Electroencephalography and Clinical Neurophysiology, 1978, 4 4 : 3 1 7 - - 3 2 7

317

© Elsevier/North-Holland Scientific Publishers Ltd.

SPECTRAL ANALYSIS OF THE ELECTROMYOGRAM OF THE TEMPORAL MUSCLE IN THE RHESUS MONKEY (MACACA MULATTA)* A.J. MILLER

Center for Craniofacial Anomalies and Department of Physiology, University of California. San Francisco, Calif. 94143 (U.S.A.) (Accepted for publication: August 8, 1977)

Studies related to long-term variations in neuromuscular control frequently use electromyographic recordings (EMG) as the measurement (Lous et al. 1970; Estavillo et al. 1973; McNamara 1973). Statistical analysis of the EMG is hampered by the non-continuity in successive recording sessions due to factors which include: (1) placement of electrodes in the same relative position; (2) position of electrodes to the axis of the muscle fibers; (3) variations in the impedance of the electrodes selected for use (Buchthal et al. 1954; Kadefors et al. 1973) and the subject's response to the recording session. Spectral analysis has been applied to the EMG to determine the frequency components within the signal (Walton 1952; Gersten et al. 1965; Chaffin 1969; Kadefors and Peterson 1970). This analysis is based on the principle that the EMG is composed of simpler frequency components and that Fourier analysis can describe a periodically repeating wave shape of any degree of complexity as a summation of a specific series of sinusoidal waves (Goldman 1964). These frequency components are dependent upon the normal bi- and triphasic waveforms of action potentials (Cenkovich and Gersten 1963; Chaffin 1969), and are related to the mean duration of the waveforms in the signal (Kadefors et al. 1973). Spectral analysis has proven to be sensitive in determining alterations of the EMG in certain myopathic diseases in which many of the * This work was supported by USPHS grants from the National Institute of Dental Research (DE 02739, DE 02633).

action potentials become polyphasic accompanied by a reduction in the mean duration of the potentials and, often, with a decrease in their amplitude (Kugelberg 1949; Pinelli and Buchthal 1953). Spectral analysis of the interference pattern of these EMG's indicates that the dominant frequencies shift to higher bandwidths (i.e., 100--500 c/sec) in patients demonstrating these myopathic diseases (Walton 1952; Fex and Krakau 1957). In contrast, neuropathic diseases demonstrating longer durations of the average EMG waveform (Buchthal and Pinelli 1953) are associated with a shift of power in the spectrum to lower frequencies (Gersten et al. 1965). Almost all of the studies published to date have utilized the interference patterns of the EMG during a sustained contraction (Chaffin 1969) with little interest in the spectral analysis of spontaneous background activity in a muscle (Becket 1960). This statistical study using the spectral analysis is part of two projects studying longterm morphological and neuromuscular changes in the monkey adapting (1) to oral respiration with malocclusion and (2) after muscle detachment and determination of the effect on particular cranial sutures. A publication on certain morphological changes due to oral respiration is presently being prepared by Harvold and Tomer. Both projects include the anterior temporal muscle as one of the craniofacial muscles. The anterior temporal muscle is one of the major antigravity muscles of the mandible and usually demonstrates a background discharge of single motor units (Lund et al. 1970; McNamara 1974). The

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background discharge of this muscle's EMG was monitored during 4 experimental procedures. The first 2 o f these procedures chosen for statistical analysis induced short-term changes in muscle activity as ketamine does increase EMG activity of the temporal muscle (Kuroda and McNamara 1972) and the application of weights to the mandible increases bursts of discharges from precentral cortical cells anticipating jaw closing muscle activity (Kubota and Niki 1971). The last two procedures were selected for statistical analysis because of their proposed long-term changes in EMG activity. Chronic t e n o t o m y of the hindlimb musculature does decrease the phasic EMG levels of muscle spindles to stretch within 20 days after surgery (Yellin and Eldred 1970). Oral respiration has been demonstrated to consistently lower the mandibular posture and increase the vertical height dimensions (Harvold et al. 1973).

Methods

EMG recording sessions were relatively similar in both projects in which a total of 20 monkeys were used: 16 were from the malocclusion study and 4 from the suture study. The effect o f the drug, ketamine, on the temporalis EMG was studied at one dose in 12 animals: 8 control m o n k e y s in the malocclusion project and 4 m o n k e y s in the suture study. 6 of the control m o n k e y s in the malocclusion study and 2 from the suture study (prior to detachment of the temporal muscle} were used to assess the effects of weights on the mandible. All 4 monkeys in the suture study were used to determine the effects of unilateral detachment of the entire temporal muscle on the EMG activity of the anterior temporal muscle. The effects of inducing oral respiration on the temporal EMG were determined from comparing data of 8 control m o n k e y s to 8 established oral respiratory m o n k e y s in the malocclusion study. Each m o n k e y (7--14 kg, adolescent-young adult) was initially anesthetized with an

A.J. M I L L E R

intramuscular injection of ketamine--HC1 (8--10 mg/kg). Ketamine--HC1, which affects the ascending pathways associated with the motivational-effective aspects of pain, suppresses discharging of interneurons in lamina IV and V to noxious stimuli (Conseiller et al. 1972) and reduces evoked potentials recorded from the midbrain reticular formation and medial thalamic nuclei (Corssen and Domina 1966). Kuroda and McNamara (1972) indicate ketamine (25 mg/kg) produces some hyperactivity of the jaw-elevating muscles in the m o n k e y during the first 60--75 min after the initial dose. After the ketamine injection (10 mg/kg), the m o n k e y was removed immediately from his cage to a restraining chair. The pelvis, chest and shoulders were restrained while the head was positioned between t w o plexiglass plates which decreased lateral movements. The effects of ketamine were assessed by 5 min recording trials of the spontaneous EMG activity from the anterior temporal muscle at 30, 60 and 90 min after the first dose of ketamine; a n d at 5 min after the second dose given at the conclusion of the experiment. In those m o n k e y s in which 2 different weights were attached to the mandible, the 5 min trials with each weight (i.e., 150 and 300 g) were completed between 60 and 90 min after the ketamine. The weights were attached by a stainless steel wire (600 u m diameter) connected to an acrylic plate molded over the lower incisors and allowed to harden to a template. The EMG electrodes consisted of two platinum alloy needles, (1 cm long with a diameter of 500 p m ) placed 1 cm apart. These intramuscular electrodes consistently recorded single m o t o r units from the spontaneous activity of the temporal muscle. Contraction of the temporal muscle in mastication or in a rapid sudden elevation of the jaw was accompanied by a 3--10-fold increase in the EMG leading to an interference pattern. The two electrodes for the 0nterior temporalis were placed 1 cm rostral to the zygomatic arch, 2 cm posterior to the supraorbital ridge and parallel to the longitudinal axis of the muscle

SPECTRAL ANALYSIS OF TEMPORALIS EMG

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fibers. Five additional pairs of electrodes were placed in: the masseter muscle which is a second elevating muscle of the jaw; the suprahyoid region with muscles that lower the mandible; the upper lip region; the inferior orbicularis oris of the lower lip; and the lateral pterygoid muscle. These additional recordings combined with a continuous voice dialogue were used to monitor oro-motor responses and to determine movements of the mandible as related to the EMG activity of the temporal muscle. All EMG signals were differentially amplified (1 M~ input impedance) and filtered (3 dB level at 10--10 000 c/sec). In latter analysis to determine periods of little jaw movement, 4 recorded EMG channels were replayed at a slow speed on an oscillograph with the first channel containing the EMG of the anterior temporal muscle.

Each acceptable 5-min recording of the anterior temporal muscle was analyzed b y transmitting the original EMG signal to a spectral analyzer (Hewlett-Packard 3580) for: (1) an autospectral power estimate via a fast Fourier transform (Fig. 1) or (2) a plot of the amplitude of a given bandwidth over time (Fig. 2). In the first method, a 200 secanalysis length was chosen to provide a frequency resolution of 10 c/sec with a sampling rate of 20 sec/division and a lower and upper frequency range of 0--1 kc/sec (i.e., center frequency at 500 c/sec). The disadvantage of this first m e t h o d was that the signal source continually varied often providing t o o much fluctuation for frequency components to be a n ~ y z e d . Consequently, this m e t h o d was used as the first step in analysis and then replaced by a more thorough study with the second method. With the

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Fig. 2. E x a m p l e s o f v a r i a t i o n s in s e l e c t e d f r e q u e n c y b a n d w i d t h s ( A - - C ) o f t h e s p o n t a n e o u s l y active E M G ( D - - F ) f r o m t h e a n t e r i o r t e m p o r a l muscle. A--C: t h e p o w e r o f a given f r e q u e n c y is p l o t t e d o v e r t i m e w i t h a b a n d w i d t h c e n t e r f r e q u e n c y o f ± 1 c/sec. D: t h e original E M G r e c o r d i n g t a k e n over 100 sec f r o m w h i c h s e l e c t e d f r e q u e n c y b a n d w i d t h s o f 60, 2 0 0 a n d 4 0 0 c/sec were m o n i t o r e d . E - - F : selected s e g m e n t s of E M G activity r e c o r d e d while m o n k e y is relaxed w i t h n o o b v i o u s jaw m o v e m e n t . P o r t i o n s o f c e r t a i n r e c o r d s r e t o u c h e d for a c c u r a t e assessment.

second m e t h o d , a given frequency (i.e., 20, 40, 60 c/sec, etc.) with a 3 dB deviation of +1 c/sec was analyzed over a 100-sec period, and the amplitude of the response was measured at every fifth or tenth second to determine a mean and one standard deviation (S.D.) of the linear amplitude of that frequency bandwidth. The data of each 100-sec period was normalized b y setting the center frequency with the maximum amplitude at 100% and determining percentages of this maximum amplitude for all other frequencies. The normalized data was compared across all animals for a given paradigm.

alis (1.5 h after ketamine) indicated that this muscle demonstrated a consistent discharging of m o t o r units (Fig. I(D) and 2(D)) in the unanesthetized rhesus m o n k e y sitting upright. This background discharge could occur w i t h o u t obvious movements of the mandible and was evident in all recording sessions. Sessions in the recording chair included two initial sittings without placement of electrodes and subsequent recording sessions varying with the experimental paradigm as few as 6 sessions in 1 year to 14 in 3 months for agiven animal.

Effects of ketamine--HCl Results

Spontaneous activity EMG recordings from the anterior tempor-

Five-minute recording trials of the spontaneous activity of the temporal muscle occurring at approx. 5, 30, 60 and 90 min after a dose of ketamine--HC1 were subjected to

SPECTRAL ANALYSIS OF TEMPORALIS EMG

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80 60 40 20 o BAND CENTER FREQUENCIES (c/sec) Fig. 3. Spectral analysis of the temporalis EMG at 4 progressive periods following the administration of 8--10 mg]Kg of ketamine--HC1. Upper graph: Range of 4 time periods over a 2-h recording session from which the spontaneous EMG activity was sampled from the 12 animals. Lower graphs: Each graph is a mean and one S.D. of particular frequencies averaged during a given trial (i.e., 5-min post-ketamine period) across the 12 animals. Data normalized with center bandwidth frequency having greatest amplitude for each trial set at 100% on the ordinate, and amplitudes of remaining frequencies determined as fraction of the maximum response. Frequencies below 400 c/sec increased generally with significant increases in 20--40 c]sec (P < 0.02 Mann-Whitney U-test).

spectral analysis (Fig. 3). Data for each of the 4 trials were averaged across 12 animals. Within 5 min after administering the dissociative drug, the spectral analysis shifted the power distribution of the EMG signal (as compared to the distribution in the normal awake animal) enhancing the lower frequencies below 400 c/sec but particularly those at 20--40 c/sec (P < 0.02, Mann-Whitney U-test). By 60 min of the post-ketamine period, the power of the lowest frequencies had decreased accompanied by a decrease in the number of active motor units. This distribution of frequency components remained consistent through the final 90-min recording trial.

Effect of loading the mandible During the second hour of the recording session, weights were hung from the lower incisor template. Some of the monkeys responded with much tongue protrusion to remove the incisor plate and these recording trials were not used. In the majority of the trial sessions, the monkeys (N = 8) sat quietly

and passively lowered their jaw (1--1.5 cm with 150 g; 2--4 cm with 300 g) remaining quiet throughout the 5-min recording period. None of these jaw lowerings reached the maximum opening which the animals were capable of evoking. The 150 g weight decreased the amplitude of the frequency components but not significantly and did not alter the amplitude of the EMG (Fig. 4). In contrast, the 300 g weight decreased significantly the power in all the frequency bandwidths below 400 c/sec and decreased the range of the dominant frequencies from 20--100 c/sec to 20--80 c/sec (P < 0.02, Mann-Whitney U-test). This result accompanied a marked decrease in number of active motor units and total discharge of the units.

Effect of detachment Five-minute trials at 1.5 h after the administration of ketamine were selected from recording sessions before and after unilateral detachment of the temporal muscle in 4 of the monkeys. The frequency distributions

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were averaged over 4 control recording sessions from 4 animals (total N = 16) and this mean distribution com pared to the averaged distribution from recordings of all 4 animals for a given post-surgical day (N = 4). Spectral analysis (Fig. 5) suggested some shift in frequencies particularly those around 200--400 c/sec by days 6 and 10, but w i t h o u t statistically di fferent distributions from the control. By the 24th post-surgical day, the averaged f r e q u e n c y spectrum o f the postdet ached period was similar t o t h a t o f the predet ached c o n t r o l histogram and remained this way t h r o u g h o u t furt her tests {i.e., 46 days). This reduplication of the norm al spectrum later in the post-surgical period suggested some discrete shifts in the EMG signal t he first 20 days. However, of the 4 protocols, d e t a c h m e n t had the least effect, and visually, the EMG signal of the temporal muscle d e m o n s t r a t e d no obvious changes.

Effect on oral respiration Sixteen of the m o n k e y s were divided into 2 groups: 8 m o n k e y s served as c o n t r o l animals with normal nasal breathing; 8 more m onkeys received nose plugs and adapted over a 2-year period to oral respiration. The 8 oral respirat o r y m o n k e y s d e m o n s t r a t e d varied patterns of o r o - m o t o r adaptation to oral respiration but the majority (N = 7) consistently maintained their m out hs open with an 8--14-mm distance between upper and lower incisors. In contrast, the control m o n k e y s maintained their m o u t h s and lips closed unless demonstrating spontaneous oral movements. Five of the 8 experimental m o n k e y s d e m o n s t r a t e d r h y t h m i c jaw lowering during inspiration which raised an additional factor that could influence the level of background activity in the t em poral muscle serving as a jaw elevator. Five-minute recording trials occurred within 1.5 h after the initial dose of ketamine--HC1 were subjected to spectral analysis and the f r e q u e n c y distribution for all recording sessions o f all 8 cont rol animals (N = 32) were averaged and com pared to the mean distribution of all 8 experimental m o n k e y s (N = 32).

SPECTRAL ANALYSIS OF TEMPORALIS EMG POST-DETACHED PERIOD

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Fig. 5. The mean spectral distributions of selected frequency components in the EMG signal before (A) and after detachment (B, C and D) of the entire temporal muscle from its temporal fossa. Spectrum for control period averaged from 16 recordings while mean and one S.D. of the normalized amplitudes of the center bandwidth frequencies from trials in the post-surgical days are averaged from 4 recording sessions. Trials were recorded at 1.5 h after administration of ketamine to 4 monkeys.

Spectral analysis (Fig. 6) suggested a decrease in the power of the dominant frequency range (20--100 c/sec) in the experimental group except for the 20 c/sec bandwidth which

significantly increased its contribution to the signal (P < 0.02, Mann-Whitney U-test).

Discussion B. ORAL RESPIRATION

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Fig. 6. The mean spectral distributions of selected frequencies from the temporalis EMG are compared between those of (A) normal nasal breathing monkeys (N = 8) and (B) experimental monkeys which had adapted to oral respiration (N = 8). All trials were taken at 1.5 h after administering ketamine. Ordinate is normalized with the center bandwidth frequency having the largest amplitude set at 100%. Significant difference in amplitude of the 20 c/sec bandwidth

(P < 0.02).

Spectral analysis of the spontaneously active EMG of the anterior temporal muscle indicates changes in the frequency components of the signal under both short-term changes (ketamine over 2 h; weights for 5 min) and long-term changes (detachment over 3 months; mouth breathing through 2 years} used to modify that activity. Immediate effects of the dissociative drug, ketamine, on this antigravity muscle of the jaw, indicate that the EMG increases its lowest frequencies (i.e., 20--40 c/sec) and generally increases the contribution of the frequency components below 400 c/sec. This spectral shift occurs in association with the recruitment of more motor units particularly of larger amplitude and with an increase in discharge of the active motor units. The spectral analysis reflects the hyperactivity of the temporal muscle that results after the immediate administration of this dissociative drug. Applying increasing weights to the mandible and lowering the jaw beyond 1.5 cm (between

324 front incisors) significantly lowers the amplitude and frequency of spikes in the original EMG signal. This decrease in EMG activity is correlated with a substantial decrease in the power of all the frequency components and a suggestion of a decreased spread of the dominant frequency range (i,e., from 20--100 c/sec to 20--80 c/sec}. The loading of the jaw is hypothesized as an effective m e t h o d of lengthening the temporal muscle and increasing its tension. This effect should increase proprioceptive feedback from both stretch and suspected tension receptors (Cody et al. 1972; Kawamura and H a m o d a 1974), increasing the stiffness of the muscle (Houk et al. 1970; H o u k 1976). Stiffness is defined as the ratio of the change in force to change in length and is hypothesized as the effect (i} from the elastic properties of the muscle and (ii) from the interaction between the two proprioceptive feedbacks of length and tension on the m o t o n e u r o n o u t p u t to the muscle. In stretching the soleus muscle, the mechanical response based on the length-tension relationship of the muscle decreases its contribution to the total tension developed by the muscle while the reflexive compensation of the combined muscle spindle-Golgi tendon organ feedback contributes more to the muscle's total response and maintains this response. However, other potential factors to account for the decreased temporal muscle activity could include: (i) decreased development o f tension by the muscle in lieu of other jaw elevator muscles assuming the load {Garrett et al. 1964) and (ii) increased sensory input from the temporomandibular joint (Klineberg et al. 1970) and/or periodontal membrane supporting the template (Sumino 1971} with these inputs inhibiting the trigeminal motoneurons. In analyzing the long-term changes in spontaneous activity of the temporal muscle, detachment appears to subtly alter the frequency components of the EMG recorded from the detached muscle within the first 20 days after surgery. Visual observations of the EMG throughout the recording sessions

A.J. MILLER both in pre- and postdetachment periods suggest little change and of the four protocols subjected to spectral analysis, detachment of the temporalis appears to have had the least effect on the spectral components of the EMG signal. While detachment of the temporal muscle was unilateral and expected to effect peripheral feedback from the proprioceptors of the detached muscle, cortical involvement both in volitional contraction and in central modulation of peripheral feedback may have contributed to changes in m o t o r o u t p u t of the temporal muscle. Electrical stimulation of the lateral regions of the precentral cortex designated as the face region, elicits short latency reflexive responses both uni- and bilaterally in jaw musculature including the temporal muscle (Clark and Luschei 1974}. Electrical recordings from this precentral facial region indicate that some precentral cortical neurons discharge approx. 150 msec prior to closing movements of the jaw and before the onset of EMG in the jaw closing muscles (Kubota and Niki 1971). Cortical control can function unilaterally as in contraction of the ipsilateral temporal muscle with lateral excursion of the jaw to that side despite extensive bilateral representation of the jaw elevator muscles within the precentral cortex. The spectral analysis suggests that adaptation of the rhesus m o n k e y to oral respiration by lowering the mandible modifies the spontaneous EMG of the anterior temporal muscle which contributes to the resting posture of the jaw (Lund et al. 1970). The EMG of the anterior temporalis in some oral respiratory monkeys demonstrated bursts of discharges synchronously with respiration. Cenkovich and Gersten (1963) indicate that the frequency of a waveform should not modify the spectral analysis of the signal, only the changes in the duration of the action potentials. Kadefors et al. (1973) indicate that spectral analysis responds to the average potential duration of the active m o t o r units and depends on factors including: muscle fiber conduction

SPECTRAL ANALYSIS OF TEMPORALISEMG velocity, dispersion between the discharges of muscle fibers in one motor unit and/or variations in the recruitment of motor units with different durations. With such interpretations, the shifts in the spectral analysis may indicate variations in types of motor units which are responding, raising the question as to whether (1) recruitment of different single motor units (McPhedran et al. 1965; Olsen et al. 1968; Milner-Brown et al. 1973) and/or (2) recruitment of tonic versus phasic motor units (Tokizane and Shimazu 1964; Buchthal and Schmalbruch 1970) could partially explain the changes noted in this frequency analysis. Tokizane and Shimazu's summary (1964) suggests that both types of motor units, tonic and phasic, are active in isometric contractions, while Maton and Bouisset (1972) suggest that phasic motor units are preferentially discharged in isotonic contractions. Alteration in the type of motor unit recruited would be dependent on peripheral feedback as in lengthening or detaching the muscle, or in changes in both peripheral and central control of a muscle's activity as seen with the dissociative drug ketamine, or with the monkey trained to use a jaw elevator in modifying his upper respiratory passage. However, long-term changes in muscle use can alter the histochemistry of a muscle (Guth and Yellin 1971; Rindquist 1974) and alterations of muscle fiber properties could influence conduction velocities. Spectral analysis may suggest changes within the muscle without a specific modification in motoneuron control. These varied alternatives in interpretation reflect on the need to further define the relevance of spectral analysis to particular components of the EMG. At present, studies are progressing in this laboratory to analyze long-term changes in muscle activity using quantitative approaches of integration, frequency count and spectral analysis of the EMG.

Summary Spontaneous EMG activity of one mand-

325 ibular elevator and postural muscle, the anterior temporalis, was recorded from 20 unanesthetized rhesus monkeys subjected to 4 experimental protocols. The EMG activity was analyzed with a spectral analyzer to determine changes in particular frequency bandwidths after (1) administering a dissociative drug, (2)placing weights on the mandible, (3) detaching the muscle, and (4) adaptation of the muscle to oral respiration. The mean distribution of frequency components indicated that ketamine--HC1 increased the power of all frequencies below 400 c/sec, particularly those at 20--40 c/sec. A period of hyperactivity and increased recruitment and discharge of motor units occurred within the first 30 min following administration of the drug. Passive and sustained lowering of the jaw with increased weights indicated that increasing the front incisor distance 2--4 cm significantly decreased the frequency components below 400 c/sec accompanying a decrease in active motor units. Comparison of frequency components of the temporalis EMG before and within 40 days after detachment suggested some subtle variations in the mean distributions predominantly around 200 c/sec but without significant changes. Comparison of the mean spectral distribution between 8 nasal-breathing and 8 oral-breathing monkeys indicated a significant loss of power in the normal dominant frequency range of 20--100 c/sec in the oral respiratory group except for enhancement of the 20 c/sec bandwidth. The results suggest that the anterior temporalis alters its EMG activity during both short (i.e., min, h) and long-term (i.e., months, year) adaptations of the muscle. Rdsumd

Analyse spectrale de l'electromyogramme du muscle temporal chez le Rhesus (Macaca mulatta) L'activitd EMG spontande d'un

muscle

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~l~vateur et postural de la mandibule, le muscle temporal ant~rieur, a 6t~ enregistree chez 20 singes Rh6sus non anesth6si~s soumis a 4 protocoles exp6rimentaux. L'activit6 EMG a ~te 6tudi6e par analyse spectrale afin de d6terminer les modifications d'une bande particuliere de fr6quences apr6s: (1) administration d'une drogue dissociante, (2) 6tirement par suspension de poids fi la m~choire, (3) d6collement du muscle et (4) adaptation a la respiration orale. La distribution moyenne des composantes de fr~quence indique que la K~tamine augmente la puissance de toutes les fr~quences au

Spectral analysis of the electromyogram of the temporal muscle in the rhesus monkey (Macaca mulatta).

Electroencephalography and Clinical Neurophysiology, 1978, 4 4 : 3 1 7 - - 3 2 7 317 © Elsevier/North-Holland Scientific Publishers Ltd. SPECTRAL A...
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