Clinical Neurophysiology 131 (2020) 1354–1364

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Clinical Neurophysiology
journal homepage: www.elsevier.com/locate/clinph

Human cremaster muscle and cremasteric reflex: A comprehensive

review
Gulgun Sengul a,⇑, Cumhur Ertekin b
a
Department of Anatomy, Ege University, School of Medicine, Bornova, Izmir, Turkey
b _
Department of Neurology, Ege University Medical School Hospital, Bornova, Izmir, Turkey

a r t i c l e i n f o h i g h l i g h t s

Article history:
 Genitofemoral nerve motor conduction time and cremasteric reflex are useful for assessment of ingu-
Accepted 9 March 2020
Available online 31 March 2020
inal hernia complications.
 Transcranial magnetic stimulation elicits a descending motor response in the cremaster muscle (CM),

Keywords:
although its voluntary control is not essential.
Cremaster muscle  Sacrolumbar intersegmental reflex circuit and CM activity are useful for evaluating ejaculatory
Cremasteric reflex dysfunction.
Electrophysiology
EMG
Genitofemoral nerve a b s t r a c t
Objective: Human research on the cremaster muscle (CM), cremasteric reflex (CMR) and genitofemoral
nerve (GFN) and reports on their clinical applications using electrophysiological and histological tech-
niques are rare. We aimed to present a detailed review of the human CM and CMR based on our earlier
publications and relevant literature.
Methods: Electromyography (EMG) of the CM was recorded using disposable needle electrodes. CMR was
obtained with tactile and/or electrical stimulation of the inner thigh. Transcranial magnetic stimulation
(TMS) and magnetic stimulation of the upper lumbar roots were applied; GFN was stimulated using a sur-
face electrode at the anterior superior iliac spine.
Results: CM striated fibers comprised multiple motor end plates. CM needle EMG results were similar to
those of the limb muscles in chronic neurogenic disorders. TMS produced clear-cut evoked motor
responses from CM. GFN motor conduction time to CM was absent or delayed in patients with inguinal
hernia. EMG of CM was abnormal in 40% of patients with premature ejaculation.
Conclusion: CM is different from other skeletal muscles both morphologically and physiologically.
Intersegmental sacrolumbar reflexes are useful for evaluating ejaculatory dysfunction.
Significance: CM is an important muscle for testis thermoregulation and sexual reflexes.
Neurophysiological techniques are available for physiological and clinical studies.
Ó 2020 International Federation of Clinical Neurophysiology. Published by Elsevier B.V. All rights
reserved.

1. Introduction
Cremaster muscle (CM) is a striated muscle innervated with
spinal nerves from upper lumbar spinal cord segments. The electri-
cal activity of the CM has been shown on an anatomical basis
related to sexual reflexes especially for ejaculation in the rat
(Zempoalteca et al., 2002). Electromyography (EMG) of the pelvic
⇑ Corresponding author.
E-mail address: gulgun.sengul@ege.edu.tr (G. Sengul).
floor muscles innervated by the lower spinal cord segments has
been investigated during ejaculation in the human (Kollberg
et al., 1962; Petersén and Stener, 1970; Gerstenberg et al., 1990);
however, EMG of CM could not be recorded. Unfortunately, CM
and cremasteric reflex (CMR) cannot be used systematically in
evaluating male sexual function neurophysiology and dysfunction,
and its thermoregulatory function for testis protection could not be
well evaluated using CMR.
On the other hand, CM and CMR are being used in pediatric neu-
rology (Caesar and Kaplan, 1994; Bingöl-Koloğlu et al., 2001) in

https://doi.org/10.1016/j.clinph.2020.03.011
1388-2457/Ó 2020 International Federation of Clinical Neurophysiology. Published by Elsevier B.V. All rights reserved.
 G. Sengul, C. Ertekin / Clinical Neurophysiology 131 (2020) 1354–1364
various inguinoscrotal pathologies and urology clinics (Crawford
and Crop, 2014; Sheth et al., 2016) for the diagnosis of testicular
torsion. For these reasons, the neurologically and neurophysiolog-
ically neglected CM, CMR and GFN have been the focus of our
review.
2. Morphological features of CM
CM has been in the anatomical literature starting from Vesalius
(1543), Piolan (1658) and Winslow (1732); the last two used the
name of cremaster (Schwarz and Hirtler, 2017). CM consists of
loosely arranged fascicules surrounded with the cremasteric fascia,
a loose areolar tissue that forms a sac around the spermatic cord
and the testis. The cremasteric fascia is located deep to the external
spermatic fascia within the spermatic cord. It is not derived solely
from the internal oblique or the transversus abdominis muscles,
but from both (Schwarz and Hirtler, 2017). The lateral part of the
CM arises from the internal oblique muscle. The medial part arising
from the lower border of the transversus abdominis muscle and
the pubic tubercle is variable and may occasionally be absent
(Davies, 1972; Kayalioglu et al., 2008).
The CM has unusual features for a striated muscle. In humans,
anatomical, histochemical and immunohistochemical studies have
demonstrated that externally oriented CM fibers are composed of
striated and the middle and internal CM fibers of smooth muscle
fibers. Collagen fibers and blood vessels form a fibrous layer that
lies beneath the external CM fibers and surrounds the middle
CM. The parietal tunica vaginalis includes the internal CM fibers
on the inside (Tanji et al., 2000; Tanyel et al., 2000; Bingöl-Kolog
˘ lu et al., 2001; Kayalioglu et al., 2008). The CM has Type 1 fiber pre-
dominance (Tanyel et al., 2005; Kayalioglu et al., 2008; Aglianò
et al., 2015). There are also numerous hybrid fibers co-expressing
two or more myosin isoforms: the immature myosin and superfast
extraocular myosin (MyH13), which are absent in limb muscles,
and fibers co-expressing myosin heavy chain indicating this mus-
cle is unique both functionally and biochemically (Aglianò et al.,
2015).
There are two other significant morphological findings in stri-
ated and smooth muscle fibers of the CM that might also be signif-
icant from a physiological point of view: multiple motor end plates
that form a series of small dots or lines running alongside the stri-
ated muscle fibers; and several nerve endings that terminate on a
single muscle fiber (Fig. 1). Some other mammalian muscles
including the gracilis (Paul, 2001) and sartorius muscles (Paul,
2001; Harris et al., 2005) also have striated muscle fibers with
more than one end plate. We can consider the CM as a partly stri-
ated muscle without tendon junction.
The CM fibers run up from the distal to the proximal or vice
versa to end intrafascicularly. The multiple end plate bands at
serial intervals along a fascicle activate the sarcomers more syn-
chronously, and decrease the fiber distance when there is sudden
cold exposure. With this anatomical organization, the CM main-
tains the testis in a suspended position until the environment tem-
perature becomes ideal for the testes. Yamada (1961) observed
that smooth muscle fibers were more profuse than previously
acknowledged and also not arranged in layers, but widely scattered
between striated muscle fibers. We have demonstrated the nerve
plexuses, neurons and glial cells between the smooth muscle fibers
that provide autonomic innervation to the CM (Kayalioglu et al.,
2008). The conspicuous and heterogenous contribution of auto-
nomic innervation to the CM may be due to the possible transdif-
ferentiation of smooth muscle-like gubernaculum mesenchyma
into striated myotubes. This suggests that the CM myogenesis is
different from that of abdominal muscles (Tanyel et al., 2005;
Luria and Laufer, 2007; Niikura et al., 2008; Botti et al., 2015).
1355
3. CM motor unit action potentials (MUAPS) and cremaster
needle EMG
The EMG of the CM is rarely investigated, because it is not easy
to approach to the CM, its voluntary motor action is not probable,
and its activity is not controlled by descending motor pathways.
Therefore, it is necessary to investigate the MUAPs of the CM by
using peripheral tactile stimuli. The EMG activity of the CM is
recorded with disposable concentric needle electrodes. These nee-
dle electrodes are inserted into the inguinal canal after palpating
the intracanalicular structures. The detection of the MUAPs with
sharp configuration determines the precise location of the needle
electrodes (Ertekin et al., 2005; Özdemirkiran and Ertekin, 2011).
The most proper location for inserting the needle into the CM
was 1 cm above and 2–3 cm lateral to the midline of the penile
root. The depth of the needle varied from one to a few centimeters,
depending on subcutaneous adipose tissue thickness.
Technical details of CM stimulation were described by Ertekin
et al. (2005) and Özdemirkiran and Ertekin (2011) as: ‘‘These three
tests are performed to confirm the site of the needle tip after the
first needle insertion, and the needle tip is re-adjusted to achieve
the best position. Firstly, the CMR is elicited classically by drawing
on the inner part of the ipsilateral thigh with a blunt object. Sec-
ondly, the CMR is also induced electrically using a bipolar surface
electrode on the skin of the thigh. And finally, the GFN that inner-
vates the CM is stimulated on the anterior superior iliac spine
region.’’ (Fig. 2). The CM EMG response to the GFN will be dis-
cussed later in this review. When the needle electrode is inserted
into the CM, we first observe and/or hear the sound of two differ-
ent spontaneous activities. The first one is encountered frequently
in many needle manipulations. This is caused by continuous and
spontaneous discharges in a short time with regular high fre-
quency and small amplitude similar to fibrillation potentials, but
the voice is also similar to myotonic discharges (Fig. 3). This is like
the ‘deceleration bursts’ described for the external urethral sphinc-
ter (Fowler et al., 1985). The second kind of spontaneous activity is
caused by complex-repetitive discharges that are well known in
EMG terminology. These last longer than the so-called deceleration
discharges (Bademkiran et al., 2005; Ertekin et al., 2005).
MUAPs can be classified into two groups: simple MUAPs formed
in about 40% of CM fibers and the mean duration is about
4.7 ± 1.7 ms; the remaining percentages of potentials are polypha-
sic MUAPS with a mean duration of 10.1 ± 3.9 ms (Fig. 4). Mean jit-
ter values of potential pairs are 81.9 ± 56.8 ms (Fig. 5). Sometimes
intermittent blocking can be observed (Fig. 6). The MUAPs longer
than 20 ms are sometimes grouped as single long potential, or as
different subgroups with time intervals (Ertekin et al., 2005;
Özdemirkiran and Ertekin, 2011).
These EMG findings are similar to those acquired from patients
with chronic neurogenic disorders, although the CMs studied are
from clinically and functionally normal males. Therefore, these
data suggest that the CM is an embryonic striated muscle with
polineural innervation both at the muscle fiber and/or spinal cord
level in adult males. Thus, the CM has weak cortical control, but is
mostly excited by cutaneous tactile and thernal stimulation.
Isolated voluntary contraction of the CM is not obvious and
expected in daily life. However, transcranial magnetic stimulation
elicits a descending motor response in the CM (Ertekin et al., 2005).
4. Morphological features of the GFN
CM is innervated by the genital branch of the GFN originating
from L1 and L2 spinal nerves and consists mainly of sensory fibers
with a motor component to the CM. The GFN penetrates the psoas
muscle near the L3-L4 vertebrae and follows the medial border of
1356 G. Sengul, C. Ertekin / Clinical Neurophysiology 131 (2020) 1354–1364

Fig. 1. Histology of the cremaster muscle (CM). CM fibers stained with haematoxylene and eosin (A, B). Transverse sections of CM fibers stained with myosin slow (C, D) and
myosin fast (E, F) immunohistochemistry. Bielschowsky axonal staining showing multipl motor end-plates terminating on the CM (G). Anti-neurofilament immunohis-
tochemistry and Mayer’s haematoxylin double-staining showing axons terminating on the CM (H); (unpublished). CM: cremaster muscle.
 G. Sengul, C. Ertekin / Clinical Neurophysiology 131 (2020) 1354–1364
Fig. 2. Diagram showing the placement point of concentric electrode to the CM;
(from Özdemirkiran and Ertekin, 2011). CM: cremaster muscle.
Fig. 3. Spontaneous activity of the CM from a healthy individual. (A) After
transcranial magnetic stimulation (TMS). (B) Spontaneous activity of short duration
giving a sound similar to a dive bomber. (C) Complex repetitive discharges with a
long duration. Arrow indicates the onset of electrical stimulation; (from Ertekin
et al., 2005). CM: cremaster muscle.
the psoas muscle where it is still covered by the psoas fascia. The
mean distance from the midline to its emerging point through or
lateral to the psoas major muscle is 4.5 cm (Tubbs et al., 2005).
The GFN then perforates the fascia and splits into femoral and gen-
ital branches. The femoral branch approaches the common or
external iliac artery and passes through a vascular space named
lacuna vasorum to innervate the skin of the proximal part of the
femoral triangle or the subinguinal region. In some cases, the
GFN fuses with the lateral femoral cutaneous nerve (Feigl et al.,
2014). With a laterally directed course, the genital branch runs
retroperitoneally, follows the psoas muscle and passes through
1357
Fig. 4. Using the inner thigh tactile stimulation, two kinds of CM MUAPs were
obtained by delay-line technique: a simple potential with di- or triphasic shape (A)
or a ‘‘polyphasic” MUAP with several components (defined as five or more
deflections) (B). Five successive traces were recorded. Calibration marks: 8 ms
and 0.2 mV in (A), 8 ms and 50 lV in (B); (from Özdemirkiran and Ertekin, 2011).
CM: cremaster muscle; MUAP: motor unit action potential.
the internal inguinal ring in the spermatic cord to supply motor
fibers to the CM and sensory innervation to the scrotum
(Redman, 1996; Krähenbühl et al., 1997; Akita et al., 1999; Rab
et al., 2001; Rosenberger et al., 2000; Liu et al., 2002). The total dis-
tance from the emergence of the GFN from the spine to the ingu-
inal ligament was measured 353.1 ± 12.5 mm in adult human
male cadavers (Uysal et al., 2012). The genital branch gives up to
three sub-branches. All branches of the GFN are located medial
to the iliohypogastric and ilioinguinal nerves and ventral to the
psoas muscle. The genital branch runs retroperitoneally and enters
into the internal inguinal ring. The femoral branch accompanies
the external iliac artery and passes under the inguinal ligament
(Reinpold et al., 2015).
Sensory afferent fibers in the GFN originate exclusively from
neurons of the L1 and L2 dorsal root ganglia in small vertebrates
(Nagy and Senba, 1985). In humans, the receptive field of the
GFN is also the L1, L2 and L3 dermatomes. If there is a thoracolum-
bar or lumbosacral vertebral transition, a dermatomal gap is
observed that lies more ventrally than in adults with normal spinal
configuration (Seyfert, 1997). However, when the dermatomes are
examined with CMR, the actual dermatomal distribution may not
be of much significance as CMR can be evoked by larger der-
matomal segments (Ertekin et al., 2005).
5. Central nervous system innervation of the CM
Our knowledge on the neural connections of the CM in the
spinal cord is based on experimental animal studies. CM motor
neurons are richly innervated by a number of peptidergic neuron
terminals and serotonergic terminals (Nagy and Senba, 1985;
1358 G. Sengul, C. Ertekin / Clinical Neurophysiology 131 (2020) 1354–1364
Fig. 5. Examples of different individual recordings with concentric needle electrode
single-fiber EMG (CNE-SFEMG). Normal jitter and no blocking were obtained in
some recordings (A); increased jitter was found frequently (B); occasionally two
spikes with increasing jitter from the second to the third spike were also recorded
(C). Calibration marks: sweep speed is 1 ms in all and gain is 50 lV in A and B,
0.2 mV in C (from Özdemirkiran and Ertekin, 2011).
Kojima and Ohe, 1986; Kar et al., 1990; Botti et al., 2006;
Gajendiran, 2008). Serotonergic fibers concentrated on the CM
motor neurons are involved in involuntary contraction of the CM.
Increased serotonergic innervation of the CM motor neurons have
a capacity to induce sustained membrane depolarization without
excitatory synaptic input to these motor neurons (Koyanagi et al.,
Fig. 6. Motor unit action potential (MUAP) groups were strictly or loosely bound to each other. They were locked to each other with short intervals and less complex shapes.
There was intermittent blocking in between two groups. The second group was sometimes blocked. Calibration marks: 8 ms and 0.1 mV; (from Özdemirkiran and Ertekin,
2011).
2006). This might be another possible reason for the prolonged
CMR in normal human adults and group MUAP discharges in
EMG, and contribute to the prolonged CMR in normal human
adults and wide-receptive fields of the CMR further described in
this review. Sometimes the CMR can be prolonged more than
250 ms despite very short electrical stimulation much below the
pain threshold. This may be interpreted as the so-called plateau
potential of the spinal motor neurons (Hultborn et al., 1975;
Collins et al., 2002; Gorassini et al., 2002; Hornby et al., 2003;
Nickolls et al., 2004; Kiehn and Eken, 1997). However, this should
remain to be elucidated for CM neurophysiology. The GFN motor
nucleus is a sexually dimorphic structure, with motor neurons
located in L1-L2 spinal cord segments. Calcitonin gene-related pep-
tide (CGRP) is released from sensory nerve endings of the GFN and
controls inguinoscrotal descent by gubernacular proliferation, pro-
viding a chemotactic gradient towards the scrotum and rhythmic
CM contraction (Larkins and Hutson, 1991; Schwindt et al., 1999;
Hrabovszky et al., 2000; Lie and Hutson, 2011).
6. Peripheral nerve root and transcranial magnetic stimulation
The CM is a striated muscle, although its voluntary control is
usually not necessary. Current knowledge on the functional control
of the CM is mainly limited to the evaluation of the CMR. However,
CM can be elicited by transcranial magnetic stimulation (TMS) of
the motor cortex and stimulated from the back at the level of L1
and L2 motor roots giving off their contributing motor fibers to
the CM. Finally, motor latency from the GFN to the CM could also
be investigated (Ertekin et al., 2005). Motor evoked potentials in
the CM are constantly obtained by TMS of the motor cortex using
a circular coil, whereas this is hard to elicit using a butterfly coil.
Ertekin et al. (2005) observed that the cortical threshold to the
CM was similar to lower abdominal muscles; however, the MEP
mean latency values were longer. The average central motor con-
duction time with regard to the latency values obtained from stim-
ulation of the roots over the thoracolumbar spine was longer for
CM than those of abdominal muscles (16.5 ± 2.8 ms vs
14 ± 2 ms, p < 0,001). This indicates that although there is a CM
is representation in the motor cortex, voluntary contraction is
not obvious in daily life and may be activated with contraction of
abdominal and pelvic floor muscles.
 G. Sengul, C. Ertekin / Clinical Neurophysiology 131 (2020) 1354–1364 1359

The threshold, latency and amplitude values of MEPs of the CM et al., 2005). CM response is rarely recorded on both sides due to
indicate that its cortical representation may be considerably small the subtle location of CM insertion site, except in patients with uni-
and buried in the depths of the cortex. Another possibility is that it lateral lesions of the GFN (Bademkiran et al., 2005).
may be possible to stimulate the CM subcortically using a circular
magnetic coil (Ertekin et al., 2005).
7. Clinical implications of the motor conduction time
The CM responses to magnetic stimulation are usually obtained
at the L1-L3 vertebrae level. During magnetic stimulation of the
Motor conduction to the CM may have some clinical implica-
lumbar roots, the nerves can be excited distal to the root exit zone
tions; e.g. chronic groin pain may occur following interventions
(Ugawa et al., 1989; Ertekin et al., 1994a,b). Thus, the proximal part
to the lumbar part of the abdomen due to entrapment of the
of the GNF is stimulated in the back; however, the exact location of
GFN fibers (Akita et al., 1999). Thus, motor conduction time of
the stimulation is not well-defined. Motor conduction time to the
the GFN may be an important tool to elucidate GFN injuries.
CM obtained by stimulation of the GFN near to the anterior supe-
rior iliac spine was measured 5–8 ms (average value 4.9 ± 1.97) in
31 adult men (Fig. 7). The amplitude and shape of the CM response 8. The cremaster muscle reflex (CMR)
to stimulation of the GFN varied significantly among subjects. The
subcutaneus adipose tissue on the anterior superior iliac spine area CMR is neurologically a well-known superficial/skin reflex
was the most important factor for this variation. Also, the course of (Haerer, 1992), but neurologists often neglect to test CMR. This is
the branches of the GFN is also very variable in this region probably due to the general concept that its significance is minimal
(Rosenberger et al., 2000; Rab et al., 2001; Liu et al., 2002) and is neurologically. CMR was first described by Jastrowitz in 1875
probably another factor for the variation of the amplitude and (cited from Van Gijn, 1996) and demonstrated that the CMR disap-
shape of the CM response to stimulation of the GFN (Ertekin peared on the hemiparetic side (Van Gijn, 1977, 1996). Later, CM

Fig. 7. CM and ABD motor evoked potentials, after stimulation of the scalp (A) and L1 spine level (B) from a normal subject. Superimposed CM responses to genitofemoral
nerve stimulation near the anterior superior iliac spine from a normal subject (C); (from Ertekin et al., 2005). CM: cremaster muscle; ABD: lower abdominal muscles.
1360 G. Sengul, C. Ertekin / Clinical Neurophysiology 131 (2020) 1354–1364
reflex was re-described by de Monrad-Krohn and Kornfeldt in 1925
(Schwarz and Hirtler, 2017). The lack of fine motor control in CM
can be overbalanced with dense reflex activities, including ther-
moregulation of testes and facilitation of the coital or sexual
reflexes.
The role of the CMR in thermoregulation of testicular function
and spermatogenesis is very important because the testicular tem-
perature in man is maintained approximately 2–3°C lower than the
intraabdominal temperature (Vash et al., 2002; Skandhan and
Rajahariprasad, 2007). Thus, the CMR maintains the temperature
of the testes for the preservation of vitality for spermatogenesis
(Nagy and Senba, 1985; Kojima and Ohe, 1986; Redman, 1996).
For this purpose, the natural CMR is also one of the important
defending mechanisms against cold exposure in man (Waites,
1991). CMR retracts the testes, and deep scrotal tissue is very sen-
sitive to the even relatively mild stimulation (Nagy and Senba,
1985). So, the importance of thermoregulatory input from the scro-
tum may result with the clinical CMR (Pierau et al., 1975;
Kumazawa and Mizumura, 1980).
CMR in clinical use is an artificial reflex and is elicited by draw-
ing on the inner thigh using a blunt object. According to Seyfert
(1997), the receptive field of CMR in the dermatomes L1, L2 and
even L3 terminates abruptly at the S2 and S3 dermatome border.
Thus, the CMR cannot be elicited with adequate innocuous stimuli
from beyond that. However, CMR can be elicited by tactile stimu-
lation, larger than the dermatomal region from sacral to thoracic
spinal segments. Tactile stimulation to ipsilateral CMR is variable
from contact to contact on the inner side of thigh. It is tended to
habituate and the duration of CMR is grossly parallel to the dura-
tion of the moving tactile stimulation. It is obvious that the CMR
can be clearly investigated by using needle EMG examination.
The applications of EMG into CM have been mentioned previously
in this review. In fact, CM can be activated reflex or voluntarily
either with the abdominal muscles or alone; i.e. drawing on the
inner thigh skin elicits CMR alone without activation of the lower
abdominal muscles. The CM is also activated during abdominal
muscle voluntary contraction. The attempt to retract the CM vol-
untarily produces a definite, but smaller CM involvement.
Using EMG and stimulating the inner aspect of the thigh ipsilat-
erally, the minimal latency of CMR was measured 38.1 ± 15.8 rang-
ing between 22 to 85 ms, which is reasonable from L1-L3
dermatomes to the CM via the same roots. However, electrical
stimuli from the inner side of the thigh did not always produce a
simple CMR and in some cases, enhanced CMR appears with some
later components. These later components were not clearly distin-
guished and documented in the tactile and cold stimulation, but
tendency of consecutive EMG bursts could still be observed at
the later parts of the reflex (Bingöl-Koloğlu et al., 1999).
Cold stimulation on the inner side of the ipsilateral thigh elicits
very dense EMG responses sometimes with irregular bursts sepa-
rated from each other with short intervals. However, CMR obtained
by cold stimulation is also variable and even habituated, if the cold
stimulation is repeated with very short intervals. Cold stimulation
is unpleasant for some male subjects.
Electrical stimulation to the thigh can also produce contralat-
eral CMR, but the EMG responses are weaker and later in latency
compared to the ipsilateral side. Similarly, tactile stimulation with
a blunt subject may elicit contralateral CMR less frequently. This
may indicate the presence of some neural connections to the other
side in the segmental cord level (Ertekin et al., 2005).
At first sight, when we take into account the parameters of the
mean latency and prolongation of the duration of the ipsilateral
thigh CMR together with the bilateral stimulation of the reflex,
we may propose that CMR is a kind of withdrawal reflex like
reported in human lower limbs (Hugon, 1970; Ertekin et al.,
1975; Willer, 1977; Willer et al., 1978; Meinck et al., 1983). How-
ever, CMR is different by various aspects from such cutaneous
reflexes. First of all, CMR is obtained by ipsilateral thigh stimula-
tion much below the pain threshold using tactile and single electric
stimulation, though, the mean values in adult males (Sugiyama
et al., 1994; Bademkiran et al., 2005; Ertekin et al., 2007) and in
boys (Bingöl-Koloğlu et al., 1999) were found similar by electrical
stimuli for so-called RIII response of the biceps femoris muscle.
However, one of the important difference of CMR with low thresh-
old and prolongation in response duration could be found similar
both for nociceptive (i.e., cold stimulation) and non-nociceptive
(i.e., tactile/electric stimulation) stimuli. In withdrawal reflex
response in limbs, tactile and nociceptive components could be
easily differentiated from each other by stimulation threshold,
manipulation of electrical stimuli and response characteristics
(i.e., RII and RIII responses) (Pierrot-Deseilligny and Burke, 2005).
Furthermore, CMR could be elicited by stimulation from the plan-
tar surface (upper sacral dermatomes) to the chest wall (upper tho-
racic dermatomes), although it depended on the stimulation type
and varied between individuals. Such a wide reflex spreading can
only be observed for withdrawal reflex in spastic quadriplegia fol-
lowing spinal cord injury (Dimitrijević and Nathan, 1968; Pierrot-
Deseilligny and Burke, 2005).
The main findings of CMR are summarized as follows:
1. CMR was constantly obtained by the inner side of the ipsilateral
thigh excited by the tactile, electrical and cold stimuli.
2. The duration of the EMG response of CMR was prolonged and
even fragmented, mostly lasting more than 200 ms, in spite of
very short duration of single electrical stimulation, even below
the pain threshold.
3. Although it is variable from case to case, CMR could be some-
times elicited by the stimuli at a long distance from sacral to
thoracic dermatomes.
4. CMR could be more sensitive to the abdominal skin for cold
stimulation, while the genital skin by tactile and electrical stim-
uli could evoke higher incidence of CMR than cold stimulation.
9. Clinical applications of CM, CMR and GFN
Although the diagnostic value of CMR is considered minimal in
neurology, when the CM, CMR and GFN techniques are evaluated
altogether, it may be useful for diagnosing some neurological and
urological disorders. A number of disorders can be reviewed from
the following aspects:
The GFN may be compressed or injured during hernia repair
operations. This is mostly transient in nature and rarely causes per-
sistent symptomes (Cunningham et al., 1996; Krähenbühl et al.,
1997; Bauer et al., 1998; Akita et al., 1999; Liu et al., 2002). Motor
involvement of the GFN is common in patients after inguinal
herniorrhaphy, whereas 23% of patients not undergoing surgery
had involvement. Herniated mass may also lead to motor involve-
ment of the GFN in some patients before surgery (Bademkiran
et al., 2005). Similar results were reported in children with inguinal
hernia repair (Soyer et al., 2008). Subclinical motor involvement of
the GFN can be demonstrated electrophysiologically. One of the
most important electrophysiological finding is the absence or
delaying of latency of the GFN Fig. 8. CMR is either absent on the
operated side or the CMR response to the physical or electrical
stimulation on the operated side is weak in comparison to the nor-
mal side. Weak or absent ipsilateral CMR on the affected side may
result in a descended testis; in contrast, the contralateral intact CM
becomes more excitable and the testis ascends. This may be
explained by the bilateral organization of the motor neurons of
the CM (Zempoalteca et al., 2002)
 G. Sengul, C. Ertekin / Clinical Neurophysiology 131 (2020) 1354–1364 1361

Fig. 8. Genitofemoral nerve (GFN) motor conduction in patients with inguinal hernia (IH). (A) Absent M response of the CM on the operated side in a patient, 3 months after
herniorrhaphy. (B) GFN motor conduction was delayed on the operated side in this patient, 6 months after surgery. (C) Unoperated patient. The GFN motor conduction is
delayed on the IH side. Note the increased CMR latency (right lower trace); (from Bademkiran et al., 2005). CM: cremaster muscle; CMR: cremaster muscle reflex.

Testicular distortion is an acute urological disease. In a children
and adult patients, unilateral swelling, pain and absent unilateral
CMR on the pathological side are main clinical symptoms. Absent
CMR is also found 95% in testicular torsion (Boettcher et al.,
2012). However, although CMR is a useful test, it is useful together
with other signs of testicular torsion, and further investigations are
necessary (Nelson et al., 2003; Ringdahl and Teague, 2006;
Boettcher et al., 2012; Sharp et al., 2013; Boettcher et al., 2013;
Liang et al., 2013; Barbosa et al., 2013; Crawford and Crop, 2014;
Sheth et al., 2016). Although data on the CMR at birth is controver-
sial with a positive reflex reported between 2% to 92% (Caesar and
Kaplan; Bingöl-Koloğlu et al., 2001). Thus, the absence of CMR in
25–30% of otherwise healthy younger boys remains of obscure sig-
nificance (Bingöl-Koloğlu et al., 2001). Therefore, it is wise to
examine and compare both sides of the CMR especially in boys
before hormonal transfer in the adolescence when the spermatoge-
nesis begins. And the previous claims for the absence of CMR in
children with undescended testis should be evaluated as doubtful
signs.
It is very interesting that the abdominal reflexes and CMR
can still be elicited after brain death (Crüger and Hagenah,
1976). Although it is a debatable topic, the CMR is found as a
useful test to follow up spinal anesthesia during lower body
surgery in adult cases. Before spinal anesthesia, CMR should
be clinically present, and then, if the spinal anesthesia is effec-
tive and blocks the L1-L3 roots, CMR becomes absent bilaterally
(Okuda et al., 2001). These studies found the CMR very sensi-
tive and reliable.
1362 G. Sengul, C. Ertekin / Clinical Neurophysiology 131 (2020) 1354–1364

Lower sacral segmental stimulation (LSS) via the dorsal nerve of

penis elicits a reflex output named the bulbocavernosus muscle
reflex (BCR) from the bulbocavernosus muscle (BC), an oligosynap-
tic lower sacral spinal cord reflex (Ertekin and Reel, 1976).
The sensory input to the upper lumbar dermatomes and the
output of the CMR occur within the upper lumbar spinal cord seg-
ments (Ertekin et al., 2005). Thus, activity in the upper lumbar
spinal cord segments can be evaluated with CMR either clinically
or electrophysicologically (Bademkiran et al., 2005; Ertekin et al.,
2005). In normal adults and patients with mid-thoracic spinal cord
injury, the representative BCR is from the lower sacral segments
(LSS), therefore LSS stimulation evokes reflex responses of BCR
and CMR altogether, while the electrical stimulation of the upper
lumbar dermatomes (ULS) elicits alone a stable CMR, but not BCR
(Ertekin et al., 2007; Figs. 9 and 10). However, Courtois and
Charvier (2014) showed that the LSS did not elicit CMR, while
the BCR was obtained in patients with premature ejaculation and
concluded that the sacral sensory inputs reached the upper lumbar
spinal cord through a sacrolumbar pathway. The neurological
responses in BC and CM during stimulation of the sacral or lumbar
dermatomes provide evidence for a sacrolumbar intersegmental
reflex that may have an essential role in ejaculation. The interseg-
mental sacrolumbar reflex circuit may be functionally disturbed in
some patients with premature ejaculation. Although each input
arising from genital stimulation (or LSS) may ascend to the lumbar
spinal cord and to supraspinal levels, this may not produce
descending impulses to the sacral spinal cord at rest (Ertekin
et al., 2007; Fig. 11).

Fig. 10. In a patient with high thoracic spinal cord injury, the basic electrophys-
iological features did not differ from the normal control subjects. The electrical
stimulation of the upper lumbar dermatomes (ULS) showed stable reflex responses
from the CM, while there was no EMG response in the bulbocavernous (BC)
muscles. Lower sacral stimulation (LSS) evoked reflex responses from both muscles
(from Ertekin et al., 2007). BC: bulbocavernous muscle; CM: cremaster muscle;
EMG: electromyography.

Thus, CM is a distinctive striated muscle associated to nerves

Fig. 9. Schematic illustration of the intersegmental sacrolumbar reflex circuits with
some possible interactions into two segments. (+): excitation ( ): inhibition; (from
Ertekin et al.; 2007).
from lower sacral spinal cord segments. Experimental studies have
shown the anatomical basis of its activity in the sacrolumbar reflex
circuit is mainly related to sexual reflexes (Sachs and Garinello,
1979; Carro-Juárez and Rodríguez-Manzo, 2000; Lucio et al.,
2001; Zempoalteca et al., 2002).
Bademkiran et al. (2010) reported a male patient who experi-
enced continuous up and down movement of the right testis even
while sleeping. A concentric needle electrode was inserted into the
CM on the right side. When the right testis moved upwards, the CM
fired; however, there was no firing in the CM during downward
movement. Unilateral testicular movement was possibly con-
trolled by the lumbar root of the GFN, because the MEP following
root magnetic stimulation was slightly delayed on the affected
side. CMR was found bilaterally. Since these patients do not com-
plain of these testicular movements and experience them inciden-
tally, it is possible that more patients can be encountered in any
male population.
 G. Sengul, C. Ertekin / Clinical Neurophysiology 131 (2020) 1354–1364
Fig. 11. Patient with premature ejaculation. LSS did not elicit reflex response from
the CM while the BC reflex was obtained; (from Ertekin et al., 2007). LSS: lower
sacral stimulation; CM: cremaster muscle; BC: bulbocavernous muscle.
10. Conclusion
Preclinical studies of CM and GFN have been performed espe-
cially at the experimental level; studies in human are mainly on
pure clinical basis. Human research using electrophysiological
and histological techniques are also rare, even for patients with
1363
entrapment of GFN at the pelvic level, any kind neurologic disor-
ders involving CM and GFN, or premature ejaculation where exec-
utive organs are again CM and pelvic floor muscles. It has been
clearly shown that GFN motor conduction time is abnormal in
patients with inguinal hernia. A new way of research has been
offered for the topic of premature ejaculation which is a very
important and frequent problem in adult human males. Further
studies in this direction may open a new avenue and reveal novel
data on the CM and CMR.
Declaration of Competing Interest
None of the authors have potential conflicts of interest to be
disclosed.
Acknowledgements
The Scientific and Technological Research Council of Turkey
(TUBITAK); Grant number: SBAG 3119.
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