Quantitative management of contraction in lowest level co-ordination. Hughlings Jackson Lecture. (Given January 29, 1931). By C.S. Sherrington. Brain 1931: 54; 1–28
‘Compact in Hughlings Jackson was a fine vein of pithy thought and phrase.’ Thus, Sherrington introduces the printed version of his Hughlings Jackson lecture, delivered only 2 months before publication (in contrast to the Silliman lectures that took 2 years to see through the press). He reminds us of Jackson's hierarchies—the nervous centres rising in three tiers or levels: ‘no illustrations happier than the notable studies of asynergia, rigidity and tremor’ (in striatal disease) representing a ‘pulling to pieces from the top downwards ... so likewise physiological experiment ... starts lower ... a rump of mechanism, a stump of spinal cord ... these it interrogates through perhaps a single afferent for answer by a single efferent ... its hope is, since bottom is basal, to reach bottom, though even there the elemental may not prove to be the simple’. At that lowest Jacksonian level is the ‘old-fashioned if time honoured entity, the motor centre’.Afferent stimulation shows that every reflex fractionates its responsive muscle, but not right down to the single muscle-fibre. As part of ‘nervous co-ordination’, to paraphrase Hughlings Jackson, the territory of each anterior horn cell selects around 150 muscle fibres from amongst 30–40 000 available within most muscles. These constitute what ‘may be called for short a motor unit’ dividing the (feline) limb muscles into a manageable 200–450 such units. Their ‘all or nothing’ responses yield contraction waves of around 2.5 g but, in reflex activities, those derived from separate motor units overlap to create a maximum tetanic response of up to 30 g in the cat gastrocnemius. Testing tetanic motor units parcels out the share of each reflex for a given muscle, revealing that every afferent nerve contributes reflex activity to practically every muscle within the limb. And, in turn, this distributed anatomy of the muscle fibre dependence on the spinal cord is matched by the richness of descending central terminals on the anterior horn cell, such that the largest motor units are more widely at call and more often in play. Under Faradization of the feline tibialis anterior, the saphenous nerve can tetanize 120 motor units, the popliteal 290 and the dorsal digital nerve 135. But these limits are not anatomically constrained. Rather, they are a temporary limit from within a larger potential pool that may be modified by circumstance. For, besides those motoneurones that the afferent nerve excites, exists ‘a subliminal fringe on which it acts but fails to bring to discharge ... the proof of this is that an excitation similarly subliminal from another source when brought to bear concurrently on this subliminal fringe does bring it to discharge ... (the) explanation of the variation in the number of motor units a given afferent at different time will excite may lie partly in subliminal excitation from some other reflex or central source being in or out of action on some of the motoneurones at the time’.
Conversely, tetanic excitation of two separate afferents may produce supra-maximal excitement within one efferent nerve. Such a response can also be achieved by Faradic stimulation of a single afferent fibre because there is central overlap between that nerve bundle's efferent dependents. From this it follows that, within any pool, are motoneurones in ‘zero, subliminal, maximal and supramaximal’ states of excitation. Sherrington's colleagues and students—ED Adrian with Detlev Bronk (1897–1975: professor of medical physics at the University of Pennsylvania 1929–49, president of Johns Hopkins University 1949–53, and of the Rockefeller University 1953–68), and Derek Denny Brown—have shown that reflex firing within a motor unit can be elicited at variable rates well within the subliminal threshold, especially when this involves an internuncial spinal neurone and not a simple reflex involving a single spinal synaptic pathway. And the repetitive stimulus that produces these subtetanic responses may be accompanied by repetitive after-discharge from a single centripetal volley that, especially in the crossed reflexes, ‘may reach extraordinary proportions’. This apparent semi-independence of the efferent response from its afferent stimulus under moderate Faradic stimulation, resulting from the intrusion of secondary discharges, may seem contradictory. Reconciliation lies in the motor centre being a ‘summation-mechanism’ that reflects the time to reach discharge point, and with some individuality of the refractory phase.
Sherrington does not conceal his admiration for the work of ED Adrian (1889–1977) who has shown that the same impulse-shower characterizes reflex responses to natural stimuli, such as pressure on the foot, as he has shown with electrical excitation of the bared nerve. (The following year, Sherrington and Adrian received the Nobel Prize for Medicine or Physiology.) Here, the centripetal stream—varying in regularity, intensity of stimulus at different sense organs, and periods of crescendo, adaptation and fatigue—‘resemble(s) less a noise than a musical note’. By comparison with Faradic stimulation of the bared nerve, natural stimulation has its impulses less synchronized and in more dissimilar individual trains. This results in richer inequality of excitation of the motoneurone pool, nonetheless proceeding from a functionally related set of receptors, and resulting in still greater diversity between the firing of individual motor units. Now, Sherrington feels ready to characterize in a cartoon (Fig. 1) the interplay of maximal (including supra-maximal), subtetanic and subliminal reflex responses in terms of variable deployment of the subliminal fringe and the entirety of the motor unit pool at their disposal.
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As a stimulus is reduced, the field and density of the exciting central terminals also falls. Contraction, therefore, decreases because the total excited field shrinks (the line
'–ß rises from the abscissa less far to the left); firing slackens throughout as motor units drop through the maximal to the subtetanic, and from the subtetanic into the subliminal ranges; pairs of responsive motor units interfere with each other, waxing and waning until only one continues to fire; occasionally, one unit becomes more excitable as the general trend to sluggishness proceeds but this effect is usually not co-ordinated and fails overall to enhance responsiveness. These features are not to be confused with the demonstration—again made by Adrian and colleagues—that, by comparison with the ‘d’emblée’ opening of direct (but not crossed) Faradic spinal reflexes that tetanize all at once, natural reflexes open slowly, reach a climax and than fade—displaying an overall parabolic stimulus-response shape that reflects the involvement of intermediate neurones in the circuit subserving these responses (Fig. 2). According to the scheme, this represents a natural reflex ... starting somewhere low down in the subtetanic grade and then climbing to take a more settled place in, if the reflex be strong, the maximals ... (the) lineThe terminal phase of the reflex is merely a manifestation of dynamic properties dependent on reduced stimulus intensity, as already described. Thus the gradual onset and recovery of natural reflexes offers a paradigm for the rhythmicity of actions such as breathing and stepping that have as their basis the oscillation of responses in a discrete number of motor units that are repeatedly being stimulated, rather than reflecting additional recruitments.
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Adjustments by subliminals, subtetanics and maximals contribute to fine-tuning of the reflex contraction. ‘The subliminal fringe adjusts ... on the basis of extensity ... it recruits from the quiescent pool; back into that pool it sheds ... (and) ... it also, of course, feeds the supraliminal field’. Therefore, refractory motor units do not respond to a rapidly repeated stimulus whereas those that are subliminally stimulated may now respond to the second volley. These fringes are effective in co-ordinating liaison and combination between the reflexes of synergic muscles. ‘If the head and neck be passively turned into the so-called favourable position, the same limb stimulus evokes(s) a much greater reflex (in the ankle extensor) than before even although the new posture of the head and neck evoked no reflex from the muscle.’ And this situation reverses with return of head and neck posture to the less favourable position, the facilitation being entirely subliminal. So, too, with Rademaker's supporting reaction between the sole of the foot and the soleus reflex, and Bremer's cerebellar influence on reflex extension of the limb—‘(the) inhibitory fringe (giving) Hughlings Jackson's "release" as luminously expounded by Sir Henry Head’.
Rates of firing of the motor unit in the subtetanic range grade contraction by spacing successive waves, so that their integrated tension falls short of the full tetanic—the increment in contraction-tension for a given increase in firing frequency reducing in proportion until it is saturated (that is, ‘occluded’). The subtetanic contraction of any one individual motor unit will wax and wane. If a number of such units fall into step, both with respect to their contractions and proprioceptive pauses, tremor or muscle clonus may ensue. ‘Inherent in the operation of subtetanic motor units is, besides tremor, some waste work, an uneconomy ... can we be sure that nature is in love with economy? In this instance the uneconomy seems more than offset by the advantage gained in delicacy and range of means of grading reflex contraction strength’. Perhaps not, since—when considering maximals—contraction-tension is maintained at a smaller expenditure of energy in a stronger than weaker reflex, added motor units beefing up the response and removals reducing it, and ‘occlusion’ being a prominent feature of strong reflexes. ‘The motor centre is a central instrument which adjusts actively the contraction-strength of its reflexes ... driven and fed by centripetal impulses ... it is, in short, a "summation-mechanism" ... one secret of its coordinative power lies in ... summating with almost negligible time-lag shifting fringes and mobile shades of excitation that ... expand and shrink as afferent channels ... come into or drop out of action’ but showing greater resistance to fatigue and adaptation than the responses of a receptor—as shown by ED Adrian.
Variation in the strength of contraction may shift the scope of a given response and so achieve a qualitative change in the outcome of any reflex. Every stimulus applied to a bared afferent nerve yields a dominant response that may conceal others, and representing a compromise between potentially conflicting reactions. These subtleties are well shown by the extensor reflex of the limb. Here, the animal must integrate stimulation from the labyrinth and anti-gravity effects of weight transferred to that limb—eliciting a ‘standing’ reflex adjuvant to geotropism that varies in its grade depending on postural context, but requiring mild contraction-strength only. This extensor reflex involves the soleus but not the gastrocnemius and, at the knee, the crureus and vasti but not the rectus. With propulsion, as in locomotion, it increases to convert reflex walking and running into a gallop. Thus, the dog—after recovering from the spinal shock of cervical cord section—will ‘gallop’ with all four limbs in response to plantar pressure on one footpad, engaging the pale-muscle motor units of the gastrocnemius and generating a response that is thrice as powerful and rapid as that generated by slow red-muscle motor units of the soleus. These muscles hold in reserve >1000 motor units capable of generating 170 kg (in a 3.5 kg cat) when the rapidly contracting, more powerful and non-economical units are deployed in the reflex gallop. ‘Such dynamic properties have been ably demonstrated by Grace Lady Briscoe’ (1881–1973: née Stagg who married Sir John Briscoe Bt, physician to Kings College Hospital and worked in the Physiological Laboratory of the London School of Medicine for Women). Accompanying every reflex movement like a shadow is posture which punctuates the beginning and end of every action. ‘The simplest spinal reflex, as Hughlings Jackson was wont to insist "thinks" in movements not in muscles.’ The scratch reflex in the spinal cat uses 19 muscles in rhythmic action at 5 beats/s lasting 1/9th s and 17 in steady postural action driven from the hind-limb region of the cord. Stepping is broadly similar although the central rhythm generator—that results in walking, running and galloping as the stimulus increases—has a more sophisticated expression in the cyclical flexion and extension movements of opposite limbs that depend on dorsal and ventral sites for the stepping and standing components, respectively. Both act independently of local centripetal (i.e. afferent proprioceptive) properties of the limb itself; and facilitation is always partially modulated by inhibition.
Sherrington closes with a battle-cry for clinical science and an advertisement for ‘Queen Square’ where, evidently, the lecture was delivered:
I must not detain you longer ... the present offer(s) enhanced promise for neurological investigation ... (but) for effective cooperation clinic and laboratory (must) lie near together ... the laboratory in a word has to be on the spot ... where in all the world could be more fitting a point for such liaison than at the Institution, which, with its noble tradition of teaching and research enshrines within its portal with particular right the bust of the great master ... Hughlings Jackson ... (who) in his writings turns back and forth between muscular co-ordination and mental experience as if for him they were but aspects of a single theme.
Cambridge
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