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 Table of Contents  
ORIGINAL ARTICLE
Year : 2021  |  Volume : 38  |  Issue : 4  |  Page : 226-233

The effect of cold on the trigeminal reflexes


1 Department of Neurology, Kartal Dr. Lütfi Kırdar City Hospital, İstanbul, Turkey
2 Department of Neurology, İstanbul University Cerrahpaşa Faculty of Medicine, İstanbul, Turkey

Date of Submission13-Dec-2020
Date of Decision22-Mar-2021
Date of Acceptance26-Mar-2021
Date of Web Publication29-Dec-2021

Correspondence Address:
Rahsan Inan
Department of Neurology, Kartal Dr. Lütfi Kırdar City Hospital, İstanbul
Turkey
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/nsn.nsn_220_20

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  Abstract 


Objective: Effects of muscle cooling on the spinal stretch and monosynaptic reflexes have been studied to describe the properties of Group I and II afferents of muscle spindles. Masseter muscle differs from extremity muscles in structural and numerical features of the muscle spindles. The aim of this study was to examine the muscle spindle afferent features of masseter muscle by applying cold to understand the role of Group I and II afferents in reflexes of masseter. Patients and Methods: We included 12 healthy subjects (7 females and 5 males) in the study. Masseter inhibitory reflex (MIR), jaw tendon reflex (JTR), trigeminal motor evoked potential (MEP), and trigeminal somatosensory evoked potential (SEP) were studied before and after cold application. Left masseter muscle was cooled down to 18°C. We compared the data obtained before and after cold application. Results: After cold application, the mean total duration of MIR was shortened and it was absent in four subjects. The mean amplitude of JTR was higher after cold application (P = 0.018) without any significant change in latency. The mean latency of MEP was delayed without any change in amplitude (P = 0.003). There was no significant difference in SEPs. Conclusions: Changes observed in MIR, JTR, and MEP could not be ascribed to any specific type of muscle spindle afferents. Delayed mean reflex latencies were attributed to the effect of cold on nerve conduction. Summation of peripheral cold and pain receptor features, spindle afferents, and cortical mechanisms might have caused cold-associated changes.

Keywords: Cold application, jaw tendon reflex, masseter inhibitory reflex, masseter muscle, muscle spindle, trigeminal motor evoked potential, trigeminal somatosensory evoked potential


How to cite this article:
Inan R, Erdemir-Kızıltan M. The effect of cold on the trigeminal reflexes. Neurol Sci Neurophysiol 2021;38:226-33

How to cite this URL:
Inan R, Erdemir-Kızıltan M. The effect of cold on the trigeminal reflexes. Neurol Sci Neurophysiol [serial online] 2021 [cited 2022 Aug 19];38:226-33. Available from: http://www.nsnjournal.org/text.asp?2021/38/4/226/334053




  Introduction Top


Cooling a muscle leads to the generation of action potentials similar to those when the muscle was stretched.[1] The same authors concluded that the afferents in cold modulation were from muscle spindles, since a stretch interrupted the firing due to cold. The muscle spindle and tendon organ themselves supposedly have a temperature sensitivity; however, not all muscle spindles in the cooled muscle preparation became active in this study and they revealed that cold response was directly related to fiber diameter and conduction velocity.[1]

In another study performing single unit recordings from afferents of muscle spindles and tendon organs during slow and fast temperature changes, cold was shown to depress the activity of Group I afferent units, whereas it increased the activity of Group II afferents. Therefore, in a cold environment, the Group I afferent units of a moderately prestretched muscle would reduce their discharge. Group II spindle afferents were not active under resting conditions. They activated by cooling, and then, they became silent on rewarming. However, there were Group II afferents behaving similar to Ia afferents, i.e., depressed by cooling and activated by warming, thus possessing a response behavior.[2] Similar results were also found by Michalski and Séguin.[3]

Thus, it is possible to distinguish Group I and II afferents through cold response. Some studies investigated the role of Group I and II afferents in several reflex responses using cold response. For example, Matthews used the extremity cooling method to show that long latency reflexes recorded from intrinsic hand muscles were not only through cutaneous afferents, but they also suggested that the fast-conducting Group Ia muscle spindle afferents also contributed to these responses.[4] Following studies have employed the technique of cooling the muscle to identify the role of the Group I and II afferents in the stretch responses of hand and arm muscles.[5],[6] Other studies examining the effects of cold on H reflex and tendon reflex revealed that simple local cooling facilitates the excitatory alpha motoneuron pool and suppression of muscle spindle activity, by Group II afferents.[7],[8],[9],[10] There are also studies conducted in humans to modulate the functions of muscle spindles by cooling as a therapeutic option.[10],[11],[12]

It is known that the jaw-closing muscles, particularly the masseter muscle, differ from extremity muscles in distribution, number, and morphology of muscle spindles. The adult human masseter muscle contains large and complexly arranged muscle spindles.[13] The largest and most complex spindles are located in the deep masseter, which is composed mainly of type I afferents.[14] However, the number of synapses between a single spindle Ia afferent and an α-motor neuron innervating masseter muscles is much smaller than those for limb muscles.[15],[16] This complex morphology of masseter spindles compared to extremity muscle spindles indicates a more advanced proprioceptive control of the masseter muscle.[13] Therefore, it would be interesting to understand the role of Group I and II afferents in reflexes of masseter. Here, we used cold application to analyze the contribution of muscle afferents in the inhibitory and excitatory reflex responses of masseter muscle, i.e., masseter inhibitory reflex (MIR) and jaw tendon reflex (JTR), respectively, in healthy individuals. We also recorded motor evoked potentials (MEPs) and somatosensory evoked potentials (SEPs) to exclude the changes related to cold application on nerve trunk.


  Patients and Methods Top


Patients

We included 12 healthy volunteers (7 women, 58%) in the study. The ages were between 25 and 44 years, and the mean age was 34.4 ± 5.5 years. Subjects with epilepsy, headache, craniofacial pain, cardiac pacemaker, previous cerebrovascular disease, jaw joint disorders, and bruxism were excluded from the study. None of the healthy subjects used any medications that would alter neuromuscular excitability or lower the pain threshold within 48 h before examination.

The study was approved by the local ethical committee in accordance with the Declaration of Helsinki (April 05, 2011-12818), and a written informed consent was obtained from each participant.

Methods

All electrophysiological examinations were conducted while the subjects were seated, in a dim and quiet environment, and using a four-channel Nihon Kohden electromyography (EMG) device (Neuropack RMEB-5504 K, Nihon Kohden, Tokyo, Japan).

The following electrophysiological tests were performed before and after cooling. Cold application was performed on the left masseter muscle, which was cooled down to 18°C by an ice cube placed in the mouth mucosa and an ice pack applied externally on the skin. Cooling was continued for an hour until all examinations were completed. The temperature was kept steady by monitoring with a digital skin thermometer (Derma Temp DT-1001). We applied cooling each time when we investigated a different reflex. We randomized the order of recordings, and we waited for at least 10 min between different reflex recordings to let the masseter muscle re-warm.

Masseter inhibitory reflex

The Ag/AgCl surface electrodes were placed on the right and left masseter muscles; the active electrode was placed at the center of the masseter muscle, while the reference electrode was placed below the angle of the mandible. We placed the ground electrode on forehead. The subjects were asked to adjust the EMG activity of both masseter muscles to around 90% of maximum strength by clenching the teeth, controlled by visual and acoustic feedback. Left mentalis nerve at the mental foramen was stimulated using a single electrical stimulation (20–30 mA in intensity and 0.2 ms in duration). The low-high-frequency filters were 5 Hz to 20 kHz. The analysis time was 20 ms/div. The sensitivity was 200–500 μV. The examination was repeated five times at 10–30 s intervals, and the responses were averaged and rectified. After cold application on the left masseter muscle, we repeated the MIR recording over the left masseter muscle after left mentalis nerve stimulation.

Jaw tendon reflex

The recordings were performed using surface electrodes placed on the masseter muscles bilaterally by means of the muscle belly-tendon technique (similar to that in the MIR recordings). We placed the ground electrode on the forehead. The JTR response was obtained by tapping an electronic reflex hammer to chin connected to the EMG device during mandibular rest. Band-pass filters were 20 Hz to 5 kHz, the analysis time was 10–20 ms/div. The sensitivity was 200 μV to 1 mV. We recorded five responses, rectified, and averaged. After cold application on the left masseter muscle, we repeated the JTR recording over left masseter muscle.

Trigeminal somatosensory evoked potential

The recording electrodes were placed 2 cm behind the C5–C6 electrodes corresponding to the trigeminal sensory field in the 10–20 electrode system, while the reference electrode was placed in the Fpz electrode position. We placed the ground electrode over the chin. We stimulated mentalis nerve with an electrical stimulus of 0.2 ms in duration and 3 times the sensory threshold in intensity. The responses were recorded over the scalp after stimulation of contralateral mentalis nerve. We recorded each side subsequently. The band filters were 0–3000 Hz, the analysis time was 10–20 ms/div, and the sensitivity was 10 μV/div. The recordings were averaged 200 times and repeated twice. Cold application was performed on the left masseter muscle, and we repeated the SEP recording after left mentalis nerve stimulation in the postcooling period.

Trigeminal motor evoked potential

The stimulations were delivered using a Magstim 2002-model (Magstim Company Limited, Britain) monophasic transcranial magnetic stimulation (TMS) device. The surface electrodes were placed on bilateral masseter muscles similar to those in the MIR recordings. The single pulse TMS was delivered through a standard 90 mm round coil, at the 6–7 cm lateral and the 2–4 cm anterior of the CZ electrode corresponding to the contralateral trigeminal motor field on the 10–20 electrode system over the vertex. The coil was placed on the parasagittal plain at a 45° angle, the hand-held portion of the coil facing the rear. The signal was filtered using the 1–1000 Hz range, the sensitivity was set to 1 Mv/div, and the duration of the analysis was to 10–20 ms/div.

The resting motor threshold (RMT) was determined as the lowest intensity capable of inducing five out of ten MEPs of at least 50 μV peak-to-peak amplitude.[17] Following the RMT determination procedure, five single pulses at 120% of RMT were delivered at random intervals during a slight contraction of the masseter muscle (30% of the maximum contraction). After that, we recorded MEP responses using stimulations at an intensity of 60%–70%, and we calculated the average value.

Cold application was performed on the left masseter muscle, and we repeated the MEP recordings on the left masseter muscle in the postcooling period.

Statistical analysis

  • For MIR, the onset latency and duration of the early and the late exteroceptive suppressions (ES1 and ES2) were measured using cursors. Total suppression duration (ES1 + ES2) and suppression ratio as percentage (calculated as the percentage of the average rectified EMG amplitude divided by the average rectified baseline amplitude) were calculated
  • For JTR, the onset latency and peak-to-peak amplitude of JTR response were measured using cursors
  • For trigeminal SEPs, the latencies of N1, P1, N2, P2, and the amplitude of N1–P1 were measured
  • For MEPs, the latency and amplitude of MEP responses were measured.


The data were analyzed using the SPSS for Windows 11.5 package software (SPSS Inc., Chicago, Illinois, USA). The complementary statistics were shown as average, standard deviation, median, and minimum and maximum for continuous variables, as well as number of cases and percentage for categorical variables. Whether the distribution of continuous variables was close to normal was investigated by Shapiro–Wilk test. The existence of a statistically significant difference in the clinical measurement before and after cooling was evaluated using the Wilcoxon signed test.

The results were considered statistically significant for P < 0.05. However, the Bonferroni correction was done to control the Type I error in all possible multiple comparisons.


  Results Top


All of the volunteers who participated in the study completed the study without any complaints of pain. Several subjects defined the electrical and magnetic stimulations as an “unpleasant feeling.” The visual analog scale (VAS) values were identified as 5.5 ± 0.9.

Masseter inhibitory reflex

In all healthy subjects, bilateral ES1 and ES2 responses were elicited after left mental nerve stimulation before cold application. There was no side-to-side asymmetry.

In group analysis, there were no differences in the latencies of ES1 or ES2 as well as suppression index after cold application compared to before cold application [Table 1]. Total duration of MIR was shorter after cold application compared to before cold application condition (P = 0.028). In individual basis, no ES1 and ES2 responses were present in one subject, while ES2 response was absent in three subjects [Figure 1].
Figure 1: (a) Pre-cooling right masseter (top line) and left masseter (bottom line) ES1 and ES2 periods. (b) ES2 is absent on cooled left masseter muscle (arrow)

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Table 1: Measurements of masseter inhibitory reflex parameters elicited by cooled left masseter

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Jaw tendon reflex

It was consistently bilateral in all subjects. There were no significant differences for latency, occurrence, and amplitude between right and left sides [Table 2].
Table 2: Measurements of jaw reflex parameters before and after cooling

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In group analysis, the mean amplitude of JTR was higher after cold application (P = 0.018). There was no significant change in latencies.

On individual basis, JTR was absent after cold application in one subject.

Trigeminal motor evoked potential

We obtained MEP responses in all healthy subjects. Following cold application, the latency of MEP response was delayed (P = 0.003). There was no statistically significant increase in MEP amplitude [Table 3].
Table 3: Pre- and post-cooling measurements of transranial magnetic stimulation components

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Trigeminal somatosensory evoked potential

There was no statistically significant change in N1, P1, and P2 latencies or in the N1–P1 amplitude after cold application. The latency of N2 was slightly delayed (P = 0.05) [Table 4].
Table 4: Pre- and post-cooling trigeminal somatosensory evoked potential measurements

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  Discussion Top


The major findings in this study were delayed latencies in evoked potential studies, shortening of total ES period, and loss of MIR response in some patients and increased amplitude in JTR after cold application.

Studies investigating the feedback properties and neuronal connections of masseter afferents showed that sensory inputs from periodontal mechanoreceptors and spindles play a crucial role in controlling isometric contraction of masseter muscles.[18],[19],[20] Applying ice intraorally and over masseter skin might have changed the activity of periodontal mechanoreceptors and spindle endings in a way that mechanical stimulation elicited an illusion as if the muscle was stretched as suggested in previous studies.[21],[22] The authors considered that spindle primary endings were responsible for such illusion, based on the difference in sensitivity to vibration among spindle primary and secondary endings and Golgi tendon organs.[23],[24] However, in the present study, it is hard to suggest that spindle primary and secondary endings are primarily responsible for MIR changes upon cold application.

There may be different hypotheses for the shortness of total ES duration and loss of MIR responses after cold application in the present study. Since ES2 is of a polysynaptic structure and its connections are wide and more sensitive to modulation, ES2 may play a more important role in MIR changes.[25] Applying ice intraorally and on the masseter muscle might have activated the nonnociceptive Aβ along with the nociceptive Aδ and C afferents of periodontal cutaneous and mucosal receptors. Although the healthy subjects participating in the study did not complain of severe pain (VAS: 5.5 ± 0.9), the cold we applied was below 20°C, at which the cold nociceptors are activated and we consider it to have been sensed as a painful stimulus.[26] Some authors suggested that occurrence of ESs was not related to the severity of the sensed pain.[27],[28] Although nociceptive character of MIR afferents is controversial, we believe that the nociceptive afferents are responsible for the absence of ES2 responses since there was no distinct change in the ES1 responses and that there are a greater amount of data in the literature, indicating that ES2 is mostly transmitted over nociceptive fibres. Moreover, since unmyelinated C fibers sensitive to cold stimulus above 0°C are mostly placed along vessel walls, we may suggest that, also with the effect of the cooling of the intraoral mucosa, the afferent fibers of the ES2 cycle predominantly consist of nociceptive C fibers.[29],[30] In the present study, ESs could not be obtained in four subjects following cooling. Based on the studies related to pain, it may be possible to attribute the changes to mechanisms relating to pain rather than to spindle afferents.

Exteroceptive suppression of the masseter muscle activity following electrical stimulation has been used as a method to assess the different trigeminal somatosensory pathways.[27] Of the elicited responses, ES1 is assumed to be a pontine di- or oligosynaptic. ES2 is considered a pontomedullary polysynaptic reflex.[31],[32] Nociceptors, with Aδ afferent fibers, are involved in the reflex complex largely. However, since electrical stimulus is not selective, mechanoreceptors with Aβ afferents may become activated which can mediate a similar reflex complex.[31] Romaniello et al. showed that durations of ES1 and ES2 were shortened when the perioral region was stimulated simultaneously by nociceptive and nonnociceptive stimulations.[33] They reported that the sum of stimulations resulted in a modulation on the excitability of the ES1 and ES2 cycles in the wide dynamic range neurons found in the trigeminal nucleus complex.

Tendon reflex studies recorded on the extremities showed that following cold application, the reflex latencies were delayed and the amplitudes were decreased due to prolongation of refractory period, slowing of current velocity, and the suppressive effect of cold on muscle spindle activity.[7],[8],[34],[35] In the present study, after cold application, the latency of JTR remained unchanged, but a distinct increase in the amplitude was observed. However, since the amplitudes were variable interindividually and the standard deviations were too wide, this finding was somewhat difficult to interpret significant. There may be more than one explanation for this result. The largest and most complex spindles are located in the deep masseter; we may not be able to stimulate these spindles adequately with superficial recording.[14] A limited distribution of the muscle spindle input to masseter motoneurons, which was demonstrated in animal studies[15],[16] and human H reflex studies,[36] could be another reason. In extremity stretch reflex studies, it was shown that the “cold response” was prominent in secondary endings (Group II fibers), while this response did not occur in primary endings (Group I fibers).[4],[5] Since JTR is a monosynaptic reflex transmitted over Ia fibers, considering the cold response, spindle-type differentiation may not be possible through this reflex. Further, we may suggest that the increase in the afferent activity of muscle spindles through nociceptive receptors as a result of cold application is a probable other mechanism for the JTR amplitude increase since it has been demonstrated in the study of Wang et al. that the activation of the nociceptive afferents caused a change in presynaptic modulation in the Ia afferent fibers projected to the motor neuron pool.[25] Even so, we could not attribute the changes in the amplitude only to the cold effect. As a conclusion, it may suggest that since the number and structure of masseter muscle spindles differ from those in the extremity muscles, the organization of the stretch reflexes in the trigeminal motor system is different from the monosynaptic reflexes observed in the extremities.

The TMS has been used to examine the neurophysiological basis of thermal stimulation on corticomotor excitability.[37] As a result of extensive neural activation, at the subcortical, cortical, and secondary (somatosensory) areas, variable responses in MEP responses, either enhanced or suppressed, were observed.[37],[38] It was proposed that cold-induced variations in corticomotor excitability could be related to individual differences in the way thermal afferents are processed centrally through sensorimotor integration.[37] In the present study, a significant delay in MEP latency was present, but no significant change in amplitude was observed. Delayed MEP latency would be compatible with a depressed excitability at the cortical level since prolonged latency could reflect a reduced excitatory drive to corticobulbar neurons, but also a temperature-dependent decrease in the peripheral nerve conduction is also possible to account for the prolonged MEP latency. It has been reported that variations in MEP amplitude were largely independent of individual changes in skin temperature, confirming that the degree of skin cooling is not a critical factor in determining the sign of modulation.[37] Therefore, alternative explanations, for example, altered sensory feedback from cold and pain receptors, might be sufficient to explain this finding. An interpretation as cold causes change in cortical excitability or muscle spindle activity is controversial. It is not possible to say that a single mechanism is responsible for this situation. We may attribute MEP findings to spatial summation of corticobulbar and spindle afferent inputs to masseter.

We observed no significant change in trigeminal SEP responses, except an insignificant prolonged N2 latency, which can be explained by the effect of cold application on nerve conduction. Since cold evoked potentials assess the integrity of spinothalamic tract, standard SEP techniques evaluating only dorsal column-lemniscal system failed to demonstrate the processing of cold sensation.

Among the limitations of the study were the ability to cool only a very short section of the nerve due to its anatomic characteristic, less stimulation repeats after cold application than before due to the limited cold tolerance of the subjects, and technical difficulty in keeping the temperature constant due to melting of ice. Since it was difficult to prevent the opposite masseter muscle from cooling intraorally, responses were recorded unilaterally. Since a layer of other facial muscles covers masseter muscle, it is not possible to claim that EMG activity recorded using surface electrodes comes just from masseter muscle itself.


  Conclusions Top


The findings in the present study are inadequate to demonstrate which spindle afferents are selectively affected by cooling, and it is not possible to attribute the findings to a direct effect of cold or to a modulation in pain pathways. The muscle-specific features and differences in the reflex and descending control of trigeminal motoneurons might have caused the changes observed. The summation of multiple factors such as the changes due to activation of muscle spindle afferents by cold, different structure of the masseter muscle from extremity muscles, the activation of on the Aδ and C fibers-mediated nociceptive inhibitory control neurons by cold, and excitability changes occurring at cortical level may play a role. Further studies using other modalities such as vibration, ischemia, exercise, and selective Group II afferent inhibitors in addition to the application of cold are needed to identify the role of specific muscle afferents.

Financial support sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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