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Experimental Physiology 89.1 pp 82-88
DOI: 10.1113/expphysiol.2003.002637
© The Physiological Society 2004
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Comparison of the firing patterns of human postganglionic sympathetic neurones and spinal {alpha} motoneurones during brief bursts

Vaughan G. Macefield1 and Mikael Elam2

1 Prince of Wales Medical Research Institute and the University of New South Wales, Sydney, Australia2 Institute of Clinical Neuroscience, Sahlgren University Hospital, Göteborg, Sweden


   Abstract
Top
 Abstract
Introduction
 Methods
 Results
 Discussion
 References
 
Focal recordings from individual postganglionic sympathetic neurones in awake human subjects have revealed common firing properties. One of the most striking features is that they tend to fire only once per sympathetic burst. Why this should be so is not known, but we propose that the short duration of the burst may limit the number of times a sympathetic neurone can fire. Indeed, while the normal variation in cardiac interval and burst duration is too narrow to reveal a correlation between burst duration and the number of spikes generated, we know that spike generation is doubled when burst duration is doubled following ectopic heart beats. To test the hypothesis that the burst duration constrains the firing of individual sympathetic neurones to one per burst, we used the human skeletomotor system as a model for the sympathetic nervous system, which allowed us to vary burst duration and amplitude experimentally. Intramuscular recordings were made from 27 single motor units ({alpha} motoneurones) in the tibialis anterior or soleus muscles of seven subjects; multiunit EMG activity was recorded via surface electrodes and blood pressure was recorded continuously. Subjects were instructed to generate EMG bursts of varying amplitude in the intervals between heart beats. By constraining the firing of {alpha} motoneurones to brief (~400 ms) bursts we could emulate real sympathetic bursts. Individual motoneurones generated 0–7 spikes during the emulated sympathetic bursts, with firing patterns similar to those exhibited by real sympathetic neurones. Eleven motor units showed significant positive linear correlations between the number of spikes they generated within a burst and its amplitude, whereas for 17 motor units there were significant positive correlations between the number of spikes and burst duration. This indicates that burst duration is a major determinant of the number of times an {alpha} motoneurone will fire during a brief burst, and we suggest that the same principle may explain the firing pattern typical of human sympathetic neurones.

(Received 31 July 2003; accepted after revision 10 October 2003)
Corresponding author V. G. Macefield: Prince of Wales Medical Research Institute, Barker St, Randwick NSW 2031, Australia.  Email: vg.macefield{at}unsw.edu.au


   Introduction
Top
 Abstract
 Introduction
Methods
 Results
 Discussion
 References
 
It has been known since the first direct recordings of sympathetic neural traffic were made in awake human subjects, via tungsten microelectrodes inserted percutaneously into a peripheral nerve, that sympathetic outflow to muscle and skin occurs in bursts (Hagbarth & Vallbo, 1968; Delius et al. 1972; Hagbarth et al. 1972). And since the first single-unit recordings were made from identified muscle vasoconstrictor neurones in awake human subjects (Macefield et al. 1994) a consistent feature of the firing properties of all postganglionic sympathetic axons – whether they be muscle vasoconstrictor (Macefield et al. 1994; Macefield & Wallin, 1999a), cutaneous vasoconstrictor (Macefield & Wallin, 1999b) or sudomotor (Macefield & Wallin, 1996) neurones – has been their tendency to fire only once per burst (for review see Macefield et al. 2002). We have also confirmed this pattern in patients with pathological increases in sympathetic drive (Macefield et al. 1999; Elam et al. 2002). Indeed, in patients with severe heart failure – in whom muscle sympathetic drive is greatly elevated – we have shown that the percentages of bursts in which muscle vasoconstrictor neurones (n= 16) generated one, two, three or four spikes per burst (71.4 ± 5.6%, 18.2 ± 2.3%, 7.0 ± 1.9% and 2.2 ± 1.0%, respectively) were statistically identical to those of 33 neurones recorded in heathy subjects at rest (72.7 ± 3.3%, 18.4 ± 2.0%, 5.1 ± 1.1% and 2.9 ± 1.1%; Macefield et al. 1999, 2002). But why should individual sympathetic neurones adopt this pattern, given that they can generate up to eight spikes per burst (Macefield et al. 2002)? It is known that injecting a depolarizing current into postganglionic vasoconstrictor (‘phasic’) neurones in the guinea pig produces a burst of impulses (Cassell et al. 1986), so biophysical properties do not prevent multiple firing in these neurones. And even if preganglionic properties limited multiple firing, the strong EPSPs exerted by two or more convergent preganglionic neurones would certainly promote multiple firing of the postganglionic neurone (McLachlan et al. 1997). We also know that a shift towards multiple firing does occur during the long sympathetic bursts that follow ectopic heart beats, in which muscle vasoconstrictor drive is acutely elevated (Elam & Macefield, 2001).

If there is no increase in multiple firing during increases in sympathetic drive, this suggests that the increase in burst intensity is brought about primarily by the recruitment of silent neurones (Macefield et al. 2002). There is an attractive teleological argument for limiting the firing of individual postganglionic neurones to only one spike per burst: this would reduce the likelihood of transmitter depletion from the nerve terminals. Indeed, evidence for transmitter depletion at sympathetic nerve terminals has been shown (e.g. Lin et al. 2001). However, there is another explanation. What if there simply isn't enough time for neurones to fire more often within a burst? We know that the duration of multiunit sympathetic bursts varies within a given subject (Sundlöf & Wallin, 1977), but we do not know whether this variation matches that of the cardiac interval.

We wanted to test the hypothesis that burst duration constrains the firing pattern of individual sympathetic neurones by looking at another motor system – the skeletomotor system. Because this is under voluntary control we can produce patterns of motor output that have the characteristics of sympathetic bursts. By recording from individual {alpha} motoneurones (i.e. from individual motor units within the contracting muscle) we can compare their behaviour during bursts of electromyographic activity (EMG) that emulate sympathetic bursts. Our data show for the first time that human {alpha} motoneurones, which normally fire in long trains, can exhibit patterns of activity that are essentially identical to those of human postganglionic sympathetic neurones. This leads us to conclude that the characteristic firing pattern of sympathetic neurones is simply an ‘emergent property’ of the fact that sympathetic bursts are too short to allow prolonged firing. A small part of this work has appeared in a recent review (Macefield & Elam, 2003).


   Methods
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 Abstract
 Introduction
 Methods
Results
 Discussion
 References
 
Experiments were performed on seven seated male subjects (28–44 years), including the two authors, and were conducted under the approval of the Human Research Ethics Committee of the University of New South Wales. A high-impedance tungsten microelectrode (type TM33B20, World Precision Instruments, Sarasota, FL, USA) was inserted into the belly of the tibialis anterior muscle (in one subject the soleus muscle was used) and a search for unitary EMG activity made during weak contractions. Surface EMG was recorded with Ag–AgCl electrodes placed approximately 5 cm apart. Arterial blood pressure was monitored continuously via radial arterial tonometry (Colin NIBP 7000, Colin Corp., Kamaki, Japan) and the beat-to-beat waveform displayed with the unitary and surface EMG signals on a computer monitor in front of the subject. Single-unit EMG activity was amplified (200x), filtered (10 Hz to 5 kHz), digitized at 12.8 kHz (12 bits) and stored on disk via the SC/ZOOM data acquisition and analysis system (Department of Physiology, University of Umeå, Sweden). Surface EMG (gain 100x, 10 Hz to 1 kHz) was sampled at 3.2 kHz and blood pressure at 400 Hz. Subjects were asked to perform weak isotonic movements of the ankle at various amplitudes in the intervals between heart beats; they were not instructed to make the movements particularly brisk. An average of 102 ± 11 (mean ±S.E.M.) bursts were sampled from each recording site, following which the microelectrode was adjusted and another unit sought. Between three and six successful unitary recordings were made in each subject. During off-line analysis a copy of the surface EMG signal was RMS processed to emulate a leaky integrator (time constant 100 ms) and the morphology of every spike of a candidate unit carefully checked using the spike recognition facility incorporated in the SC/ZOOM software. Cursors were placed at the beginning and end of the EMG burst (as defined by the RMS-processed signal) and the computer measured the burst duration and peak amplitude and the number of spikes a unit fired in each burst. Bursts longer than a cardiac interval were not included in the analyses. All values are expressed as means and standard errors. All statistical evaluation of the data was performed in STATISTICA for Windows v.6 (StatSoft Inc., Tulsa, OK, USA), using ANOVA. Differences were considered statistically significant at P P 0.05.


   Results
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 Abstract
 Introduction
 Methods
 Results
Discussion
 References
 
Single-unit recordings were made from a total of 27 motor units (23 in tibialis anterior, 4 in soleus) during brief, self-paced isotonic movements of the ankle. As there were no differences in firing patterns recorded from the two muscles the data were pooled. All motor units had low recruitment thresholds (P5% of maximal voluntary contraction). Multi-unit EMG bursts were generated in the intervals between heart beats in a manner that emulated multiunit sympathetic bursts, i.e. waves of bursts that waxed and waned in amplitude. Across subjects the mean duration of the EMG bursts (as measured from the surface EMG) was 401 ± 11 ms (n= 27). An example of a unitary recording from tibialis anterior is shown in Fig. 1. In the left panel the unit fired 2–3 spikes per emulated sympathetic burst, but could generate anywhere between 0 and 7 spikes per burst. As shown in the right panel, this motor unit could – as expected – fire in a sustained fashion during a slowly ramping contraction, as could all units recorded in the present sample.



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  		Figure 1. 
Single motor unit firing in brief bursts and maintained contraction. Intramuscular recording from a single motor unit in the tibialis anterior muscle during brief phasic contractions in the interval between heart beats, emulating sympathetic bursts (left panel), and during a slowly ramping contraction (right panel). The motoneurone fired usually only 2–3 spikes per burst in the former condition, but in a sustained fashion in the latter.

 
Experimental records from another unit are shown in Fig. 2. This also tended to fire very few spikes per burst yet, as illustrated in the right panel, the number of spikes the motoneurone generated appeared to depend more on the duration of the burst than on its amplitude. Three examples of the firing pattern of individual motoneurones when constrained into a brief burst of activity are shown graphically in Fig. 3. The histograms in the top panels indicate the number of times a unit fired per EMG burst, including those when it was not recruited into the burst (open columns); the corresponding histograms in the lower panels represent only those bursts in which the unit was active. It is apparent from these examples that the firing probability (the proportion of bursts in which a motoneurone was active) varied across units. It is also apparent that in each of these examples the motoneurone primarily discharged only one spike per EMG burst.



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  		Figure 2. 
Single motor unit firing in emulated sympathetic bursts. Intramuscular recording from a single motor unit in the tibialis anterior muscle during emulated sympathetic bursts (brief phasic contractions in the interval beween heart beats). The unit fired 1–3 times in the brief bursts shown in the left panel, but often 4 times during the longer bursts shown in the right panel.

 


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  		Figure 3. 
Single motor unit firing patterns in emulated sympathetic bursts. Examples of the firing distributions of three single motor units in tibialis anterior during brief phasic contractions that emulate sympathetic bursts. Upper rows, percentage of cardiac intervals in which the motoneurones were quiescent (open columns) or fired 1, 2, 3 or 4 spikes (filled columns) per cardiac interval. Lower rows, same data after excluding those cardiac intervals in which a unit was silent.

 
Across motor units three patterns were seen: (i) 8/27 motor units (30%) fired mostly one spike per burst, as exemplified by Fig. 3, (ii) for 11 units (40%) the median number of spikes per burst was two, and (iii) for 8 units (30%) the median spike number was three. These firing distributions are shown graphically in Fig. 4A–C. It is striking that each of these patterns has also been seen in the discharge pattern of single sympathetic neurones recorded in awake human subjects. This is illustrated in the lower panels of Fig. 4, in which we show examples of the firing patterns of single muscle vasoconstrictor neurones recorded from patients with severe heart failure (data from Macefield et al. 1999 and Elam & Macefield, 2001).



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  		Figure 4. 
Firing distributions of motoneurones and sympathetic neurones. Mean firing distributions of single motor units during emulated sympathetic bursts (upper panels), grouped according to a median spike number of 1 (A), 2 (B) or 3 (C). To illustrate the similarity in firing patterns the lower panels show data from real sympathetic neurones recorded in patients with heart failure (data from Macefield et al. 1999 and Elam & Macefield, 2001).

 
Despite the differences in the median number of spikes generated by single {alpha} motoneurones during brief bursts there were no significant differences in mean duration of the parent EMG bursts (measured from the surface EMG) between the three groups of motor units shown in Fig. 4A–C (406 ± 28 ms, 403 ± 24 ms and 394 ± 28 ms, respectively). However, calculated from individual motor units there were significant correlations between the number of spikes generated in a burst and the duration and/or amplitude of the burst, though it must be recognized that correlating a quantal measure (number of spikes) against a continuous measure (burst duration or amplitude) may not allow the tightest of correlations.

Nevertheless, for 17 units (63%) significant positive linear correlations (r = 0.18–0.81) were found between burst duration and the number of spikes. As expected, the strongest correlations were observed for those units that generated a wide range of spikes per burst. For 11 units (40%), there was a significant positive correlation (r = 0.17–0.72) between the number of spikes and burst amplitude; with one exception, each of these units also exhibited significant correlations to burst duration. Graphical data from two motoneurones exhibiting a tight coupling between the number of spikes generated per burst and the duration of the burst are shown in Fig. 5. Both of these units failed to show a significant correlation between number of spikes and burst amplitude (not shown).



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  		Figure 5. 
Correlations between burst duration and number of spikes for two motoneurones. Linear correlations between burst duration (measured from surface EMG) and number of spikes generated per burst for two single motor units (A, B) in tibialis anterior during brief phasic contractions emulating sympathetic bursts.

 

   Discussion
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
References
 
The purpose of this study was to try to understand the firing behaviour of human postganglionic sympathetic neurones. To this end we used the human skeletomotor system as a model for the sympathetic nervous system (given that both can seen as motor systems), taking advantage of the voluntary control exerted over {alpha} motoneurones. By instructing subjects to perform weak isotonic contractions of a leg muscle (usually tibialis anterior – the dorsiflexor of the ankle) in the intervals between heart beats, brief EMG bursts were generated that emulated sympathetic bursts. Subjects were asked to vary the intensity of their contractions but to limit the duration of the EMG bursts to lie within the cardiac interval. Subjects observed their EMG and beat-to-beat blood pressure (recorded continuously) on a computer monitor. The emulated ‘sympathetic’ bursts were similar in duration (~400 ms) and range of relative burst amplitudes to those of real multiunit muscle sympathetic bursts.

Recordings from single motor units (i.e. {alpha} moto-neurones) in the contracting muscles revealed that individual motoneurones exhibit firing patterns that are strikingly similar to those of sympathetic neurones. Similar patterns have been recorded from human motor units during ballistic contractions of tibialis anterior, in which subjects were instructed to make a maximal isometric voluntary contraction as quickly as possible (Desmedt & Godaux, 1977). However, while units were observed to fire only a few spikes within the burst – and these were clustered at the beginning of the contraction – the number of spikes each unit generated within a burst (the firing distribution) was not reported. Nevertheless, these authors did show that the firing of human {alpha} motoneurones during these brief bursts was characterized by lower recruitment thresholds during ballistic versus slow ramp contractions and ‘unusually high instantaneous frequencies (60–120 Hz) at the onset of the contraction’, a feature that would result in the production of greater force in a shorter time. This mechanism has been observed during microstimulation of single human motor axons (Macefield et al. 1996; Thomas et al. 1999; Bigland-Ritchie et al. 2000), and greater effector–organ responses have been produced by stimulation of sympathetic axons with irregular stimuli that include intermittent high frequencies (Nilsson et al. 1985; Kunimoto et al. 1992).

All of the motor units recorded in the present study had low recruitment thresholds during brief bursts and during slow ramping contractions. The firing probability of a given unit during a sequence of emulated sympathetic bursts depended on the range of burst amplitudes the subjects generated; units were often silent in the smallest bursts but could generate up to seven spikes in the larger bursts. Indeed, for 11 motor units there was a significant positive linear correlation between burst amplitude and the number of spikes. For 17 units there was a significant positive correlation between the number of spikes and the duration of the burst. This merely confirms that, for the {alpha} motoneurone system, burst intensity is graded by firing probability (a unit is brought into a burst when it reaches its firing threshold) and an increase in multiple firing; it is also clear that recruitment of additional motoneurones plays a major role in increasing skeletomotor output, although it has been argued that changes in discharge frequency (rate coding) are more important in the gradation of muscle force (Kernell, 1992).

These same mechanisms are utilized by the sympathetic nervous system which, as noted above, can be seen simply as another motor system (or more correctly, another sensorimotor system). We know that individual postganglionic neurones, whether they be muscle vasoconstrictor, cutaneous vasocontrictor or sudomotor, behave in similar ways – in particular, they tend to fire only once per sympathetic burst (Macefield et al. 1994, 1999, 2002; Macefield & Wallin, 1996, 1999a,b; Elam & Macefield, 2001; Elam et al. 2002). This pattern, in which the median number of spikes generated by a sympathetic neurone in a burst is one, was observed in a third of the motor units during the emulated sympathetic bursts recorded in the present study (Fig. 4A). The second pattern (median number of spikes = 2; Fig. 4B) is similar to that seen during the large, broad bursts that are evoked by the long cardiac intervals following an ectopic heart beat (Elam & Macefield, 2001). In this condition, burst duration and amplitude are doubled – the amplitude is increased because the burst rise time is increased (i.e. the slope remains the same but the burst is terminated later), a phenomenon observed also during spontaneous variations in burst amplitude in healthy subjects at rest (Wallin et al. 1994). The third pattern (median number of spikes = 3; Fig. 4C) has been seen only once in the discharge of a single sympathetic neurone – a muscle vasoconstrictor neurone (with an unusual tendency to fire multiple spikes) that was recorded in a patient with severe heart failure (Fig. 4F).

The fact that each of the firing distributions seen in single motor units during emulated sympathetic bursts has been observed in the firing of real sympathetic neurones suggests that the characteristic firing pattern of sympathetic neurones is simply a reflection of the fact that, normally, sympathetic bursts are too short to allow prolonged firing. Not withstanding biophysical differences between postganglionic sympathetic and {alpha} motoneurones, we postulate that were it not for the bursting pattern imposed on the sympathetic neurones they would tend to fire in long trains – just like {alpha} motoneurones. In subjects with low heart rates (i.e. long cardiac intervals) muscle sympathetic activity is often high, yet in such a group we found that there was no shift towards multiple firing (Macefield & Wallin, 1999a). Data reanalysed from a group of heart-failure patients examined previously (Macefield et al. 1999; Elam & Macefield, 2001) revealed that there is no correlation between burst duration (or the number of spikes generated by individual muscle vasoconstrictor neurones) and cardiac interval across a range of heart rates (r = 0.05, n= 111 intervals). However, as pointed out above, it is also known that the prolonged cardiac intervals that follow ectopic heart beats in these patients evoke compensatory bursts that are twice as long (and twice as large) as sympathetic bursts produced in normal sinus rhythm (Elam & Macefield, 2001). This suggests that the physiological range of cardiac intervals, and the variation in duration of muscle sympathetic bursts, is so narrow that the number of spikes generated by muscle vasoconstrictor neurones within a given sympathetic burst is generally limited to one. It is only when the cardiac interval (and burst duration) is doubled that the number of spikes produced is also doubled, as we had previously demonstrated (Elam & Macefield, 2001).

It is known that the arterial baroreceptors provide the primary source by which the muscle vasoconstrictor neurones are constrained into firing in the intervals between heart beats, although cardiac rhythmicity is also expressed to a smaller extent by cutaneous vasoconstrictor (Macefield & Wallin, 1999b) and sudomotor neurones (Bini et al. 1981; Macefield & Wallin, 1996). However, even though cardiac rhythmicity is abolished after interupting all baroreceptor inputs by anaesthetic block of the glossopharyngeal and vagus nerves in human subjects, a bursting pattern is preserved – although with an increased burst duration (Fagius et al. 1985). This indicates that intrinsic mechanisms shape the sympathetic outflow into a bursting pattern (see Fagius, 1988), and suggests that if one were to record from individual sympathetic neurones during these prolonged bursts their discharge pattern would be characterized by a shift in their firing distribution away from solitary spikes towards multiple spikes – just as is seen following ectopic heart beats.


   References
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 
Bigland-Ritchie B, Zijdewind I & Thomas CK (2000). Muscle fatigue induced by stimulation with and without doublets. Muscle Nerve 23, 1348–1355.[CrossRef][Medline]

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Elam M & Macefield V (2001). Multiple firing of single muscle vasoconstrictor neurons during multiple cardiac dysrhythmias in human heart failure. J Appl Physiol 91, 717–724.[Abstract/Free Full Text]

Elam M, McKenzie D & Macefield V (2002). Mechanisms of sympatho-excitation: single-unit analysis of muscle vasoconstrictor neurons in awake OSAS subjects. J Appl Physiol 93, 297–303.[Abstract/Free Full Text]

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   Acknowledgements
 
This work was supported by the Prince of Wales Medical Research Institute, the Faculty of Medicine at the University of Göteborg and the Swedish Medical Research Council (MFR grant no.12170). V. G. Macefield is supported by the National Health and Medical Research Council of Australia (Program Grant 002306).





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