Influence of the shape of intracellular

potentials on the morphology of single-fiber

extracellular potentials in human muscle
fibers

Javier Rodriguez-Falces, Javier Navallas,

Luis Gila, Armando Malanda & Nonna
Alexandrovna Dimitrova

Medical & Biological Engineering &

Computing

ISSN 0140-0118

Med Biol Eng Comput

DOI 10.1007/s11517-012-0879-7

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Med Biol Eng Comput
DOI 10.1007/s11517-012-0879-7
ORIGINAL ARTICLE
Influence of the shape of intracellular potentials
on the morphology of single-fiber extracellular
potentials in human muscle fibers
Javier Rodriguez-Falces • Javier Navallas •
Luis Gila • Armando Malanda •
Nonna Alexandrovna Dimitrova
Received: 18 December 2011 / Accepted: 24 February 2012
Ó International Federation for Medical and Biological Engineering 2012
Abstract Attention of the investigators is usually pointed
to the peak-to-peak characteristics of single-fiber action
potentials (SFAPs) that are mainly determined by the
depolarizing phase of the intracellular action potential
(IAP). However, the final portion of the SFAP has often
specific shape that has to be related to peculiarities of the
repolarization phase of IAP and the duration of its spike. A
novel piecewise SFAP model is proposed to achieve
greater insight into the nature of declining portion of the
negative phase and of the third phase of SFAP. It was
found that the SFAP third phase is essentially determined
by the specific profile of the transition of the IAP falling
phase toward the resting voltage, whereas the SFAP
declining negative phase is more dependent upon the width
of the corresponding IAP spike. We tentatively suggest that
the duration of the spike of human IAPs should be over
approximately 0.75 ms.
J. Rodriguez-Falces  J. Navallas  A. Malanda
Department of Electrical and Electronic Engineering, Public
University of Navarra, 31006 Pamplona, Spain
Present Address:
J. Rodriguez-Falces (&)
Universidad Pública de Navarra D.I.E.E, Campus de Arrosadı́a
s/n, 31006 Pamplona, Spain
e-mail: javier.rodriguez@unavarra.es;
javier.rodriguez.falces@gmail.com
L. Gila
Department of Clinical Neurophysiology, Virgen del Camino
Hospital, 31008 Pamplona, Spain
N. A. Dimitrova
Institute of Biophysics and Biomedical Engineering, Bulgarian
Academy of Sciences, 1113 Sofia, Bulgaria
Keywords Intracellular action potential  IAP spike
duration  SFAP third phase  SFAP morphology
1 Introduction
Since the advent of single-fiber electromyography
(SFEMG), a number of studies have analyzed the mor-
phological aspects of experimental single muscle fiber
potentials (SFAPs) in human fibers [11, 12, 35, 36]. Greater
insight into the SFAP generation was obtained from theo-
retical models that permits calculating the SFAP in terms of
the volume conductor properties, position of the recording
site with respect to the active fiber, and the intracellular
action potential (IAP) [2, 4, 7, 17, 26, 29, 34]. The most
critical aspect of SFAP formulations is the IAP description
chosen, since, at short fiber-to-electrode (radial) distances,
SFAP characteristics are essentially determined by the IAP
waveform and duration [6, 8, 11, 29, 34].
The accuracy of SFAP models is predominantly related to
their ability to generate potentials as similar as possible to
experimental recordings. The majority of studies evaluate
the resemblance between measured and computed SFAPs by
analyzing only the features of the SFAP principally depen-
dent upon the IAP depolarization phase: peak values of the
first two phases, peak-to-peak duration, and peak-to-peak
voltage [11, 14, 31, 37]. However, limited knowledge still
exists about the SFAP characteristics more dependent upon
the IAP repolarization phase: namely, the time course of the
declining negative phase of the SFAP and its third phase [11].
The reason for this is that the last portion of the SFAP has
longer duration and thus much lower frequency content than
the SFAP rising phase and therefore it is markedly more
affected by slow components, such as potentials from the
cannula or from distant fibers, or by filter settings.
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Inability to determine when (and to what extent) the
terminal portion of the SFAP is contaminated by nearby
fibers or by technical factors [11] partially explains the
relative uncertainty about the character of the repolariza-
tion phase of the IAP in human muscle fibers. An imme-
diate consequence of this incertitude is that, in the last
decades, authors have used different descriptions for the
IAP with large discrepancies in the duration of the spike.
The IAP spike duration can be estimated as the depolar-
ization–repolarization time (DRT) [32]. The well-known
IAP analytical expression defined by Rosenfalck [34] had a
spike with a DRT of *1.0 ms (Fig. 3 of the cited paper).
The IAP approximation used by Andreassen and Rosen-
falck [4] was based on the in vitro human IAP recorded by
Ludin [23], which had a DRT of *0.75 ms. In an attempt
to accommodate the characteristics of simulated SFAPs to
those of real recordings, Nandedkar and Stålberg [26]
modified Rosenfalck’s IAP model by dividing the time
scale by two, and therefore obtaining an IAP with a DRT of
*0.50 ms.
Subsequent authors who used the Nandedkar and Stål-
berg IAP’s description [10, 13, 25] did not perceive that
certain morphological aspects of SFAPs simulated with this
particular IAP were not found in experimental potentials.
As an example, computed SFAPs exhibit a well-defined
third phase, whereas SFAPs measured from humans appear
either biphasic (Fig. 1a, b) [11] or present a rather small
and prolonged third phase (Fig. 1c, d). Another remarkable
morphological feature that is frequently observed in human
SFAPs is an abrupt change in the slope of the declining
negative phase (Fig. 1c, d). Such a feature, hereafter
referred to as a slope-discontinuity point (S-D point), is not
observed in the SFAPs simulated using Nandedkar and
Stålberg’s model [26].
Traditionally, authors have investigated how alterations
in the asymmetry and duration of the IAP are translated into
variations of the SFAP shape [11, 14, 31, 37]. However,
when changing the characteristics of the IAP, the authors did
not have independent control over its de- and repolarization
phases, which limits their capability to interpret correctly the
changes in the shape of the resulting SFAP. In the present
paper, we have proposed an SFAP model that allows for
independent calculation of the two hypothetical potentials
that would arise from de- and repolarization phases of the
IAP. The ultimate objective of the present study is to use this
piecewise SFAP description to investigate the effects of
changes in the IAP falling phase (and IAP spike duration) on
the morphological characteristics of the last portion of the

Fig. 1 Superimposed 0.5

representations of four sets of 0.6 (a) (b)
consecutive SFAPs recorded
from the tibialis anterior muscle 0.4
using a single-fiber electrode.
0.2
Voltage (mV)

a, b Representative examples of
SFAPs with a biphasic shape.
0
c, d Representative examples of 0
SFAPs with an abrupt change in -0.2
the slope of the descending part
of the negative phase (i.e., the -0.4
slope-discontinuity point)
-0.6

-0.8 -0.5
0.5 1 1.5 2 0.5 1 1.5 2 2.5 3

1.5
(c) 0.8 (d)

1 0.6 S-D point

S-D point
Voltage (mV)

0.4
0.5
0.2

0
0

-0.5 -0.2

-0.4
0.5 1 1.5 2 2.5 3 1 1.5 2 2.5 3
Time (ms) Time (ms)

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SFAP and the way these characteristics change with the v  ðz0  vtÞ
fiber-to-electrode (radial) distance. IR(r; vtÞ ¼
½ðz0  vtÞ2 þ Kan  r 2 3=2
We hypothesize that the characteristics of the SFAP v  ðz0 þ vtÞ
third phase are directly related to the character of the þ ð2Þ
½ðz0 þ vtÞ2 þ Kan  r 2 3=2
transition of the IAP falling phase toward the resting
voltage. In addition, taking as a reference data from Parameters z0, Kan, v, and r were referred to as IR
experimental SFAPs, we raise the hypothesis that for an variables and by default their values were set to
S-D point to appear in the SFAP declining negative phase, z0 = 20 mm, Kan = 5 [4, 16, 34], v = 3.5 m/s [26, 27],
an IAP with sufficiently long spike duration is necessary. and r = 0.15 mm. A muscle fiber with a length of 90 mm
and a right semi-length of 40 mm were considered. The
time step (sampling interval) used in the simulations was
2 Methods 10 ls (100 kHz).

2.1 Dimitrov and Dimitrova SFAP convolutional
model
Simulations of SFAPs were performed using the model
proposed by Dimitrov and Dimitrova (D–D) [7]. In this
model, the fiber is considered as a time-shift invariant
system, and SFAPs can be expressed as a convolution of
the input signal and impulse response (IR) of the corre-
sponding system:
oIAPðtÞ
SFAP(tÞ ¼ Can   IR(tÞ
ot
The coefficient of proportionality, Can, is defined in [7].
The input signal is the first temporal derivative of the IAP,
qIAP(t)/qt. The impulse response (2) comprised the
anatomical [semi-lengths of the fiber (L1, L2 in mm)] and
physiological [anisotropy ratio (Kan), propagation velocity
(v, in mm/ms)] properties of the fiber, as well as the
detection conditions [radial distance (r, in mm), and
longitudinal distance of the electrode relative to the
endplate (z0, in mm)]. Equation 2 is an approximation of
the IR for the finite-length fiber case.
2.2 Description of three IAP models
Three different IAP models were used for the simulations, all
of them based on the IAP analytical expression proposed by
Dimitrov and Dimitrova [7]. These IAP descriptions were
convenient for our study, because they allowed the de- and
repolarization phases to change independently. Moreover,
they permitted an independent control of different portions
of the IAP falling phase, thereby enhancing the flexibility to
change the profile of this phase. The type-I IAP model had a
ð1Þ time course divided into four portions: the rising phase, the
rapidly falling phase, the transition phase and the slowly
falling phase (i.e., the after-potential) (Fig. 2a). The char-
acter of the rising (depolarization) phase is determined by
three coefficients: A1, A2, and A3 (3):
IAPdep ðtÞ ¼ A1  tA2 t  eA3 t ; 0  t  Tdep ð3Þ
The duration of the rising phase can be calculated as
Tdep = A2/A3. The point of steepest rise (d1) along this
phase occurs at Td1 , and is approximately Tdep/2 (Fig. 2a).
The time course of the repolarization (falling) phase of
the IAP is determined by three equations and three

Type-I IAP Type-II IAP Type-III IAP

100 100 100
Rising (a) Rising (b) Rising (c)
Rapidly Rapidly Rapidly
80 falling 80 falling 80 falling
Voltage (mV)

60 60 60
d1 d2 d2 d2

40 Transition 40 40
After-potential
Transition
Transition
20 Vspl 20 20
Td1 Tdep Td2 Tspl
0 0 0
0 0.5 1 1.5 2 0 0.5 1 1.5 2 0 0.5 1 1.5 2
Time (ms) Time (ms) Time (ms)

Fig. 2 a Time course of the type-I IAP model divided into four divided intro three portions. The curvature of the transition phase of
portions. Tdep is the duration of the IAP rising phase. d1 and d2 are the the type-II IAP is smaller than that of the type-I IAP and the type-III
points of steepest rise and decay, respectively, along the IAP spike. IAP has the transition with the smallest curvature
b, c Time courses of the type-II and type-III IAP models, respectively,

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parameters, namely Tspl, Vspl, and C1ap. The rapidly falling the after-potential, greater control of the transition of the
phase was approximated by a cubic spline function IAP falling phase toward a constant voltage value was
described in (4) obtained (see Fig. 2b, c). It should be mentioned that the
2  profile of type-I IAP approximated to that recorded by
t3 t
IAPFalling ðtÞ ¼ B1   ðTspl þ Tdep Þ  þ Tspl  Tdep  t Hanson [19] and Radicheva et al. [30], and the shape of
3 2
type-II IAP approached to that recorded by Wallinga et al.
Tdep  t  Td2 ð4Þ [39] or that simulated by Fortune and Lowery [15] on the
where basis of physiologic-realistic parameters. However, the
type-III IAP model exhibited a falling phase with a more
6  ð100  Tspl Þ gradual transition toward a constant voltage that was not
B1 ¼ ð5Þ
ðTspl  Tdep Þ3 found to correspond to any previously recorded IAP.
Tspl and Vspl are the coordinates of the spline function end
2.3 Definition of the duration of the IAP spike
on the time and potential axis, respectively (Fig. 2a). The
point of steepest decay (d2) of the falling phase occurs at
We defined the duration of the IAP spike or the depolar-
Td2 (Fig. 2), and can be calculated as
ization-to-repolarization time (DRT) as the time interval
ðTspl  Tdep Þ between the centers of mass of the positive (CM1) and
Td2 ¼ Tdep þ ð6Þ
2 negative (CM2) phases of the IAP first temporal derivative
The transition phase and after-potential phase were (Fig. 3b), as established in [32].
defined using differential equations as follows As shown in [32], because of the special architecture of
the D–D IAP, the point of steepest rise of the IAP depo-
dIAPTransition ðtÞ t  Td 2 larization phase (point d1, Fig. 3a) lies approximately at the
¼ 1  C1ap   IAPTransition ðtÞ
dt Tspl  Td2 center of mass of the positive phase of the IAP first
Td2  t  Tspl derivative. Similarly, the point of steepest decay of the IAP
ð7Þ repolarization phase (point d2, Fig. 3a) nearly coincides
with the center of mass of the negative phase of the IAP
dIAPAfter ðtÞ
¼ 0:9  IAPAfter ðtÞ Tspl  t  Tend ð8Þ first derivative. Thus, for the particular case of the D–D
dt
IAP, the DRT of the spike can be calculated approximately
where C1ap was a coefficient whose value was within the as Td2  Td1 . In addition, for the D–D IAP, points d1 and d2
range 0.001 and 0.5, depending on the IAP shape simulated. lie approximately at 50% of the IAP amplitude in the
The type-II and type-III IAP models were the same as depolarization and repolarization phases, respectively.
the type-I model but without the fourth phase. By removing From (6), it can be seen that Td2  Td1 nearly equals Tspl/2.

De-and repolarization phases Phases of the IAP first De-and repolarization components
of the IAP derivative of the SFAP
1
100 Depolarization Repolarization
phase
(a) 600
(b) 0.8 Depolarization SFAP (c)
phase EDep component
80 0.6
~ DRT 400
Voltage (mV)

Voltage (mV)

0.4
(mV / ms)

60 (0.5 ms)
CM1
d2 0.2
d1 DRT
200
40 0

20 0 -0.2

-0.4
CM2 Repolarization
0 ERep NPD
Td1 Tdep Td2 Tspl -200 -0.6 component
(0.5 ms)
-20 -0.8
0 0.5 1 0 0.5 1 2 2.5 3 3.5 4 4.5
Time (ms) Time (ms) Time (ms)

Fig. 3 a Time course of type-I IAP model in which the de- and
repolarization phases are represented using lines with open and closed
circles, respectively. The IAP has been truncated for the sake of
clarity. b Time course of the IAP first derivative, with two phases,
Edep and ERep, corresponding to the de- and repolarization phases of
the IAP, respectively. The depolarization-to-repolarization time
(DRT) is the time separation between the centers of mass of Edep
(CM1) and ERep (CM2). c Depolarization and repolarization compo-
nents of the SFAP that result from the convolution of Edep and ERep,
respectively, and the system impulse response. The duration of the
negative phase (NPD) is also indicated (color figure online)

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2.4 Definition of the depolarization and repolarization
components of the SFAP
To get more insight into the SFAP generation, let us con-
sider the two hypothetical potentials that would result from
the propagation of the de- and repolarization phases of the
IAP, separately, along the fiber (Fig. 3a). These potentials
were referred to as the de- and repolarization components
of the SFAP (Fig. 3c). These components were obtained by
splitting the time course of the IAP first derivative into the
two portions resulting from the de- and repolarization
phases of the IAP [EDep and ERep shown in (9) and (10),
respectively] and convolving each of these portions, sep-
arately, with the system impulse response (2).
 oIAPðtÞ
EDep ðtÞ ¼ ot 0  t  Tdep ð9Þ
0 Tdep \t  20 ms
 the corresponding SFAPs at r = 0.075 and 0.275 mm.
0 0  t  Tdep
ERep ðtÞ ¼ oIAPðtÞ ð10Þ
ot Tdep \t  20 ms
In Fig. 3c, the SFAP components arising from the IAP
de- and repolarization phases of Fig. 3a are represented
using lines with red, open and blue, closed circles,
respectively. Due to the linearity of the convolution
operation, summing both components provided the final
SFAP, drawn with solid line in Fig. 3c. Note that, whereas
the SFAP has a triphasic shape, the de- and repolarization
components are biphasic. Note also that the first zero
crossing of the SFAP approximately coincides with that of
the depolarization component, while the second zero
crossing of the SFAP is practically the same as that of
the repolarization component, this being true only for short
radial distances (less than *0.25 mm). Since the zero
crossings of de- and repolarization components are
determined by the points of steepest rise and decay of the
IAP time course, respectively, the duration of the negative
phase of the SFAP (NPD) approximately equals the DRT
of the corresponding IAP [32].
2.5 Simulation details
Three sets of simulations were carried out to analyze how
changes in the profile of the IAP falling phase (and in the
IAP spike duration) affected the morphological character-
istics of an SFAP and the way these characteristics varied
with radial distance. In all cases, variation of the IAP
duration was achieved by changing the character of the
falling phase: the rising phase was left unchanged. This
simplified the study and resulted in no loss of generality, as
the Tdep measured in IAPs of normal muscle fibers was
confined within the range 0.20–0.35 ms [23, 39]. The
coefficient values used to synthesize the rising phase of the
three IAP models were A1 = 25 9 107, A2 = 4.5, and
A3 = 14. For the three IAP models, the values of coeffi-
cient Tspl used to synthesize the IAPs with DRTs of 0.5,
0.75 and 1.0 ms were 1.0, 1.5 and 2.0 ms, respectively. The
values of coefficient Vspl utilized to generate the same IAPs
were 25, 20, and 15, respectively. The coefficient C1ap was
0.01 for the type-I and type-II IAP, whereas it was 0.1 for
type-III IAP. With the exception of radial distance, all other
impulse response variables (z0, Kan, and v) were fixed to their
default values. For the first two sets of simulations, de- and
repolarization components of SFAP associated with the
corresponding phases of IAPs were also calculated.
The first group of simulations investigated the effect of a
slowing of the IAP falling phase on the third phase of the
resulting SFAP for two different radial distances. To do
this, for each IAP model, we generated three IAPs with
different DRT values (0.50, 0.75, and 1.0 ms) and obtained
The second set of simulations studied the influence of
the IAP falling phase (and spike duration) on the declining
negative phase of the SFAP for three different radial dis-
tances. This was done by generating two type-I IAPs, one
short (DRT = 0.5 ms) and one long (DRT = 1.0 ms), and
calculating the corresponding SFAPs and de- and repolar-
ization components at r = 0.075, 0.175, and 0.275 mm.
These set of simulations were not replicated for type-II and
-III IAPs
The third group of simulations analyzed how the vari-
ation of the SFAP morphology with radial distance was
influenced by the spike duration of the IAP. To do this, for
each IAP model, we simulated three series of SFAPs, each
of them with a different value of IAP DRT, namely 0.5,
0.75, and 1.0 ms. Each series comprised seven potentials
generated at different radial distances (r was increased
from 0.10 to 0.28 in steps of 0.03 mm). We shall refer to
each of these series as r-varying SFAP series.
3 Results
3.1 Effect of changes in the IAP falling phase
on the SFAP third phase for different
radial distances
Irrespective of the radial distance and IAP typology,
broadening of the IAP spike (first column of Figs. 4, 5)
brought about similar changes in the corresponding SFAP
repolarization component (blue curves in the second col-
umn of Figs. 4, 5), namely: (1) a reduction in amplitude,
(2) an increase in the overall duration, (3) a smoother
(slower) time course, and (4) a displacement of the zero
crossing to the right. The specific profile of the IAP
falling phase also influenced the characteristics of the
repolarization component. An IAP with a falling phase
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returning abruptly toward the resting potential level, as
the type-I IAPs of Fig. 4a, gave rise to a large and sharp
repolarization component (blue lines in Fig. 4b). On the
contrary, an IAP with a falling phase decreasing more
gradually toward the resting value, as the type-III IAPs
shown in Fig. 4g, led to a smaller and more prolonged
repolarization component.
The third phase of the SFAP was the result of adding
the declining negative phase of the depolarization
component and the positive phase of the repolarization
component. Characteristics of these components
depended on the distance from the fiber to the recording
point.
At very short radial distances (*0.075 mm), the depo-
larization component (red curves in the second column of
Fig. 4), with a sharp shape and a rapid return toward the
baseline, hardly overlapped with the positive phase of the
repolarization component (blue curves in the same graphs)
and, consequently, its contribution to the SFAP third phase
was practically zero. This means that, at such short radial

De-and repolarization components

Set of type-I IAPs with different DRT at r = 0.075 mm SFAPs at r = 0.075 mm
100
(a) 1.5 (b) 1.5
(c)
80 1
1
Voltage (mV)

0.5
0.5
60
0
0
40 -0.5 -0.5
-1 -1
20
-1.5 -1.5
0
0 1 2 3 5 5.5 6 6.5 7 7.5 5 5.5 6 6.5 7 7.5

Set of type-II IAPs with different DRT

100
(d) 1.5 (e) 1.5
(f)
80 1
1
Voltage (mV)

· 0.5 0.5
60
0 0
40 -0.5 -0.5
-1 -1
20
-1.5 -1.5
0
0 1 2 3 5 5.5 6 6.5 7 7.5 5 5.5 6 6.5 7 7.5

Set of type-III IAPs with different DRT

100
(g) 1.5 (h) 1.5 (i)
80 1
1
Voltage (mV)

· 0.5 0.5
60
0 0
40 -0.5 -0.5
-1 -1
20
-1.5 -1.5
0
0 1 2 3 5 5.5 6 6.5 7 7.5 5 5.5 6 6.5 7 7.5
Time (ms) Time (ms) Time (ms)

Fig. 4 First row simulation of the effects of changes in the IAP spike distance of 0.075 mm. The IAP profiles utilized correspond to type-I
width (a) on the depolarization component (line with red, open IAP. Second and third rows the same as in the first row but using the
circles) and repolarization component (line with blue, closed circles) type-II and type-III IAPs, respectively. The IAP time courses in a, d,
of the SFAP (b), and on the third phase of the SFAP (c) at a radial and g have been truncated for the sake of clarity (color figure online)

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De-and repolarization components SFAPs at r = 0.275 mm

Set of type-I IAPs with different DRT at r = 0.275 mm
100 0.4
(a) (b) (c)
0.2 0.3
80
Voltage (mV)

0.1 0.2
60
0.1
0
40 0
-0.1
-0.1
20
-0.2
-0.2
0
0 1 2 3 5 5.5 6 6.5 7 7.5 5 5.5 6 6.5 7 7.5

Set of type-II IAPs with different DRT

100 0.4
(d) (e) (f)
0.2
0.3
80
Voltage (mV)

· 0.1 0.2
60
0.1
0
40 0
-0.1
-0.1
20
-0.2
-0.2
0
0 1 2 3 5 5.5 6 6.5 7 7.5 5 5.5 6 6.5 7 7.5

Set of type-III IAPs with different DRT

100 0.4
(g) (h) (i)
0.2
0.3
80
Voltage (mV)

· 0.1 0.2
60
0.1
0
40 0
-0.1
-0.1
20
-0.2
-0.2
0
0 1 2 3 5 5.5 6 6.5 7 7.5 5 5.5 6 6.5 7 7.5
Time (ms) Time (ms) Time (ms)

Fig. 5 The same as Fig. 4, but for a radial distance of 0.275 mm (color figure online)

distances, characteristics of the SFAP third phase (graphs
of the third column of Fig. 4) were essentially determined
by positive phase of the repolarization component, i.e., by
the character of the last portion of the IAP falling phase.
Thus, with the IAP rising phase unchanged, the longer and
more gradual the transition of the IAP falling phase toward
a resting potential level, the smaller and more prolonged is
the SFAP third phase.
At higher radial distances (*0.275 mm), the SFAP
depolarization component (red curves in the second col-
umn of Fig. 5) became wider and with a more gradual
return toward the baseline and, therefore, it affected
considerably the formation of the SFAP third phase. At
such distances, the declining negative phase of the depo-
larization component overlapped with the positive phase of
the repolarization component. Specifically, the narrower
the IAP spike, the shorter was the distance between these
components and, therefore, the higher the degree of over-
lapping (also cancelation) between them. This means that
the positive phase of the repolarization component will be
comparatively more affected by the negative phase of the
depolarization component for shorter-spike IAPs than for
wider ones. As a result, for each SFAP set, the differences
among the amplitudes of the third phases at 0.275 mm

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(third column of Fig. 5) are much lower than at 0.075 mm
(third column of Fig. 4).
3.2 Effect of changes in the IAP falling phase
on the SFAP declining negative phase
for different radial distances
In the first row of Fig. 6, we show a type-I IAP with a DRT
of 1.0 ms (Fig. 6a) and the corresponding de- and repo-
larization components and SFAP simulated at radial dis-
tances of 0.075 mm (Fig. 6b), 0.175 mm (Fig. 6c), and
0.275 mm (Fig. 6d). In the second row of this figure, we
show the same diagrams as in the first one but for a type-I
IAP with a DRT of 0.5 ms.
Let us focus first on the SFAP components arising from
the wide IAP (DRT = 1.0 ms, Fig. 6a) at 0.075 mm
(Fig. 6b). The falling phase of this wide IAP was markedly
longer than its rising phase (i.e., its spike is strongly
asymmetric) and, as a result, the repolarization component
(blue curves) had much lower amplitude, slower profile,
and more prolonged time course than the depolarization
component (red curves), these differences being more
pronounced at short radial distances, as can be seen in
Fig. 6b. At these short distances, the long temporal sepa-
ration between these components (*1.0 ms), together with
the abrupt manner in which the depolarization component
approached the baseline, made this component smaller than
the repolarization one for a short interval (between 3.3 and
3.7 ms in Fig. 6b). As a result of such an overlapping, a
well-defined discontinuity appeared in the slope of the
declining negative phase of the SFAP (i.e., an S-D point).
For the wide IAP, increasing the radial distance to
0.175 mm (Fig. 6c), left the amplitude and duration char-
acteristics of the repolarization component relatively
unchanged, whereas the depolarization one became sig-
nificantly smaller (Fig. 6c), smoother (slower), and with a
more gradual decline toward the baseline. Note the great
differences between the radial declines of these compo-
nents shown in Fig. 7b. Now, the declining phase of the
depolarization component approximately equaled the
repolarization component during the interval 3.4–3.6 ms
and, as a result, the S-D point became less pronounced. A
further increase of r up to 0.275 mm (Fig. 6d) permitted
the descending portion of the depolarization component to
be larger than the repolarization component for the entire
duration of the potential, giving rise to an SFAP without
S-D point.
The interactions between the SFAP components result-
ing from the narrow IAP were strikingly different from
those of the wide IAP. The short spike of this IAP was also
rather symmetric, which means that its rising and falling
phases had commensurate durations. As a result, the dif-
ferences in amplitude and duration between their corre-
sponding de- and repolarization components were not as

SFAP, de-and repolarization SFAP, de-and repolarization SFAP, de-and repolarization

IAPs with DRT = 1.0 ms components at r = 0.075 mm components at r = 0.175 mm components at r = 0.275 mm
0.6 0.3
100 (a) 1.5 (b) (c) (d)
1 0.4 0.2
Voltage (mV)

80
0.5 0.2 0.1
60
0 0 0
40 -0.5
-0.2 -0.1
20 -1
-0.4 -0.2
-1.5
0
0 0.5 1 1.5 2 2 2.5 3 3.5 4 4.5 2 2.5 3 3.5 4 4.5 2 2.5 3 3.5 4 4.5

IAPs with DRT = 0.5 ms

2 0.8 0.4
100 (e) (f) 0.6
(g) (h)
0.3
Voltage (mV)

80 1 0.4 0.2
60 0.2 0.1
0
0 0
40
-0.2 -0.1
-1
20
-0.4 -0.2
0
0 0.5 1 1.5 2 2 2.5 3 3.5 4 4.5 2 2.5 3 3.5 4 4.5 2 2.5 3 3.5 4 4.5
Time (ms) Time (ms) Time (ms) Time (ms)

Fig. 6 First row simulation of a type-I IAP with a DRT of 1.0 ms
(a) and its corresponding depolarization component (line with red,
open circles), repolarization component (line with blue, closed
circles), and SFAP (black solid line) at radial distances of
0.075 mm (b), 0.175 mm (c), and 0.275 mm (d). Second row the
same as in the first row but for a type-I IAP with a DRT of 0.5 ms.
The horizontal straight line shown in b and c indicates the interval
during which the repolarization component is greater than or equal to
the depolarization one, giving rise to the slope-discontinuity point
(color figure online)

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Fig. 7 IAPs (left column) and Radial decline of SFAP components

IAPs with DRT = 1.0 ms 8
radial declines of the peak-to-
peak amplitude (right column) 100 (a) (b)
of the depolarization (red, open
circles) and repolarization 6
80
(blue, closed circles)

Voltage (mV)
components within the range
0.03–0.3 mm for a long (first 60
4
row) and a short (second row)
type-I IAP (color figure online) 40
DRT = 1.0 ms
2
20

0 0
0 0.5 1 1.5 2 0 0.1 0.2 0.3

IAPs with DRT = 0.5 ms Radial decline of SFAP components

8
100 (c) (d)

80 6
Voltage (mV)

60
4

40

2
20
DRT = 0.5 ms
0 0
0 0.5 1 1.5 2 0 0.1 0.2 0.3
Time (ms) Radial distance (mm)

pronounced as in the case with the wide IAP. Additionally,
because of the proximity in time between the two SFAP
components (*0.5 ms), the second phase of the depolar-
ization potential overlapped to a large extent with the first
phase of the repolarization one (Fig. 6f). As a consequence,
the transition between the second and third peaks of the
resulting SFAP was rather smooth even at short radial
distances (black solid line in Fig. 6f).
From Fig. 7, it can be readily seen that the radial
declines of the depolarization and repolarization compo-
nents are much more similar for the narrow than for the
wide IAP. Thus, for the narrow IAP, increasing radial
distance from 0.075 to 0.175 and 0.275 mm led to depo-
larization and repolarization components more comparable
in terms of amplitude and duration (compare Fig. 6f–h). In
addition, for radial distances of 0.175 and 0.275 mm, the
second phase of the depolarization potential broadly
overlapped with the first phase of the repolarization one.
This explains why SFAPs simulated at these radial dis-
tances had a declining negative phase with a practically
constant slope, i.e., without an S-D point (black solid lines
in Fig. 6g, h).
Since the first portion of the IAP falling phase (i.e., from
the IAP peak to dipole d2) was the same for the three IAP
models, it can be assumed that the above results would be
practically identical for the SFAP components arising from
the type-II and -III IAPs.
3.3 Effect of changes in the IAP falling phase
on the variation of the SFAP waveform
with radial distance
Figure 8 shows, for each type of IAP (Fig. 5, left column),
three series of SFAPs simulated with three different values
of IAP DRT (0.5, 0.75, and 1.0 ms), each series consisting
of seven potentials generated at varying radial distances.
SFAP series contained in the first column of Fig. 8 were
simulated using IAPs with different shapes, but with the
same (narrow) spike width (DRT = 0.5 ms). As can be
seen, within each of these SFAP series, changes in the
radial distance brought about commensurate changes in the
whole SFAP waveform. Irrespective of the IAP profile and
radial distance, the descending portion of the negative
phases of these SFAPs exhibited a roughly constant slope.
In addition, only the SFAP series simulated with the type-I
and type-II IAP models (Fig. 8a, d) showed a well-defined
third phase. In the three SFAP series simulated with IAPs
of DRT = 0.75 ms (second column), increasing the radial
distance gave rise to marked reductions of the two first
peaks of the SFAP, while the decline in the SFAP third

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SFAP series simulated with type-I IAPs of different DRTs

1.5 1.5 1.5
(a) (b) (c)
S-D point
1 1 less pronounced 1
S-D point
Voltage (mV)

0.5 0.5 0.5

0 0 0

-0.5 -0.5 -0.5

-1 DRT = 0.5 ms -1 DRT = 0.75 ms -1 DRT = 1.0 ms

5.5 6 6.5 7 5.5 6 6.5 7 5.5 6 6.5 7

SFAP series simulated with type-II IAPs of different DRTs

1.5 1.5 1.5
(d) (e) S-D point (f)
1 1
less pronounced 1
S-D point
Voltage (mV)

0.5 0.5 0.5

0 0 0

-0.5 -0.5 -0.5

-1 DRT = 0.5 ms -1 DRT = 0.75 ms -1 DRT = 1.0 ms

5.5 6 6.5 7 5.5 6 6.5 7 5.5 6 6.5 7

SFAP series simulated with type-III IAPs of different DRTs

1.5 1.5 1.5
(g) (h) S-D point (i)
less pronounced
1 1 1
S-D point
Voltage (mV)

0.5 0.5 0.5

0 0 0

-0.5 -0.5 -0.5

-1 DRT = 0.5 ms -1 DRT = 0.75 ms -1 DRT = 1.0 ms

5.5 6 6.5 7 5.5 6 6.5 7 5.5 6 6.5 7
Time (ms) Time (ms) Time (ms)

Fig. 8 First row simulation of sets of SFAPs using the type-I IAP 0.1 to 0.28 mm (see ‘‘Methods’’ for details). Second and third rows
with DRT values of 0.5 (a), 0.75 (b), and 1.0 ms (c). Each set the same as in the first row but using the type-II and type-III IAPs,
comprises seven SFAPs simulated at increasing radial distances from respectively

phase was comparatively less prominent. In these series,
SFAPs simulated at short radial distances exhibited a
declining negative phase with visible changes in the slope.
In the three SFAP series synthesized with wide
(DRT = 1.0 ms) and strongly asymmetric IAPs (third
column), potentials detected at short distances displayed a
distinct S-D point in the descending portion of the negative
phase. In these series, the S-D point could be used as a
reference to divide the SFAP time course into two different
portions that were affected to different degrees by the same
change in radial distance: the portion delimited between the
SFAP onset and the S-D point underwent pronounced
changes in amplitude, whereas the terminal portion of the
SFAP (from the S-D point onwards) experienced much less
change in amplitude. In addition, irrespective of the IAP
typology and radial distance, the third phases of these
SFAPs were of very small amplitude and had a markedly
prolonged duration.

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4 Discussion
As pointed out by Dumitru [11], some morphological
aspects found in human SFAPs are not sufficiently well
accommodated by simulated potentials. Definite answers to
the discrepancies between measured and computed SFAPs
are not straightforward, as the formation of an SFAP is the
result of intricate interactions between the potential fields
produced by the de- and repolarization phases of its cor-
responding IAP, these interactions being strongly depen-
dent upon the fiber-to-electrode distance [32, 33]. The
model proposed in the present paper provides insight into
these interactions by combining an IAP description that
affords the possibility of making independent changes in its
de- and repolarization phases with an SFAP formulation
that allows computing separately the potentials arising
from these phases.
4.1 Relationship between the IAP falling phase
and the SFAP third phase
According to Dumitru’s study [11], the initiation of the IAP
repolarization phase essentially generates the SFAP third
phase. Our results, however, indicate that characteristics of
the SFAP terminal portion are more coupled to the specific
profile (curvature) of the last part of the IAP falling phase
(i.e., the transition phase) than to the outline of its first part
(i.e., the rapidly falling phase). This is clearly demonstrated
by the observation that an IAP with a transition with large
curvature leads to an SFAP third phase with a much larger
amplitude and shorter duration as compared to that
resulting from an IAP with a transition of smaller curvature
(compare IAPs and SFAPs of the first and third rows of
Fig. 4). Further support for this result has been provided by
Rosenfalck [34] who used a collection of IAPs recorded
from frogs and rats at different temperatures to calculate
SFAPs (Figs. 11 and 13 of the cited paper). In Rosenfalck’s
work, one can clearly appreciate that the specific shape of
the transition of the IAP falling phase toward the resting
voltage (at times the after-potential) is the characteristic
that most significantly affects the SFAP third phase, though
the author did not comment on this result. A similar con-
clusion can be obtained from subsequent simulation studies
that calculate the SFAP in terms of the IAP [25, 28, 37].
Radial distance has been shown to influence the formation
of the SFAP third phase. Increasing the distance from the
electrode to the active fiber brings about stronger interactions
between the potential fields produced by the IAP de- and
repolarization phases [32, 33], i.e., a higher degree of over-
lapping between the SFAP de- and repolarization compo-
nents. Specifically, for radial distances greater than
*0.275 mm (Fig. 5), the depolarization component affects
noticeably the two phases of the repolarization component
and, consequently, the SFAP third phase cannot be consid-
ered to depend only on the IAP falling phase.
The width of the IAP spike was also found to have a
profound influence on the SFAP third phase. This finding,
however, can be misleading because, in the present study,
broadening of the IAP spike was accompanied by a
lengthening (and slowing) of its falling phase (the rising
phase remained unchanged). Thus, the fact that widening
of the IAP results in an SFAP with smaller and more
prolonged third phase is not merely due to the longer time
separation between the SFAP de- and repolarization com-
ponents, but also, and especially, to the concomitant
elongation of the IAP falling phase (and the more gradual
transition of this phase toward a constant voltage) follow-
ing the IAP widening (Fig. 4).
Another important observation is that, when different
types of IAPs were simulated to have narrow spikes (of
DRT = 0.5 ms), the third phases of the resulting SFAPs
exhibit marked differences in amplitude and duration (first
column of Fig. 8). However, when these same IAPs were
synthesized so as to generate broad spikes (of DRT =
1.0 ms), the third phases of the corresponding SFAPs display
much more similar characteristics: they were all decidedly
small and less pronounced (second and third columns of
Fig. 8). The explanation for the above observation lies in the
fact that, when IAPs of different shapes are simulated with
the same DRT, the relative differences between their corre-
sponding falling phases decrease as the DRT increases.
The lack of an IAP model that affords introducing fine
modifications along its time course has led some authors to
unrealistic interpretations about the nature of the SFAP
third phase. As an example, Dumitru’s group [11], in their
search for the IAP specifications required to generate a
‘‘biphasic’’ SFAP, came up with the conclusion that the
duration of the IAP repolarization phase should be longer
than *23 ms. Such a conclusion is probably due to the fact
that Dumitru’s group used the IAP description of Gootzen
et al. [17], which does not permit introducing fine and
independent changes in the different portions of the IAP
falling phase. In fact, we have found that an IAP with a
DRT value of only *1.0 ms (i.e., with a duration of the
IAP falling phase of approximately 3.0 ms) is sufficient to
simulate SFAPs that can be considered as primarily
biphasic (Fig. 4). Therefore, Dumitru’s group overesti-
mated by a factor of 8 the duration of the IAP spike
required to generate practically biphasic SFAPs.
4.2 Relationship between the IAP falling phase
and the SFAP declining negative phase
In their study of the SFAP morphology, Dumitru’s group
directed special attention to the descending portion of the
SFAP negative phase [11]. The authors claimed that the
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majority of SFAPs, being essentially biphasic, had a steep
declining negative phase with an approximately constant
slope. However, they also reported the existence of some
SFAPs with a distinct shoulder-like feature (and therefore
an S-D point) in the terminal negative phase. The appear-
ance of this shoulder could hardly be attributed to distant
signals overlapping with the near-field SFAPs, as these
SFAPs were recorded in the absence of cannula potential.
Other authors before Dumitru did not comment on such a
feature in the SFAP time course, although in their studies
one can easily find examples of recorded SFAPs with an
apparent S-D point (Fig. 23 of [12], Fig. 4.1 of [36], and
Figs. 4.10 and 5.25 of [18]). In addition, the SFAPs sim-
ulated by Andreassen and Rosenfalck [4] taking as a ref-
erence experimental human IAPs also displayed a visible
S-D point. Thus, the presence of the S-D point does not
seem to be the result of low-frequency components from
distant fibers or from artefacts.
Our simulations have helped to elucidate the origin of
the S-D point in the SFAP. It was found that when the three
types of IAPs proposed in the paper were simulated to
produce narrow spikes (of DRT = 0.5 ms), they all give
rise to SFAPs with an approximately linear transition
between the second and third peaks (first column of Fig. 8).
When these same three IAP descriptions were adjusted so
as to synthesize wide spikes (of DRT = 1.0 ms), they all
result in SFAPs with a distinct S-D point in the descending
portion of the negative phase (second and third columns of
Fig. 8). Thus, it appears that the declining negative phase
of the SFAP is more dependent on the width of the cor-
responding IAP spike than on the specific outline of the
IAP falling phase.
The explanation for the above conclusion is as follows.
The character of the SFAP declining negative phase
depends on the temporal summation, and more specifically
on the degree of overlapping of the SFAP de- and repo-
larization components, which is determined by the tem-
poral separation between them. Then, IAPs with narrow
spikes (DRT = 0.5 ms), irrespective of their shape, lead to
SFAP de- and repolarization components separated by a
short time interval, which favors the highest overlapping
between them. As a result, the declining negative phase of
the corresponding SFAP has an approximately constant
slope. In the case of wide-spike IAPs (DRT = 1.0 ms),
however, the SFAP de- and repolarization components are
separated by a long time interval which prevents a com-
plete overlapping between them. As a result of this ‘‘par-
tial’’ overlapping, the declining negative phase of the
resulting SFAP exhibits an apparent S-D point.
The S-D point in the SFAP time course vanishes pro-
gressively with increasing radial distance. The reason for
this is that, at higher distances from the fiber, both the de-
and repolarization components of the SFAP become slower
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and with a more gradual decline toward the baseline, and
also they become more comparable in terms of amplitude
and duration. As a result, increasing the radial distance
brings about an increase in the degree of overlapping
between the de- and repolarization components, leading to
a gradual vanishing of possible discontinuities in the slope
of the SFAP declining negative phase. According to our
simulations, for radial distances [0.15 mm, the S-D point
should not be expected to appear clearly in the SFAP time
course.
4.3 Relationship between the IAP falling phase
and the variation of the SFAP waveform
with radial distance
Expressing the SFAP as a function of its de- and repolar-
ization components also improves the understanding of
why (and how) the variation of the SFAP shape with radial
distance depends on the characteristics of the IAP spike. In
the r-varying SFAP series generated using symmetric
short-spike IAPs (first column of Fig. 8), the three phases
of the SFAP undergo comparable amplitude variations.
Two reasons are needed to account for such behavior. First,
the de- and repolarization components arising from such
IAPs have rather similar declines with radial distance.
Second, these components, being of comparable magni-
tude, are separated by a short time interval which favors
their overlapping, thereby reducing the cancelation
between their corresponding phases.
On the contrary, in the r-varying SFAP series simulated
with strongly asymmetric long-spike IAPs, one can easily
appreciate that the first two peaks of the SFAP decline at a
much higher rate than the terminal phase (third column of
Fig. 8). The first reason for this behavior is that, for these
IAPs, the depolarization component has a much more abrupt
radial decline than the repolarization one because of their
different length [9]. In addition, for the different declines to
become apparent, it is necessary that the depolarization and
repolarization components are separated by a long time
interval, something that occurs in IAPs with long spikes.
4.4 Applicability and limitations of the results
4.4.1 Can the results of the present study be used to infer
characteristics of human IAPs?
The findings of the present study suggest that the DRT of
human IAPs cannot be as short as 0.5 ms. First, when using
the two physiologically realistic IAP models to synthesize
spike widths of *0.5 ms, the resulting SFAPs show a large
and well-defined third phase, a feature not commonly
found in real SFAPs. Even for the type-III IAP model, with
an overly gradual falling phase, the spikes with DRT of
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*0.5 ms have been shown to result in SFAPs with a vis-
ible third phase (Fig. 8g). Second, with a spike width of
*0.5 ms, our three IAP descriptions can only generate
SFAPs whose declining negative phase approximates to a
straight line (first column of Fig. 8). However, several lines
of evidence have demonstrated clear changes in the slope
(including S-D points) of the declining negative phase of
human SFAP. Third, values of DRT within the range
0.43–0.66 ms have only been measured under in vitro
conditions in rat IAPs [1, 3, 19, 39], whose characteristics
should not necessarily be identical to those of human IAPs.
Despite the above arguments, many authors [5, 14, 24],
following the modifications introduced in the IAP analyt-
ical expression by Nandedkar and Stålberg [26], have
preferred to use IAP models with a DRT of approximately
0.5 ms to simulate EMG signals.
The possibility that human IAPs have a DRT greater
than *0.75 ms appears to be more plausible. First, for the
three IAP descriptions considered here, a spike DRT
[0.75 ms has been shown to generate SFAPs with a
decidedly prolonged and small third phase which, under the
typical conditions of noise and baseline drift of SFEMG
[36], would be easily lost in the baseline. Thus, the
resulting SFAPs would appear as essentially biphasic, in
good accordance with the experimental data. Second, with
an IAP DRT greater than *0.75 ms, the corresponding
SFAPs would show apparent S-D points in the declining
negative phase, a characteristic recurrently observed in
human SFAPs. Third, the only data available on intracel-
lular potentials recorded from human muscle fibers comes
from the experiments performed by Ludin between 1969
and 1973 [21–23] involving the in vitro measurement of
IAPs from the human intercostal muscle. These IAPs had
DRT values of about 0.78 ms.
4.4.2 Limitations
The above speculations about the spike duration of real
IAPs are grounded on the hypothesis that the core-con-
ductor model (on which our SFAP model is based) is valid
to accurately describe the generation of extracellular
potentials. However, the core-conductor model is grounded
on two major simplifications: the excitation source is
assumed to be distributed along the axis of the fiber and the
influence of the extracellular potential field on the IAP
generation is neglected [20, 38]. Therefore, it is only by
assuming that these simplifications do not distort exces-
sively the true relationship between the IAP and SFAP that
the above hypothesis concerning the IAP spike width can
be regarded as valid. Future studies involving simultaneous
recording, from the same fiber, of the IAP, transmembrane
current, and SFAP are needed to establish the extent to
which the assumptions of the core-conductor model are
correct and to validate the above inferences above the
duration of human IAPs.
Summarizing, we tentatively suggest that IAPs recorded
in humans should have a DRT longer than about 0.75 ms.
The shape of the spike of these intracellular potentials
should be strongly asymmetric, provided that its rising
phase is about 0.3 ms.
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