Charles Sherrington

Yale, 1906

Integration is the whole argument

Charles Scott Sherrington is the scientist who turned tone from a clinical impression into a measurable claim about the nervous system. He delivered the Silliman Lectures at Yale in 1904 and published them in 1906 as The Integrative Action of the Nervous System (Sherrington 1906), and he states his thesis on the second page.

His argument is that nervous reaction is what welds a multicellular animal together and constitutes it, from a mere collection of organs, an animal individual. That is the load bearing sentence of the book and it is the cleanest historical warrant anyone has for treating the nervous system as one regulator rather than a bundle of separate parts.

Comparative, not grandiose

Why the nervous system is the fast one

Sherrington did not claim the nervous system was the body's only integrator, which is exactly why his claim holds. He lists the others in turn: mechanical connection by connective tissue, chemical integration by hormones, citing Bayliss and Starling 1902, and integration by the circulating blood.

What separates nervous integration is speed. It works through living lines of stationary cells despatching waves of physico chemical disturbance, which gives it, in his phrase, relatively high speed. The body has several ways of acting as one. Only one of them is quick enough to run behavior.

Lecture IV

The nervous system functions as a whole

By the fourth lecture Sherrington abandons the isolated reflex as a working fiction and states the whole system principle in six words. He backs it anatomically, noting the system is connected throughout its whole extent, and quotes Donaldson to the effect that a group of nerve cells disconnected from the rest would be without physiological significance. He adds that a reflex detached from the general nervous condition is hardly realizable.

This is worth sitting with. The founder of reflex physiology, the man who made the reflex arc a scientific unit, spent his central lectures warning against treating any part of the system as separable from the rest.

A caution he wrote himself

The simple reflex is an abstraction

Sherrington defined the reflex arc as receptor, conductor and effector, and called it the unit mechanism of the nervous system regarded in its integrative function. Then he immediately refused to let anyone reify it. A simple reflex, he wrote, is probably a purely abstract conception, because all parts of the nervous system are connected together and no part is probably ever capable of reaction without affecting and being affected by other parts. The system, he added, is certainly never absolutely at rest.

He was not a mechanist who thought the body was a switchboard of independent circuits. He said the opposite, in print, in the book that made his name.

The final common path

Everything competes for the same outlet

Sherrington's most durable structural idea is the final common path. Each sensory neuron is a private path serving one receptive point. The motor neuron at the end of the chain is a public path, receiving impulses from many sources across the body, and he named that terminal link the final common path, noting that the motor nerve to a muscle is a collection of them.

The consequence is unavoidable. Every influence in the body that is going to reach a muscle has to arrive through the same limited outlet and compete there. Nothing reaches a muscle in isolation, because there is no isolated route for it to take.

The funnel

Built for convergence

Sherrington quantified the convergence and the numbers make the architecture obvious. Citing Donaldson's counts, he notes that afferent fibers entering the human spinal cord outnumber the efferent fibers leaving it by roughly three to one, and by about five to one once the cranial and optic nerves are included.

He describes the receptor system as bearing to the efferent paths the relation of the wide ingress of a funnel to its narrow egress. The nervous system is built to compress an enormous sensory inflow into a small motor output. It is a machine for deciding, and the deciding is continuous.

1906, and the word

He named the third sensory world

Sherrington divided the body's receptors into three fields and gave two of them names that had not existed before. The surface field open to the environment he called extero ceptive. The visceral field he called intero ceptive. And the field whose receptors lie in the depth of the organism, in muscles, tendons, joints and blood vessels, stimulated by the organism's own activity, he called the proprio ceptive field.

That third category is the one this practice is built on. Proprioception is the body's continuous report on its own position and tension, and Sherrington is the reason we have a word for it.

1894

Muscle is a sense organ

The anatomy under all of it came first. In 1894, in the Journal of Physiology, Sherrington showed that the nerves to skeletal muscles carry large numbers of afferent, that is sensory, fibers (Sherrington 1894). He described pure spindle nerves of large spinal ganglion fibers supplying the muscle spindles, and introduced the terms intrafusal and extrafusal to separate the fibers inside the spindle from ordinary muscle fibers.

Muscle is not merely something the nervous system commands. It is something the nervous system is constantly listening to. A muscle reports its own length and tension back to the cord, without pause, for a lifetime.

The 1898 paper

Reflex tone was on the record by 1898

Sherrington put the physiology of exaggerated tone on the record in 1898, in a Journal of Physiology paper titled Decerebrate rigidity, and reflex coordination of movements, volume 22, pages 319 to 332 (Sherrington 1898). The paper established the decerebrate preparation, the sustained extensor rigidity that grips neck, jaw, elbow, knee, shoulder and hip, and gave the laboratory a form of tone steady enough to interrogate.

Muscle tone has been standard physiological vocabulary since that work. The Silliman Lectures came eight years later and drew the meaning out of the rigidity: a contraction this extreme, held this long, is still a state the nervous system is actively producing. The decisive demonstration was one cut away.

The decisive experiment

Tone is something the system is doing

Sherrington proved that muscle tone is reflex, not a property stored in the muscle, and the proof is clean enough to state in a sentence. His decerebrate preparation produced sustained extensor rigidity across neck, jaw, elbow, knee, shoulder and hip (Sherrington 1898). Cutting the afferent, sensory, roots of a single limb made that limb fall flaccid at once, even at the height of the rigidity, and the effect was strictly local to the limb whose roots were cut.

Cut the incoming information and the tone collapses. That is the whole demonstration. Tone is not stiffness sitting in tissue. It is a state the nervous system is actively holding, moment to moment, on the sensory information arriving from the body itself. Everything this practice calls tone follows from that finding.

Page 231

A background of active equilibrium

Sherrington gave tone its most useful description in a single phrase, and it is worth quoting exactly because it is doing precise work. He observed that the tonic reflexes of posture sit at the bottom of the potency scale, so that even weak noxious stimulation at the foot can lower or abolish the knee jerk or the extensor tonus of elbow or knee. He treated that as an advantage rather than a flaw, because a postural background should be easy to override if the animal is going to respond quickly.

He also noted that tonic postural reflexes can persist hour after hour with little or no sign of fatigue, while the intercurrent reflexes that interrupt them fatigue early. A background that never tires, and yields instantly when something matters more. That is a good description of a well regulated nervous system, written in 1906.

New York, 1919

He wrote the history of the word tone himself

Sherrington cared enough about the word to write its biography. In 1919 he contributed Note on the History of the Word Tonus as a Physiological Term to the tribute volume for Sir William Osler, published in New York by Paul B. Hoeber, pages 261 to 268, the byline reading C. S. Sherrington, Oxford (Sherrington 1919).

Eight pages on the lineage of one term is a telling act. The man who proved what tone is also documented what tonus had been called and by whom, treating the word as an inheritance whose record was worth keeping straight. Modern physiology's account of tone begins with him because he took custody of the term twice: once in the laboratory, and once in the library.

The inheritance

What he handed forward

Sherrington's laboratory is one of the great teaching lines in medicine. John Eccles, Ragnar Granit and Howard Florey all trained under him and all won Nobel Prizes of their own. Wilder Penfield, who mapped the human cortex in awake patients, studied with him at Oxford. Harvey Cushing, the founder of modern neurosurgery, worked in his Liverpool laboratory in 1901. He shared the 1932 Nobel Prize with Edgar Adrian for discoveries regarding the functions of neurons (Nobel Prize 1932), was knighted in 1922, and served as President of the Royal Society.

After retiring from Oxford in 1936 he gave the Gifford Lectures at Edinburgh, published in 1940 as Man on His Nature (Sherrington 1940), where he wrote the most quoted sentence in neuroscience. He remained careful to the end about what physiology may claim, noting that as followers of natural science we know nothing of any relation between thoughts and the brain except as a gross correlation in time and space.

First in the lineage

Regulation science spent a century extending his argument

Sherrington heads the lineage of regulation science, with one predecessor. Claude Bernard had established before him that the body defends the constancy of its own internal environment. After 1906 the argument grew in his direction. Walter Cannon named that defense homeostasis. Hans Selye showed that sustained defense carries a cost the body eventually pays. Norbert Wiener gave regulation its formal grammar of feedback. Ilya Prigogine showed how open systems held far from equilibrium generate order rather than lose it. Yoshiki Kuramoto supplied the mathematics by which independent rhythms lock into a common one.

Each answered a different question: what holds the readings steady, what defending them costs, how the loop is wired, why order arises at all, how separate rhythms agree. Sherrington's question sits underneath every one of them. What makes many parts answer as one body? Integration is the largest claim in the set, and the physiology of regulation has been circling it since 1906.

Sherrington and the model

The Unified Model of Tone begins where Sherrington began

The Unified Model of Tone names Sherrington first in its lineage: he brought tone into modern physiology, in the same work that named integration as the nervous system's defining task. Both halves of that sentence carry weight. Tone gave the model its variable. Integration gave it its architecture.

The model keeps his definition of tone and widens the aperture. Physiology gave tone to the muscle as its standing readiness to respond. The early clinical literature gave it to the nerve as a normal degree of tension, whose every variation marked the beginning of disease. The model holds that readiness and tension are what tone looks like when a single instrument is pointed at a single tissue. Read across every tissue at once, they are one integrated state.

His whole-system claim returns with a correction attached. The nervous system is often called the body's master regulator, and the model refuses the phrase, because regulation is distributed: cells register their own conditions, tissues integrate many cells, organs regulate their internal relationships. What distinguishes the nervous system is concentration. It is the body's most concentrated system for integrating, modeling, prioritizing and redistributing what every tissue is already registering, the highest-density integrator of a distributed regulatory whole. That is Sherrington's 1906 claim restated with a century of cell biology underneath it.

The final common path scales the same way. Sherrington named the motor neuron the final common path because every influence bound for a muscle competes at one limited outlet. The model finds the identical funnel a level up, in Eduardo Benarroch's Central Autonomic Network (Benarroch 1993), the distributed brain circuit that sets autonomic state. There, tone is set by the whole network, with the brainstem as the final common pathway. Emotional state, cognitive load and postural input all move heart rate and blood pressure because they converge there.

Say plainly where the record ends and the model begins. Sherrington established that tone is reflex, that muscle is a sense organ, and that integration is what a nervous system is for. He wrote nothing about muscle tone, vascular tone, autonomic tone and cortical tone as one regulatory system read at different sites, and he is not enlisted as endorsing that claim. The unification is staked on predictions that can fail, and it belongs to the model alone. The unification is the model's. The integration is his.

What the record shows

The physiology of tone in seven dated findings

• 1894. Sherrington showed in the Journal of Physiology that the nerves to skeletal muscles carry large numbers of sensory fibers serving the muscle spindles, and coined intrafusal and extrafusal (Sherrington 1894). Muscle reports its own length and tension without pause.
• 1897. He introduced the word synapse, first in print in the chapter he wrote for Michael Foster's Textbook of Physiology (Foster and Sherrington 1897). The Cambridge classicist Arthur Verrall supplied the Greek at his request.
• 1898. Decerebrate rigidity, and reflex coordination of movements, Journal of Physiology volume 22, pages 319 to 332 (Sherrington 1898), established the preparation that made exaggerated tone a laboratory object.
• 1906. The Integrative Action of the Nervous System, from the 1904 Silliman Lectures at Yale (Sherrington 1906), named the proprioceptive field and argued that nervous reaction welds a collection of organs into an animal individual.
• 3 to 1. Citing Donaldson's counts, Sherrington noted that afferent fibers entering the human spinal cord outnumber efferent fibers by roughly three to one, and by about five to one once the cranial and optic nerves are included (Sherrington 1906). The nervous system is a funnel built for convergence.
• 1919. His essay Note on the History of the Word Tonus as a Physiological Term appeared in the Osler tribute volume, pages 261 to 268 (Sherrington 1919). He wrote the history of the word himself.
• 1932. The Nobel Prize in Physiology or Medicine, shared with Edgar Adrian, for discoveries regarding the functions of neurons (Nobel Prize 1932).