Presaccadic spike potential: a computer model based upon motor unit recruitment patterns in the extraocular muscles

Brain Research, 422 (1987) 377-380 Elsevier

377

BRE 22525

Presaccadic spike Ual: acomputer model recruitment patterns in the extr

unit rnmmies

Gary W. Thickbroom and Frank L. Mastaglia Departments of Medicine and Neurology, Queen Elizabeth I1 Medical Centre, Perth, W.A. (Australia)

(Accepted 30 June 1987) Key words: Presaccadic spike potential; Computer model; Extraocular muscle; Activation pattern

Details are presented of a computer model of the presaccadic 'spike' potential based upon the discharge properties of motor units in the extraocular muscles. The model provides support for the hypothesis that the spike potential represents the summated electrical activity from the near-synchronous recruitment of motor units in the extraocular muscles by the presaccadic burst of motoneurone activity.

A large amplitude potential of 2 0 - 3 0 ms duration is recorded near the orbits in man 10-40 ms before the onset of saccadic eye movements. This potential has been referred to as the 'spike' potential (SP) and has been thought to arise in the extraocular muscles by some workers 2'4'12 and to be of cerebral origin by others 1,8-11. On the basis of our observations in normal subjects and in patients with extraocular muscle palsies and hemispherectomy, we concluded that the SP is of myogenic origin and hypothesised that it represents the summated electrical activity from the near-synchronous recruitment of m o t o r units in the extraocular muscles, prior to the onset of the saccade 14-17. We now present further support for this hypothesis from a computer model based upon motor unit recruitment patterns in the extraocular muscles. The surface recorded ocular E M G was modelled by summing action potential trains from a hypothetical population of m o t o r units. The parameters of the model consisted of the n u m b e r of m o t o r units, the action potential amplitude and duration, the mean and dispersion of discharge frequencies for the population of m o t o r units, and the dispersion in recruitment time amongst units. Values were estimated for each of these parameters, and the effect of varying these

default values in the summed waveform was examined. The model parameters were defined as follows: (i) An arbitrary number of 250 motor units was selected. (ii) The wave shape of m o t o r umt action potentials recorded from the skin surface was assumed to be biphasic and was defined by two parameters, the durations of the negative and positive phases. Each phase was assumed to be triangular, and the amplitude of the positive (after) phase was such that the area of the two phases was equal. (iii) The discharge frequency of a single m o t o r unit was defined by the interdischarge interval (idi). The idi for a given unit was varied in time with a t 0 % jitter factor. The idi distribution for all units was defined by the mean (~i) and range (ai), the distribution being uniform in the range Pi ---oi. (iv) The recruitment time distribution was defined by an arbitrary mean onset of 100 ms and a range or (ms). Trains of action potentials for each unit were summed such that the mean time o f onset for all units was 100 ms after an arbitrary zero time point, with a dispersion across units given by o r . The distribution of recruitment times was triangular in the range 100 + a r ms.

Correspondence: F.L. Mastaglia, University Department of Medicine, Queen Elizabeth II Medical Centre, Nedtands, W.A. 6009, Australia.

0006-8993/87/$03.50 (~) 1987 Elsevier Science Publishers B.V. (Biomedical Division)

378 (v) T h e a m p l i t u d e of t h e s u r f a c e - r e c o r d e d p o t e n -

b u r s t t r a i n . T h i s was b a s e d u p o n t h e p o s s i b i l i t y t h a t

tials w a s m a d e t h e s a m e for all u n i t s , b u t p r o v i s i o n

w i t h h i g h firing r a t e s t h e m u s c l e f i b r e m e m b r a n e m a y

was m a d e for a r e d u c t i o n in a m p l i t u d e f o r a g i v e n

n o t b e fully r e p o l a r i s e d f o l l o w i n g t h e initial d e p o l a r i -

u n i t f o r its s e c o n d a n d s u b s e q u e n t d i s c h a r g e s in a

sation.

A

Fig. 1. Results of varying model parameters on modelled SP waveform. Unless otherwise stated, recruitment dispersion = + 10 ms, idi = 2 + 1 ms, duration of positive phase of action potential = 4 ms. Horizontal time axis = 850 ms. Figures given for the change in model parameters correspond respectively to the sequence of traces from top to bottom. A: recruitment dispersion increased from +2 ms to +16 ms in 2 ms steps. B: mean idi increased from 2 ms to 10 ms in 1 ms steps. Dispersion of +1 ms for all cases. C: idi dispersion increased from + 1 ms to +4 ms in 1 ms steps. Mean idi of 5 ms for all cases. D: reduction in amplitude of second and subsequent action potentials in train. Reduction of 0% to 90% of amplitude of first action potential in 10% steps (idi = 5 + 4 ms). E: increase in duration of second (+ve) component of action potential waveform of 1 ms to 4 ms in 1 ms steps (idi = 5 + 4 ms). F: sequence of 10 single sweep recordings of presaccadic spike potential (arrowheads) in a normal subject. Top trace eye velocity (mean of 10 traces); arrow indicates saccade onset. Secondary intrasaccadic SPs are seen during the accelerating phase of most of the saccades. Horizontal time axis, 1 s. Vertical calibration, 30¢tV.

379

It was found that a spike potential was generated when the following motor unit parameters were used: a recruitment dispersion of _+10 ms, an idi of 2 ms _+1 ms, and a 50% decline in the amplitude of the second and subsequent action potentials in a train. The effect on the SP of independently varying these parameters was then investigated (Fig. 1). When the recruitment dispersion (or) was increased from _+2 ms to _+16 ms with all other parameters constant the peak-to-peak and onset-to-peak amplitude of the SP decreased by approximately 60% and its duration increased from 4 ms to 11 ms. However, an SP was still clearly observable in the modelled waveform even with the longest o r. The amplitude and duration of the SP remained approximately constant when the mean idi was increased progressively from 2 ms to 10 ms while maintaining a constant dispersion of _+1 ms. With the longer mean idis, secondary intrasaccadic SPs similar to those observed in single sweep recordings from sites close to the eye in normal subjects were also generated (Fig. 1F). Similarly, an increase from i ms through to 4 ms in idi dispersion with a mean idi of 5 ms had only a negligible effect on the amplitude and duration of the SP. When the amplitude of the second and subsequent action potentials in a train was increased progressively from 0% to 100% of the initial action potential amplitude with an idi of 5 -+ 4 ms, there was a 47% reduction in peak-to-peak amplitude and a 20% increase in onset-to-peak amplitude of the SP with no change in SP duration. When the duration of the second (positive) component of the action potential was increased from i ms to 4 ms (with an idi of 5 _+ 4 ms), the SP amplitude was increased by 120% and its duration increased slightly. As actual values for the above motor unit parameters are not available for the human extraocular muscles, it has been necessary to base the model upon estimates from the known or expected properties of the extraocular muscles and by extrapolating from motor unit properties in limb muscles. The firing rate of brainstem saccade burst neurones in the monkey is of the order of 400-600/s 6. The idi was therefore initially set at 2 _+ 1 ms giving a frequency range of 300-1000 Hz. It was found that the choice of values within this range was not critical and that the SP was relatively unaffected by changes in the idi. It is known from electromyographic studies of hu-

man extraocular muscles that motor unit action potentials are of brief duration (1-2 ms) 3. However. it was considered likely that the duration of the surfacerecorded motor unit action potentials would be longer because of the slow propagation velocitv of extraocular muscle fibres, which are of small diameter t~ and because of possible capacitive effects at the recording electrodes and intervening nssues. The Initial negative phase of the surface action potential was therefore set at 1 ms 0.e. less than the mean idi) but a longer positive afterpotential of 4 ms was used. In fact, it was found that the assumption of a longer action potential duration (which should theoretically lead to a greater degree of summation of potentials from different fibres) was not essential, and the SP could still be generated with a reduced duration afterpotential. The introduction of a reduction in amplitude of motor unit action potentials following the initial potential in a train was based upon the premise that, because of the high driving frequency of motor units in the extraocular muscles, the muscle fibres may still be partially refractory on arrival of the second and subsequent impulses in a train. Although it was found that this reduction enhanced the amplitude of the SP. it was not necessary for an SP to be generated. Finally, although there is no information on the recruitment order of motor units in the human extraocular muscles, it would seem reasonable to hypothesise that for a high velocity saccadic eye movement in which the load on the eye muscles (namely the globe) is known and predictable, units should recruit virtually simultaneously, in contrast to the situation in the limb musculature where regardless of the velocity of contraction, units follow the 'size principle" of recruitment orders'7. Such a hypothesis is in keeping with experimental observations in the monkey which have shown highly synchronised high frequency discharge of saccade burst neurones m the brainstem in the immediate presaccadic period f'. The computer model illustrates that a potential comparable to the SP can be generated by the summation of muscle fibre action potentials as a result of the near-synchronous recruitment of motor units in the extraocular muscles and supports our previous hypothesis for the origin of the SP. In addition, the present theoretical considerations are pertinent to the question of the pattern of neural activation of the

380 extraocular muscles in a saccadic eye movement. The

nal Health and Medical Research Council of Austra-

present model may also provide a basis for future at-

lia, the Australian Brain F o u n d a t i o n ( W A Branch)

tempts to model the contraction of the extraocular muscles and other high velocity movements.

and the Sir Charles G a i r d n e r Hospital Research and Special Purposes Fund. Mrs. P. McBryde prepared the manuscript.

The study was supported by grants from the Natio-

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