time

Maximal distension of the UES (UES2) > maximum pharyngeal constriction (PC2)

UES2 > PC2

Biomechanical condition: Maximum pharyngeal constriction should be triggered late in the swallowing sequence to prevent biomechanical obstruction of laryngeal elevation which would obstruct UES opening

Tab. 6. Constant motor-temporal relations; left column contains data from Kendall et al., 2003

3. Motor learning

Since the facts do not support the assumption that swallowing is controlled by an iterative

CPG, the automaticity of the pharyngeal swallowing sequence cannot be explained by

iterative CPG control. We believe that motor learning provides an alternative explanation.

Automaticity of swallowing is based on improvement of swallowing motor coordination with

respect to bolus transport and airway protection, long-term storage of the resulting motor-

temporal patterns and activation of these stored patterns during swallowing:

22

Fig. 11. Motor learning

The assumption that automaticity of swallowing is based on motor learning does of course

not imply that the swallowing motor sequence is acquired by conscious learning. As pointed

out by Shadmehr&Wise (2005), ‘motor learning’ must be extended to biological learning of

unconscious sensory-motor functions, such as instinctive behaviour for example. Biologically

determined motor systems are acquired by genetic learning – evolutionary learning that

accrues over generations and becomes encoded genetically – and biological maturation.

With such an extended concept of motor learning, it is possible to trace the automaticity of

the pharyngeal swallow back to motor learning. How the swallowing motor system is

acquired based on genetic encoded principles and how this acquisition integrates experience

is unclear.

The integration of memorised motor-temporal structures makes the pharyngeal swallow

automatic and reflex-like (without being a reflex). Activating a pattern is always faster than

generating it. The drawback of increasing speed using pattern activation is a loss of flexibility,

however. The invariance of activated patterns in opposition to generated patterns does not

contradict the facts supporting variability of the pharyngeal motor sequence, as long as it is

assumed that activation of stored motor-temporal structures can be restricted to

subsequences of the pharyngeal motor sequence (selective synchronisation).

We assume that memorised motor-temporal structures are linked to bolus properties in

particular. Activation of motor plans that are specialised with respect to bolus volume or

bolus viscosity enables rapid synchronisation of the swallowing motor response with bolus-

induced variations in bolus transit. The data of Kendall et al. (2003) and Mendell &

Logemann (2007) support the assumption that if volume is high, a stored pattern with fronted

onset times is activated. The greater variability of the pharyngeal swallowing sequence in the

case of low bolus volume would follow if, in this case, no stored pattern is activated. A

preliminary hypothesis for stored motor-temporal structures that are specialised with respect

23

to bolus properties could be:

high volume + low viscosity: early onsets

low volume + high viscosity: late onsets

CPGS as motor memory

The discussion so far has underlined the need for rethinking the role of the ponto-medullary

region of the brain stem where the CPGS is assumed to be localised. If swallowing is not

controlled by an iterative CPG, what else might the role of the ponto-medullary region of the

brain stem be? It seems plausible, at least initially, that the motor memory of the swallowing

system is localised here. We therefore hypothesize that the CPGS is a motor memory which

emerged from ontogenetic development of swallowing motor coordination leading to long-

term storage of motor-temporal patterns. Following the extension of motor learning to

biological learning by Shadmehr&Wise (2005), it is evident that motor memories are not

restricted to cortical motor processing. The CPGS might be an example of an implicit or non-

declarative subcortical motor memory that is specific for swallowing. Although dysphagia

research has provided some insight into motor processing at the CPGS level, such as

identification of the ‘programming interneurons responsible for the spatio temporal

organization of the swallowing motor sequence’ (Amri et al., 1990, p. 384), a theory of the

CPGS as motor memory is still outstanding.

Cortical swallowing processing integrates the output of the CPGS motor memory into a

superior planning process that captures bolus properties that are not yet integrated at the

brain stem level (olfactory and optic bolus properties). Although the specific role of cortical

motor processing of swallowing apart from higher sensory integration is unclear, it can be

hypothetically assumed that cortical embedding enables a shift from activation of stored

motor-temporal structures to generation of motor-temporal structures by motor coordination.

Given an appropriate feedback, pharyngeal motor coordination becomes voluntarily

accessible and changeable to a certain extent, despite its automaticity, as swallowing

manoeuvres such as the ‘Mendelsohn manoeuvre’ show. This opens up opportunities for

swallowing rehabilitation.

24

Summary and Discussion

The following model summarises the assumptions made for motor processing of swallowing

as proposed in this paper:

Fig. 12. Motor processing of swallowing

Complexity and flexibility in the swallowing motor system with respect to sensory integration

of bolus features (volume, viscosity, position) as well as other data support the assumption

that swallowing is not simply a response to a stimulus related to the bolus but is based on a

process of motor planning that integrates perception related to the bolus but does not map it

directly to motor activity as basic reflexes do. However, data on the motor-temporal structure

of the pharyngeal swallowing sequence also contradict the assumption that motor planning of

swallowing is mediated by an iterative CPG. The pharyngeal swallowing sequence differs

from iterative movements: it does not include motor-temporal loops, sensory integration of

bolus properties is not restricted to a change in motor-temporal relations within a certain

25

activation order of the sequence (frequency change), the activation order of the sequence is

in part variable, and it is subject to motor-temporal transformations related to bolus properties

and bolus position. To explain these facts we have proposed a model for motor processing of

swallowing that is based on motor coordination and motor learning, two basic principles of

motor processing, which are not specific for the swallowing system. We assume that every

motor activity with a certain complexity – including swallowing – is based on a free

combinatory process of motor planning, constrained by biomechanical and functional output

conditions. Motor learning leads to storage of coordinated motor-temporal structures in motor

memories and enables rapid motor responses by activation of those structures.

In the case of swallowing, free motor coordination limited by biomechanical and functional

output conditions leads to a pharyngeal swallowing sequence that is not completely

temporally ordered. Apart from biomechanical conditions, the temporal order of the

pharyngeal swallowing sequence is based on selective synchronisation of laryngeal closure

and UES-opening with pharyngeal bolus transit, leading to motor-temporal clusters around

these synchronisation points and less motor-temporal order elsewhere. The response to

bolus properties affecting bolus transit (high volume or high viscosity) is activation of

specialised motor temporal structures, stored in the CPGS, which cause motor-temporal

transformations of the pharyngeal sequence to preserve selective synchronisation.

Localisation of the motor memory of the proposed processing model within the medullary

region of the brain stem, where the CPGS is assumed to be situated, is a first step towards

clarifying localisation of the whole processing model. We hypothetically assumed that a shift

from activation to generation of motor-temporal structures by the rule ‘coordinate’ is

associated with a shift to cortical processing. Although this is prima facie a plausible

assumption, it is unclear if motor coordination is restricted to cortical processing. The

characteristic feature of motor temporal structures generated by ‘coordinate’ is variability, in

contrast to the invariance of memorised motor temporal structures. If we look at the sensory-

motor systems of animals, however, the data contradict the assumption that absence of

cortical processing excludes variability. The sensory-motor systems of animals can be

variable and flexible with respect to integration of perception and generation of motor

response even if there is no cortex at all. Returning to swallowing, the question is whether

subcortical motor planning of swallowing can play a role beyond storing motor-temporal

structures. The identification of ‘programming’ interneurons within the medullary region of the

brainstem (Amri et al., 1990) indicates that this may be the case.

26

This paper is intended to be a step towards explaining the concept of motor planning of

swallowing. If the goal is to explore the motor planning of swallowing, localising brain regions

which have motor functions associated with swallowing is not sufficient. What is needed

beyond localisation is an attempt towards developing a theory that makes explicit the

computational structure – the algorithm – of swallowing motor planning. With the motor

grammar of swallowing outlined in this paper, we intended to take a first step towards this.

The attempt to clarify motor planning at the computational level might be brought into doubt

because it still has a weak data pool, however. In fact, techniques to visualise neuromotor

function such as Functional Magnetic Resonance Imaging (fMRI) are not yet specific enough

to allow identification of aspects of motor planning in sufficient detail. On the other hand, we

are certainly not left empty-handed. Videofluoroscopy (VFS), possibly combined with

complementary techniques such as Electromyography (EMG), gives us some access to

motor planning. VFS data provide an insight into motor planning because they provide an

insight into the motor-temporal structure of swallowing. If it is true that motor coordination is

primarily a temporal process, as we assumed with the motor grammar rule ‘coordinate’, then

it can be assumed that motor-temporal data mirror motor planning. Temporal VFS data

provide a possible but not optimal data pool for a computational theory of motor planning of

swallowing, however, since VFS does not provide direct access to muscle activity but only to

muscle activity within a certain biomechanical context (embodiment). Therefore, if future

imaging techniques will some day enable visualisation of muscle activity and neuromotor

control of muscles, then this will provide a better data pool than the current temporal VFS

data. Until then, temporal VFS data are not optimal but are nevertheless sufficient to

empirically validate attempts to develop a computational theory of motor planning of

swallowing.

If this paper is to be an appropriate step towards developing a computational theory of motor

planning of swallowing, the next steps should include the following:

1. Coordinate

We proposed a motor plan of hyoid elevation in terms of Coordinate based on data

from Pearson et al. (2010). A description of other oral and pharyngeal motor events in

terms of Coordinate is outstanding.

2. Motor constituents

Swallowing gestures such as hyoid elevation or tongue base retraction describe

swallowing at an intermediate level of motor coordination. Given the proposed

concept for motor coordination, both more elementary and more complex (temporally

defined) motor ‘constituents’ should be also relevant for motor planning of swallowing,

27

however. It should be a goal of future research to explore this ‘constituent structure’

of swallowing motor plans.

3. Biomechanical constraints

Although dysphagia research has discovered many of the biomechanical constraints

on swallowing, a specific theory of biomechanical conditions for swallowing motor

coordination has not yet been developed.

4. Selective synchronisation

Is it true that synchronisation of bolus arrival at the laryngeal vestibule with laryngeal

closure at some level and bolus arrival at the UES with UES opening satisfies

swallowing functionality? Are there other synchronisation points?

5. Specialised motor-temporal structures

Given that sensory integration of bolus properties is linked to activation of specialised

motor-temporal structures, what structures can be identified?

28

References

Amri M, Car A & Roman C (1990): Axonal branching of medullary swallowing neurons projecting

on the trigeminal and hypoglossal motor nuclei: demonstration by electrophysiological and

fluorescent double labeling techniques. Exp Brain Res (1990) 81:384-390

Brooks RA (2002): Robot: The Future of Flesh and Machines. The Penguin Press.

Chomsky N (1995): The Minimalist Program. Cambridge/London: MIT Press.

Daniels SK & Foundas AL (2001): Swallowing Physiology of Sequential Straw Drinking.

Dysphagia 16:176–182.

Daniels SK & Huckabee M-L (2008): Dysphagia following stroke. San Diego/Oxford/Brisbane:

Plural Publishing.

Dua KS, Ren J, Bardan E, Xie P, Shaker R (1997): Coordination of Deglutitive Glottal Function

and Pharyngeal Bolus Transit During Normal Eating. Gastroenterology 112:73–83.

Fagerstedt P & Ullén F (2001): Lateral Turns in the Lamprey. I. Patterns of Motoneuron Activity. J

Neurophysiol 86:2246–2256.

Hamdy S, Mikulis DJ, Crawley A, Xue S, Lau H, Henry S & Diamant NE (1999): Cortical activation

during human volitional swallowing: an event-related fMRI study. Am J Physiol Gastrointest Liver

Physiol 277:219-225, 1999.

Hiiemae KM & Palmer JB (1999): Food Transport and Bolus Formation during Complete Feeding

Sequences on Foods of Different Initial Consistency. Dysphagia 14:31–42.

Hooper SL (2001): Central pattern generators. ENCYCLOPEDIA OF LIFE SCIENCES, John

Wiley & Sons, Ltd., www.els.net.

Huckabee M-L & Kelly B (2006): Rehabilitationsmodelle im Management von Dysphagien:

Kasuistiken zur Schluckapraxie und zur Spastischen Dysphagie. In: Stanschus S (ed.):

Rehabilitation von Dysphagien. Idstein: Schulz-Kirchner Verlag, 2006, pp 137–171

Huckabee M-L, Deecke L, Cannito MP, Gould HJ, Mayr W (2003): Cortical Control Mechanisms in

Volutional Swallowing : the Bereitschaftspotenzial. Brain Topography 16:3–17.

Kendall KA, Leonard RJ, McKenzie SW (2003): Sequence Variability During Hypopharyngeal

Bolus Transit. Dysphagia 18(2):85–91.

Kendall KA, McKenzie S, Leonard RJ, Goncalves MI, Walker A (2000): Timing of Events in

Normal Swallowing: A Videoflouroscopic Study. Dysphagia 15:74–83.

Kornhuber H.H. & Deecke L. (1965): Hirnpotentialänderungen bei Willkürbewegungen und

29

passiven Bewegungen des Menschen: Bereitschaftspotential und reafferente Potentiale. Pflügers

Arch 284: 1–17

Lang IM (2009): Brain Stem Control of the Phases of Swallowing. Dysphagia 24:333–348.

Leonard R & McKenzie S (2006): Hyoid-Bolus Transit Latencies in Normal Swallow.

Dysphagia:183–190.

Levelt WJM (1989): Speaking. From Intention to articulation. MIT Press, Cambridge

(Massachusetts)/London (England)

Martin-Harris B, Brodsky MB, Michel Y, Lee F-S, Walters B (2007): Delayed Initiation of the

Pharngeal Swallow : Normal Variability in Adult Swallows. Journal of Speech, Language, and

Hearing Research 50:585–594.

Martin-Harris B, Brodsky MB, Price CC, Michel Y, Walters B (2003): Temporal coordination of

pharyngeal and laryngeal dynamics with breathing during swallowing: single liquid swallows. J

Appl Physiol. 94:1735–1743.

Mendell DA & Logemann JA (2007): Temporal Sequence of Swallow Events During the

Oropharyngeal Swallow. Journal of Speech, Language, and Hearing Research 50:1256–1271.

Pearson WG Jr, Langmore SE, Zumwalt AC (2010): Evaluating the Structural Properties of

Suprahyoid Muscles and their Potential for Moving the Hyoid. Dysphagia online: 11 November

2010

Rüffer, N (2012): Late Swallows. DysphagiEforum 1/2012, p. 40-56

Shadmehr R & Wise SP (2005): The Computational Neurobiology of Reaching and Pointing. MIT

Press, Cambridge (Massachusetts)/London (England)

Todorov E (2004): Optimality principles in sensorimotor control (review). Nat Neurosci. 2004

September; 7(9): 907–915.

Weckmueller J, Easterling C & Arvedson J (2010): Preliminary Temporal Measurement Analysis

of Normal Oropharyngeal Swallowing in Infants and Young Children. Dysphagia online: 9 June

2010

Wilmskötter J & Stanschus S (2012): Presbyphagie - im Alter wird alles schlechter?.

Sprachheilarbeit 57 (2012), 2-11

Ziegler W., von Cramon DY (1986): Timing deficits in apraxia of speech. European Archives of

Psychiatry and Neurologic Sciences. 1986;236:44-49