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1 Sobell Department of Motor Neuroscience and Movement Disorders, Institute of Neurology, London WC1 3BG, United Kingdom; 2 Neurologische Klinik und Poliklinik, Charité, Campus Virchow-Klinikum, 13353 Berlin, Germany
Submitted 10 February 2003; accepted in final form 8 May 2003
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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14 Hz in deltoid and biceps muscles only during the startle reflex. Similarly, coherence spectra of the EMG recorded between homologous proximal upper limb muscles demonstrated a peak centered 12–16 Hz during reflex startles. Coherence in the 10- to 20-Hz band was significantly greater in the startle reflex than during voluntary sham startles or voluntary tonic contraction for deltoid, but not first dorsal interosseous, muscles. The coherence at 10–20 Hz between EMGs from homologous muscles represents a potential surrogate measure of reticulospinal activity that may be useful in determining the contribution of the reticulospinal system to different types of movement in health and disease. |
INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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; Brown et al. 1998, 1999; Conway et al. 1995; Farmer et al. 1993; Gross et al. 2000; Grosse et al. 2003; Halliday et al. 1998; Kilner et al. 1999; Marsden et al. 2001b; Mima et al. 1998; Salenius et al. 1997). In contrast, knowledge of reticulospinal function has been limited by the inaccessibility of this system, both in terms of recording and stimulating and by the absence of a known surrogate measure in EMG, with the exception of the drive to motor units at >60 Hz during breathing (Carr et al. 1994; Kirkwood et al. 1982). Here, we use the acoustic startle response (ASR) to demonstrate that some forms of reticulospinal activity in the human are associated with a characteristic pattern of bilaterally synchronous oscillations with a frequency of 10–20 Hz between motor units.
As in other animals, there are several lines of evidence that the ASR in humans is relayed in the reticular formation of the lower brain stem and uses reticulospinal efferents (Davis et al. 1982; Hammond 1973; Koch 1999; Koch and Schnitzler 1997; Leitner et al. 1980; Lingenhöhl and Friauf 1992; Koch et al. 1992; Yeomans and Frankland 1996; Yeomans et al. 2002). First the startle reflex exists in anencephalic infants (Edinger and Fisher 1913). Second, the caudorostral pattern of recruitment of cranial nerve innervated muscles suggests a generator in the caudal brain stem in the startle reflex (Brown et al. 1991a; Matsumoto et al. 1992; Valldeoriola et al. 1997). Third, symptomatic cases of exaggerated startle involve brain stem pathology and sometimes responses at a latency only compatible with a brain stem relay (Brown et al. 1991b; Matsumoto et al. 1992). Finally, the startle reflex is diminished in the Steele-Richardson-Olszewski syndrome in which there are widespread pathological changes in the brain stem including degeneration of the pontine reticular formation with severe neuronal loss (Vidailhet et al. 1992).
We recorded EMG activity in proximal and distal upper extremity muscles during the physiological startle reflex to define any common drive to motoneurons from the reticulospinal system in the human. Given that the reticulospinal system projects bilaterally and preferentially innervates motoneurons of proximal muscles (Kuypers 1981), we predicted that a reticulospinal drive would be evident as significant EMG-EMG coherence between homologous proximal muscle pairs, with less coupling between hand muscles on the two sides of the body.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Healthy subjects gave their informed consent to the study, which was approved by the by the Joint Research Ethics Committee of the National Hospital for Neurology and Neurosurgery and the Institute of Neurology. Twenty-eight subjects were recorded, but only 15 had at least two auditory startle reflexes on testing. Only the results in these subjects (13 female, 2 male; mean age: 29 yrs; range: 20–59 yrs) were therefore analyzed. EMG was recorded from deltoid, biceps, finger flexor, and first dorsal interosseous (1DI) using surface electrodes (Ag-Ag, 9-mm diam) placed 3 cm apart on the muscle belly with the exception of 1DI where the reference electrode was placed over the proximal metocarpo-phalangeal joint of the index finger. EMG was also recorded from sternocleidomastoid, and the onset of activity in this muscle was used to trigger the selection of poststimulation startle blocks (see later). Facial muscles, which are usually activated during the startle response such as orbicularis oculi, masseter or mentalis (Brown et al. 1991) were not recorded as significant cross-talk between these muscles was to be expected. Coherence between right and left sternocleidomastoid muscles was not evaluated for similar reasons.
Subjects sat on a chair and were asked to provide a gentle background contraction of deltoid, biceps, finger flexors, and 1DI, bilaterally, while 1) unexpected acoustic stimuli (1 kHz tone of 50-ms duration at 98 dB) were delivered pseudorandomly and binaurally through headphones once every 5 min or so, or 2) they voluntarily mimicked a startle response at a rate of once every 10 s after an initial learning session. The voluntary startles served to show that any drive identified in the ASR was not related to background contraction, some nonspecific feature of phasic movements or of the analytical approach utilized. However, given that the physiological corticospinal drive to motor units is attenuated during movement (Brown et al. 1998; Kilner et al. 1999), voluntary startles did not allow us to contrast the pattern of the corticospinal drive to muscles with that evident during reflex startles. We therefore 3) also asked the same subjects to tonically contract their deltoid, biceps and 1DI muscles bilaterally at a level <50% maximal voluntary contraction for a period of 60s.
EMG was band-pass filtered between 53 and 1,000 Hz. The high-pass setting was chosen to limit contamination by movement artifact. Signals were amplified and digitized with 12-bit resolution by a CED 1401 A/D converter. The sampling rate was 2 kHz. Signals were displayed and stored on a PC by a software package (CED Spike 2, version 4).
Analysis
Frequency analysis was performed on the ASRs recorded in the 15 subjects. To this end, the 0.92 s after the onset of each ASR (defined in sternocleidomastoid) was extracted from the recording. Only ASRs with a mean rectified EMG level in each block greater than thrice prestimulation background (in sternocleidomastoid, deltoid, and biceps muscles) were analyzed. In this way, habituated startles were avoided. All the extracted ASRs were then concatenated to give a total record of 100 s, which was downsampled by averaging successive pairs of data points after digitally low-pass filtering at 500 Hz to avoid aliasing. Sham startle responses and submaximal voluntary contraction were processed in a similar fashion, concatenating the same data lengths as used in the ASR from each subject. Table 1 shows how many ASRs individual subjects contributed to the whole sample.
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Coherence and cumulant density estimates were estimated from rectified EMG using methods outlined by Halliday and colleagues (1995). The principal statistical tool used for data analysis in this study was the discrete Fourier transform and parameters derived from it, all of which were estimated by dividing the concatenated records into a number of disjoint sections of equal duration (512 data points) and estimating spectra by averaging across these discrete sections (Halliday et al. 1995). The frequency resolution of all spectra was 2 Hz.
In the frequency domain estimates of the autospectrum of the EMG, fAA(
) and fBB(), were constructed, along with estimates of coherence, RAB() 2 between EMG signals A and B. Coherence is a measure of the degree to which one can linearly predict change in one signal given a change in another signal (Brillinger 1981; Halliday et al. 1995; Rosenberg et al. 1989). It is a unitless measure, bounded from 0 to 1. Coherence was calculated according to
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denotes the frequency and fAB() is the cross spectrum between A and B. Coherence was considered to be significant if it exceeded the 95% confidence level.
In the time domain, the cumulant density function was estimated from the cross spectrum, fAB(), via an inverse Fourier transform. Cumulant densities provide a general measure of statistical dependence between random processes and will assume the value zero if the processes are independent (Halliday et al. 1995). Confidence limits for autospectra, coherence, and cumulant density estimates were calculated as previously described (Halliday et al. 1995).
Statistics
The power in each bin of autospectra was expressed as the relative percentage of the total power of each autospectrum to facilitate comparison between muscles and subjects. The variance of the coherence was normalized by transforming the square root of the coherence (a complex valued function termed coherency) at each frequency using the Fisher transform. This results in values of constant variance for each record given by 1/2L where L is the number of segment lengths used to calculate the coherence. To test normalized power and transformed EMG-EMG coherences for statistical significance, a repeated-measures general linear model was performed using the three contraction conditions and frequency band as the main effects. Separate models were performed for deltoid and 1DI and for deltoid-biceps and finger flexor-1DI, respectively. Where results were nonspherical, a Greenhouse-Geisser correction was used and when differences were significant a pair-wise Student's t-test was carried out.
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RESULTS |
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Figure 2 demonstrates the averaged spectra of the percentage total EMG power for deltoid, biceps, and 1DI, with the pooled data from homologous muscles on the two sides of the body. The results from ASR, voluntary sham startles and tonic voluntary contractions are illustrated. Deltoid EMG has a peak centered 12–14 Hz during the ASR. A similar, albeit less distinct feature, is seen in the ASR spectrum from biceps. This feature is absent during voluntary sham startles and tonic voluntary contraction.
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The coherence spectra between right and left deltoid, biceps, and 1DI during ASR, voluntary sham startles, and tonic voluntary contractions are given in Fig. 3, A, C, and E. The deltoid-deltoid and biceps-biceps EMG coherence during the ASR was above the 95%-significance level between 10 and 20 Hz and showed a discrete peak around 12–14 Hz. The peak was biggest in deltoid (Fig. 3A), where 20% of the activity at 12 Hz was synchronized between the two sides of the body. Conversely, in the voluntary sham startle and tonic voluntary contraction there was only minor coherence >10 Hz. Note that 1DI-1DI coherence (Fig. 3E) was little different in the ASR, sham startle, and tonic voluntary contraction. To check whether volume conduction could account for the coherence between bilateral muscles, we leveled the surface recorded analogue EMG signals and then performed frequency analysis on the two resulting point processes. The result for deltoid, the muscle with the shortest distance between itself and its homologue, is shown in Fig. 3 (inset). There remains a clear peak at 14 Hz in the point process coherence pooled across subjects. Note that, in line with the lower information content of the point process, the coherence was lower than between the analogue signals (Fig. 3A).
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Figure 3, B, D, and F, are the cumulant density estimates for the ASR. The cumulant density estimate for deltoid has a broad central peak with side-lobes every 70–80 ms (Fig. 3B). Side-lobes are much less distinct in biceps (Fig. 3B) and absent in 1DI (Fig. 3B). They were also absent during voluntary sham startles and tonic voluntary contractions (not shown) in all of the muscles. The cumulant density function was estimated from blocked and hanning windowed data. Note that the cross-correlograms between homologous muscles were almost identical to the cumulant density estimates (Fig. 3, B, D, and F), so that the periodicity evident in the cumulant density estimates for homologous deltoid and biceps muscle pairs were not epiphenomena of the way in which data were blocked.
However, pooled coherence spectra, such as those shown in Figs. 2 and Fig. 3, B, D, and F, can be relatively dominated by a few individuals with very high EMG-EMG coherence, and confidence levels established across the whole spectrum (Halliday et al. 1995) do not necessarily take this into account. To corroborate the consistency of our findings across the subject group, we therefore randomly divided the sample of 100 s of EMG from each condition into five segments consisting of 20 s. The percentage total power in each of the five segments was entered into a general linear model with conditions (3 levels: ASR, sham startle, voluntary contraction) and frequency (2 levels: 10–20 Hz, 20–30 Hz) as main effects. There was a significant interaction between condition and frequency in deltoid [F(2,8) = 50.843, P < 0.001] but not for 1DI. Post hoc analysis revealed a significant difference between the ASR and both the sham startles (P = 0.01) and voluntary contraction (P = 0.017) in the 10–20 Hz frequency band. Figure 4A shows the averaged normalized power across the five segments of 20 s.
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Similarly, transformed coherences from the 20-s segments were entered into a general linear model, which also showed a significant main effect for frequency and condition only for deltoid [F(2,8) = 27.948, P = 0.01]. Here differences were significant between the ASR and both the sham startles (P = 0.006) and voluntary contractions (P < 0.01) as well as between sham startles and voluntary contractions (P = 0.03) in the 10- to 20-Hz band Averaged transformed coherence from the five 20-s segments are illustrated in Fig. 4B. Note that power and coherence in the 10- to 20-Hz band were both higher in deltoid in the ASR than in sham startles or tonic voluntary contraction, so that changes in coherence were not due to modulations in nonlinearly related frequency components (Florian et al. 1998).
In addition, the pattern of pooled EMG-EMG coherence detailed in Fig. 3 was represented individually among those subjects with >10 blocks of EMG during reflex startles (i.e., sufficient to estimate coherence). Figure 5 contrasts power and coherence spectra in reflex and voluntary startles in two such subjects.
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Finally we should consider whether the coherence between homologous muscles at 10–20 Hz during the ASR could reflect the square wave nature of the acoustic stimulus. Could the stimulus have elicited a pulse of bilateral reflex EMG activity of similar duration, which then appeared in coherence spectra as a peak in coupling? If tone offset at 50 ms was responsible for the change, coherence spectra should be altered at 20 Hz and not the 14-Hz peak seen here. Even if we were to consider a delay in the offset of the EMG pulse, to give a period of 70–80 ms appropriate for the frequencies detected in this study, there are several reasons for believing this to be an unlikely explanation. First, reflex EMG activity was elicited in several muscles but only coherence between deltoid and, to a lesser extent biceps, demonstrated a peak at 10–20 Hz. Second, both the raw EMG records (Fig. 1A), the cumulant density estimates and the cross-correlograms of deltoid and biceps muscles (Fig. 3) indicated that reflex EMG bursts at 70–80 ms were repetitive rather than single.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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15 Hz, suggesting that the reticulospinal drive at this frequency may have mechanically important effects (Nathan and Tavi 1990).
Why should neurons in the primate motor cortex tend to synchronize motor units in the distal upper limb muscles at 20–30 Hz (Baker et al. 1997, 1999, 2001; Murthy and Fetz 1996), whereas those giving rise to the reticulospinal drive after acoustic stimulation tend to synchronize at 10–20 Hz? It seems possible that this reflects differences in the central network properties of the respective sites. In contrast, differences in peripheral feedback delays are unlikely to account for the different synchronization patterns. If anything, the shorter peripheral conduction time to and from proximal muscles would favor a higher frequency feedback drive to proximal than distal muscles, and yet the reticulospinal drive to proximal muscles causes synchronization at lower frequency than the corticospinal drive preferentially distributed to distal upper limb muscles.
The reticulospinal drive demonstrated here can be contrasted in character with the corticospinal drive to muscle. The latter does not lead to bilateral synchronization, preferentially involves distal limb muscles, and results in EMG-EMG coherence at generally higher frequencies (Carr et al. 1994; Farmer et al. 1990, 1993; Marsden et al. 1999). In voluntary tonic contractions of weak to moderate intensity, cortical drive leads to contralateral EMG-EMG coherence over the 15- to 30-Hz band (Kilner et al. 1999), whereas during strong contractions or movement cortical drive tends to synchronize motor units in the Piper range of 30–60 Hz (Brown 2000). Recently, corticomuscular coherence has been reported in the frequency range of physiological tremor (8–12 Hz). However, this coupling is generally weak, and it is unclear whether it is afferent or efferent in origin (Marsden et al. 2001; Raethjen et al. 2000b). In any case, physiological postural, action, and force tremors are not bilaterally synchronous (Marsden et al. 1969; Vallbo and Wessberg 1993), although, exceptionally, pathological tremors may exhibit synchronization across the muscles of the two sides of the body (Lauk et al. 1999; O'Sullivan et al. 2002; Raethjen et al. 2000).
In particular, the bilaterally coherent muscle activity documented here is reminiscent of that seen in the pathological condition of primary orthostatic tremor. The latter is associated with strong synchronization of muscle activity within and between limbs at 13–18 Hz. Synchronization is most evident on standing, and characteristically abates during the swing phase of gait (Britton et al. 1992; Heilman 1984; McManis and Sharbrough 1993). The tremor frequency overlaps with the frequency of synchronization seen in the ASR, and it is interesting to note that reticulospinal neurons in the cat medullary and caudal pontine regions exhibit phasic modulation that is correlated to locomotor activity (Drew et al. 1986; Orlovsky 1970; Perreault et al. 1993; Shimamura and Kogure 1983; Shimamura et al. 1982). A similar phenomenon may be seen in humans where the 8- to 20-Hz drive to tibialis anterior motor units is suppressed during the mid-swing phase of walking (Halliday et al. 2003). Recently, Sharott et al. (2003) showed that healthy subjects could develop a similar bilateral synchronization at 13–18 Hz in leg muscles when particularly unsteady. The possibility arises that the upper limb drive in the normal auditory startle reflex, pathological primary orthostatic tremor, and the orthostatic tremor of posturally challenged healthy subjects involve a similar reticulospinal generator.
In summary, we have identified a pattern of EMG-EMG coherence that is associated with nonrespiratory reticulospinal activity in the human. The challenge now is to define when this drive is manifest in health and how it may be deranged in disease.
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FOOTNOTES |
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Address for reprint requests: P. Brown, Sobell Department of Motor Neuroscience and Movement Disorders (Box 146), Institute of Neurology, Queen Square, London WC1 3BG, United Kingdom (E-mail: P.Brown{at}ion.ucl.ac.uk).
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REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Baker SN, Olivier E, and Lemon RN. Coherent oscillations in monkey motor cortex and hand muscle EMG show task-dependent modulation. J Physiol 501: 225–241, 1997.[ISI][Medline]
Baker SN, Spinks R, Jackson A, and Lemon RN. Synchronization in monkey motor cortex during a precision grip task. I. Task-dependent modulation in single-unit synchrony. J Neurophysiol 85: 869–885, 2001.
Brillinger DR. Time Series-Data Analysis and Theory (2nd ed.). San Francisco, CA: Holden Day, 1981.
Britton TC, Thompson PD, van der KW, Rothwell JC, Day BL, Findley W, and Marsden CD. Primary orthostatic tremor: further observations in six cases. J Neurol 239: 209–217, 1992.[ISI][Medline]
Brown P. The Piper rhythm and related activities in man. Progress in Neurobiology, 60: 97–108, 2000.[ISI][Medline]
Brown P, Farmer SF, Halliday DM, Marsden JF, and Rosenberg JR. Coherent cortical and muscle discharge in cortical myoclonus. Brain 122: 461–472, 1999.
Brown P, Rothwell JC, Thompson PD, Britton TC, Day BL, and Marsden CD. New observations on the normal auditory startle reflex in man. Brain 114: 1891–1902, 1991a.
Brown P, Rothwell JC, Thompson PD, Britton TC, Day BL, and Marsden CD. The hyperekplexias and their relationship to the normal startle reflex. Brain 114: 1903–1928, 1991b.
Brown P, Salenius S, Rothwell JC, and Hari R. Cortical correlate of the Piper rhythm in humans. J Neurophysiol 80: 2911–2917, 1998.
Carr LJ, Harrison LM, and Stephens JA. Evidence for bilateral innervation of certain homologous motoneuron pools in man. J Physiol 475: 217–227, 1994.
Conway BA, Halliday DM, Farmer SF, Shahani U, Maas P, Weir AI, and Rosenberg JR. Synchronization between motor cortex and spinal motoneuronal pool during the performance of a maintained motor task in man. J Physiol 489: 917–924, 1995.[ISI][Medline]
Davis M, Gendelman DS, Tischler MD, and Gendelman PM. Primary acoustic startle circuit: lesion and stimulation studies. J Neurosci 2: 791–805, 1982.[Abstract]
Drew T, Dubuc R, and Rossignol S. Discharge patterns of reticulospinal and other reticular neurons in chronic, unrestrained cats walking on a treadmill. J Neurophysiol 55: 375–401, 1986.
Edinger L and Fisher B. Ein Mensch ohne Gro
hirn. Pfluegers Ges Physiol 152: 535–562, 1913.
Farmer SF, Bremner FD, Halliday DM, Rosenberg JR, and Stephans JA. The frequency content of common synaptic inputs to motoneurons studies during isometric voluntary contraction in man. J Physiol 470: 127–155, 1993.
Farmer SF, Ingram DA, and Stephens JA. Mirror movements studied in a patient with Klippel-Feil syndrome. J Physiol 428: 467–484, 1990.
Florian G, Andrew C, and Pfurtscheller G. Do changes in coherence always reflect changes in functional coupling. Electroencephalogr Clin Neurophysiol 106: 87–91, 1998.[ISI][Medline]
Gross J, Tass PA, Salenius S, Hari R, Freund HJ, and Schnitzler A. Cortico-muscular synchronization during isometric muscle contraction in humans as revealed by magnetoencephalography. J Physiol 527: 623–631, 2000.
Grosse P, Guerrini R, Parmiggiani L, Bonanni P, Pogosyan A, and Brown P. Abnormal corticomuscular and intermuscular coupling in high frequency rhythmic myoclonus. Brain 126: 326–342, 2003.
Halliday DM, Conway BA, Christensen LOD, Hansen NL, Petersen NP, and Nielsen JB. Functional coupling of motor units is modulated during walking in human subjects. J Neurophysiol 89: 960–968, 2003.
Halliday DM, Conway BA, Farmer SF, and Rosenberg JR. Using electroencephalography to study functional coupling between cortical activity and electromyograms during voluntary contractions in humans. Neurosci Lett 241: 5–8, 1998.[ISI][Medline]
Halliday DM, Rosenberg JR, Amjad AM, Breeze P, Conway BA, and Farmer SF. A framework for the analysis of mixed time series/point process data—theory and application to the study of physiological tremor, single motor unit discharges and electromyograms. Prog Biophys Mol Biol 64: 237–278, 1995.[ISI][Medline]
Hammond GR. Lesions of the pontine and medullary reticular formation and prestimulus inhibition of the acoustic startle reaction in rats. Physiol Behav 10: 239–243, 1973.[Medline]
Heilman KM. Orthostatic tremor. Arch. Neurol 41: 880–881, 1984.[Abstract]
Kilner JM, Baker SN, Salenius S, Jousmaki V, Hari R, and Lemon RN. Task-dependent modulation of 15–30 Hz coherence between rectified EMGs from human hand and forearm muscles. J Physiol 516: 559–570, 1999.
Kirkwood PA, Sears TA, Tuck DL, and Westgaard RH. Variations in the time course of the synchronization of intercostal motoneurons in the cat. J Physiol 327: 105–135, 1982.
Koch M. The neurobiology of startle. Prog Neurobiol 59: 107–128, 1999.[ISI][Medline]
Koch M, Lingenhöhl K, and Pilz PKD. Loss of the acoustic startle response following neurotoxic lesions of the caudal pontine reticular formation: possible role of giant neurons. Neuroscience 49: 617–625, 1992.[ISI][Medline]
Koch M and Schnitzler HU. The acoustic startle response in rats-circuits mediating evocation, inhibition and potentiation. Behav Brain Res 89: 35–49, 1997.[ISI][Medline]
Köster B, Lauk M, Timmer J, Winter T, Guschlbauer B, Glocker FX, Danek A, Deuschl G, and Lucking CH. Central mechanisms in human enhanced physiological tremor. Neurosci Lett 241: 135–138, 1998.[ISI][Medline]
Kuypers HGJM. Anatomy of the descending pathways. In: Handbook of Physiology. The Nervous System. Motor Control. Bethesda, MD: Am. Physiol. Soc., sect. 1, part II, p. 597–666, 1981.
Lauk M, Koster B, Timmer J, Guschlbauer B, Deuschl G, and Lücking CH. Side-to-side correlation of muscle activity in physiological and pathological human tremors. Clin Neurophysiol 110: 1774–1783, 1999.[ISI][Medline]
Leitner DS, Powers AS, and Hoffman HS. The neural substrate of the startle response. Physiol Behav 25: 291–297, 1980.[Medline]
Lingenhöhl K and Friauf E. Giant neurons in the caudal pontine reticular formation receive short latency acoustic input: an intracellular recording and HRP-study in the rat. J Comp Neurol 325: 473–492, 1992.[ISI][Medline]
Marsden CD, Meadows JC, Lange GW, and Watson RS. The relation between physiological tremor of the two hands in healthy subjects. Electroencephalogr Clin Neurophysiol 27: 179–185, 1969.[ISI][Medline]
Marsden J, Limousin-Dowsey P, Fraix V, Pollak P, Odin P, and Brown P. Intermuscular coherence in Parkinson's disease: effects of subthalamic nucleus stimulation. Neuroreport 12: 1113–1117, 2001a.[ISI][Medline]
Marsden JF, Brown P, and Salenius S. Involvement of the sensorimotor cortex in physiological force and action tremor. Neuroreport 12: 1937–1941, 2001b.[ISI][Medline]
Marsden JF, Farmer SF, Halliday DM, Rosenberg JR, and Brown P. The unilateral and bilateral control of motor unit pairs in the first dorsal interosseus and paraspinal muscles in man. J Physiol 521: 553–564, 1999.
Matsumoto J, Fuhr P, Nigro M, and Hallett M. Physiological abnormalities in hereditary hyperekplexia. Ann Neurol 32: 41–50, 1992.[ISI][Medline]
McManis PG and Sharbrough FW. Orthostatic tremor: clinical and electrophysiologic characteristics. Muscle Nerve 16: 1254–1260, 1993.[ISI][Medline]
Mima T, Gerloff C, Steger J, and Hallett M. Frequency cooling of motor system coherence and phage estimation between cortical rhythm and motor neural firing in luminance (Abstract). Soc Neurosci Abstr 24: 1768, 1998.
Murthy VN and Fetz EE. Synchronizaton of neurons during local field potential oscillations in sensorimotor cortex of awake monkeys. J Neurophysiol 76: 3968–3982, 1996.
Nathan R and Tavi M. The influence of stimulation pulse frequency on the generation of joint moments in the upper limb. IEEE Trans Biomed Eng 39: 317–322, 1990.
O'Sullivan JD, Rothwell J, Lees AJ, and Brown P. Bilaterally coherent tremor resembling enhanced physiologcal tremor: report of three cases. Mov Disord 17: 387–391, 2002.[ISI][Medline]
Orlovsky GN. Work of the reticulo-spinal neurons during locomotion. Biophysics 15: 761–771, 1970.
Perreault MC, Drew T, and Rossignol S. Activity of medullary reticulospinal neurons during fictive locomotion. J Neurophysiol 69: 2232–2247, 1993.
Raethjen J, Lindemann M, Dumplemann M, Stolze H, Wenzelburger R, Pfister G, Elger CE, Timmer J, and Deuschl G. Cortical correlates of physiological tremor (Abstract). Mov Disord 15, Suppl 3: 90, 2000a.
Raethjen J, Lindemann M, Schmaljohann H, Wenzelburger R, Pfister G, and Deuschl G. Multiple oscillators are causing Parkinisonian and essential tremor. Mov Disord 15: 84–94, 2000b.[ISI][Medline]
Rosenberg JR, Amjad AM, Breeze P, Brillinger DR, and Halliday DM. The Fourier approach to the identification of functional coupling between neuronal spike trains. Prog Biophys Mol Biol 53: 1–31, 1989.[ISI][Medline]
Rosenberg JR, Halliday DM, Breeze P, and Conway B. A. Identification of patterns of neuronal activity, partial spectra, partial coherence, and neuronal interactions. J Neurosci Methods 83: 57–72, 1998.[ISI][Medline]
Salenius S, Portin K, Kajola M, Salmelin R, and Hari R. Cortical control of human motoneuron firing during isometric contraction. J Neurophysiol 77: 3401–3405, 1997.
Schultz G, Lambertz B, Schultz B, Langhorst P, and Krienke B. Reticular formation of the lower brain stem. A common system for cardio-repiratory and somatomotor functions. Cross-correlation analysis of discharge patterns of neighboring neurones. J Auton Nerv Syst 12: 35–62, 1985.[ISI][Medline]
Sharott A, Marsden J, and Brown P. Primary orthostatic tremor is an exaggeration of a physiological response to instability. Mov Disord 18: 195–199, 2003.[ISI][Medline]
Shimamura M, Kogure I, and Wada SI. Reticular neuron activities associated with locomotion in thalamic cats. Brain Res 231: 51–62, 1982.[ISI][Medline]
Shimamura M and Kogure I. Discharge patterns of reticulospinal neurons corresponding with quadrupedal leg movements in thalamic cats. Brain Res 260: 27–34, 1983.[ISI][Medline]
Spauschus A, Marsden JF, Halliday DM, Rosenberg JR, and Brown P. The origin of ocular microtremor in man. Exp Brain Res 126: 556–562, 1999.[ISI][Medline]
Vallbo AB and Wessberg J. Organization of motor output in slow finger movements in man. J Physiol 469: 673–691, 1993.
Valldeoriola F, Valls-Solé J, Tolosa E, Nobbe FA, Muñoz JE, and MartíJ. The acoustic startle response is normal in patients with multiple system atrophy. Mov Disord 12: 697–700, 1997.[ISI][Medline]
Vidailhet M, Rothwell JC, Thompson PD, Lees AJ, and Marsden CD. The auditory startle response in the Steele-Richardson-Olszewski syndrome and Parkinson's disease. Brain 115: 1181–1192, 1992.
Yeomans JS and Frankland PW. The acoustic startle reflex: neurons and connections. Brain Res Rev 21: 301–314, 1996.
Yeomans JS, Li L, Scott BW, and Frankland PW. Tactile, acoustic and vestiblar systems sum to elicit the startle reflex. Neurosci Biobehav Rev 26: 1–11, 2002.[ISI][Medline]
Yeomans JS, Rosen JB, Barbeau J, and Davis M. Double-pulse stimulation of startle-like responses in rats: refractory periods and temporal summation. Brain Res 486: 147–158, 1989.[ISI][Medline]
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G. Mochizuki, T. D. Ivanova, and S. J. Garland Factors Affecting the Common Modulation of Bilateral Motor Unit Discharge in Human Soleus Muscles J Neurophysiol, June 1, 2007; 97(6): 3917 - 3925. [Abstract] [Full Text] [PDF]
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J.-S. Blouin, J. T. Inglis, and G. P. Siegmund Startle responses elicited by whiplash perturbations J. Physiol., June 15, 2006; 573(3): 857 - 867. [Abstract] [Full Text] [PDF]
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