What is a reflex? Part 1

Some ideas from Moshe, Magnus and Sherrington

 

Sir Charles Sherrington’s 1906 work, The Integrative Action of the Nervous System, is regarded as the founding text of modern neuroscience and is largely devoted to the working of the innate reflex systems of the vertebrate animal. Within that framework, Sherrington’s contemporary, and protégé, Rudolph Magnus, an almost certain Nobel prize-winner were it not for his sudden early death, devoted his research talents to elucidating the postural reflexes. The best part of a century later, their neurological discoveries and insights retain most of their freshness and relevance. Moshe cited Sherrington and Magnus extensively in Body and Mature Behavior and was quite proud of his ability to take this primary research and turn it into something concrete and useful for everyone (Amherst lecture).

The work of these and other early neuroscientists looked at the overall patterns of neuromuscular functioning in vertebrates. The postural reflexes are not solely concerned with the way we sit and stand. When these reflexes are allowed to do their job properly, they automatically bring about a smooth and harmonious integration of the different parts of the body in all its activities. When they are prevented from working as they should, the functioning of the whole musculature deteriorates, leading to localized joint and muscle problems as well as damaging effects on our physical and psychological health and well-being.

Even among scientists, the term reflex is used in a variety of ways. But if care is taken to be clear about what is meant by it, the term reflex can fill a need. For the purpose of our study of the FM, We can look at how Sherrington’s definition is adopted by Moshe and woven through his method. In the introduction to the 1947 re-publication of The Integrative Action of the Nervous System Sherrington wrote:

The behaviour of the spider is reported to be entirely reflex; but reflex action, judging by what we can sample of it, would go little way toward meeting the life of external relation of a horse or cat or dog, still less of ourselves. As life develops it would seem that in the field of external relation “conscious” behaviour tends to replace reflex, and conscious acts to bulk larger and larger. Along with this change, and indeed as part of it, would seem an increased role for “habit”. Habit arises always in conscious action; reflex behaviour never arises in conscious action. Habit is always acquired behaviour, reflex behaviour is always inherent and innately given. Habit is not to be confounded with reflex action.

Berta Bobath, whose well-known text on Abnormal Postural Reflex Activity describes her pioneering approach to the treatment of cerebral palsy and other neurologically based muscular disorders, also had doubts about the use of the term reflex. She suggested it would be more useful to refer to “postural reactions” or “responses” but settled for Sherrington’s definition. In the third edition of her text, published in 1985, she says:

In keeping with the publications available to us in 1965 and 1971, we used the term ‘reflexes’ rather loosely. However, we now accept Sherrington’s view that a reflex is a stereotyped response, always recurring in the same unchanging manner…

As Sherrington defined it, much of what commonly passes for reflex action is, in fact, learned behavior. Certain actions become learned so thoroughly that they are carried out without conscious thought. It is easy to recognize this in the “mindless” routines of household or work tasks; but it is also true of the way athletes perform in their sports.

Despite the common journalistic description of various rapid sporting responses as reflex, no one is born with the ability to return a high-speed tennis serve or respond to a starter’s gun in one-hundredth of a second; these are learned skills. Pavlov’s so-called “conditioned reflex” is another example of learned behavior. So also are the distinctive ways in which each one of us walks, sits, breathes, talks and carries out the countless actions of daily life. All these activities carry the imprint of learned experience.

In the context of our study of the FM, Sherrington’s distinction is important because it draws a line between activities that can be learned and those which are evoked from the innate capacities of the neuromuscular system. This is not a differentiation between types of muscle behavior – whether reflex or voluntary, muscle contractions are essentially the same – but of whether they are controlled from the cortex or subcortically.

In addition to recognizing the importance of the distinction between learned and reflex, it is also important to note that there are linkages between our consciously-willed actions and the underlying patterns of reflex and learned behavior. In a striking passage in his last book, Sherrington says:

It is largely the reflex element in the willed movement or posture which, by reason of its unconscious character, defeats our attempts to know the “how” of the doing of even a willed act…Of the proprioceptive reflexes as such, whether of muscles or ear (vestibule) we are unconscious. We have no direct experience of the ‘wash’ of the labyrinthine fluid or, indeed, of the existence of the labyrinths at all…

In this passage, Sherrington is pointing out that even our simplest voluntary actions are supported on a dynamic infrastructure of innate reflex muscle activity. Whenever we do something deliberately, we unconsciously bring into play a huge number of reflex responses, varying from subtle balancing adjustments in the tone, or tension, in the muscles in various parts of the body – these are referred to as “tonic reflexes” – through to the quick and often effortful movements of limbs that take place. For example, when we towel ourselves vigorously after a shower or make a dash for a bus. The important point is that whatever deliberate action we perform and no matter how we concentrate on it, the details of the associated supporting and compensatory muscular contractions and releases happen reflexly, independently of any conscious input from the brain.

It is thus paradoxical that although we readily take responsibility for our conscious acts we do not know exactly how we manage to do them. More interestingly, it is the superstructure of consciousness which enables humans – unlike horses, dogs, and still less spiders – to acquire habits that distort and interfere with the working of their reflexes and undermine the functioning of their own selves. The way in which human learned behavior interacts, often detrimentally, with the relationship between the deliberate and the reflex is a theme which we have been exploring in this past segment through ATM and FI explorations.

It is also worth making clear that Sherrington had no sympathy with the reductionist view that all activity is reflex, simply the result of automatic neurological responses to external or internal stimuli. Although the reflexes provide the essential underpinning for all the body’s activities, for Sherrington the volitional decision-making mind occupies the primary role in human behavior.

The word posture is also used in widely different ways. Many of its meanings are associated with deliberately assumed ways of holding the body. Walking about, stiffly balancing a book on the head, used to be a common way of training young people in what was supposed to be good posture. For this discussion the word posture refers to the natural, or innate, relationship of the parts of the body to each other in sitting, standing or walking; it is perhaps best approximated by the old-fashioned word “carriage” (as in moshe’s “carriage of the head”) or his term “acture” (action +posture).

The question of posture, at first sight, seems an unlikely focal point for some of the major advances in neuroscience made in the early decades of the from an early date Sherrington had seen how the maintenance of posture was just as complex and demanding of the nervous system as movement. As he said:

...much of the reflex reaction expressed by the skeletal musculature is postural. The bony and other levers of the body are maintained in certain attitudes both in regard to the horizon, to the vertical, and to one another...Innervation and co-ordination are as fully demanded for the maintenance of a posture as for the execution of a movement. 12 Far from representing a fixed and rigid configuration of the muscles, posture displays them in action in patterns as dynamic, if not so immediately evident as those of movement.

This is the problem Magnus set out to define in his research: Posture is in constant flux. The flow of nerve impulses from the nervous system to the muscles is continually changing in response to the sensory inputs from the external world as well as those from the various feedback systems within the body itself. Magnus set himself the task of identifying the separate functions of the different interacting systems involved in this. He was particularly interested in clarifying the role of the postural reflex systems and distinguishing their activity from that deriving from voluntary or learned patterns of behavior.

Here is a synopsis of his basic findings:

The Vestibular Apparatus

The balance, or equilibrium, of the body is intimately related to posture. The term static equilibrium is often used to refer to when the body is retaining its position relative to the force of gravity. The body must also be able to retain its balance when its parts are moved relative to each other and when the whole body is in motion; this is usually referred to as dynamic equilibrium. Both of these aspects of balance are largely controlled by the vestibular apparatus.

Since the vestibular apparatus was the subject of many of Magnus’ experiments, it is worth outlining briefly what is involved. The inner ear houses a maze of winding passages, collectively called the labyrinth. The labyrinth is divided into three areas, the vestibule and, projecting above and backwards from it, the three curved ducts known as the semicircular canals; and the cochlea which contains the hearing receptors. Within the vestibule are two sacs, the utricle and saccule, known as the otolith organs. The utricle and the saccule, together with the semicircular canals, are known as the organs for equilibrium and make up the vestibular apparatus. The otolith organs provide information on the tilt of the head. The walls of both the saccule and the utricle contain a small thickened area called the macula. Each of the two maculae, which are set at right angles to each other, supports a set of tiny hair cells. The hair cells are bathed in a gelatinous layer called the otolithic membrane in which is embedded a layer of dense calcium carbonate crystals called otoliths – otolith literally means “ear-stone”.

When the head is in its normal position with the gaze horizontal, the hair cells in the utricle are positioned horizontally and those in the saccule are positioned vertically. When the head is then tilted forward, backward or sideways, the otolithic membrane lags slightly behind the movement of the head. This causes the hair cells to bend, resulting in the transmission of impulses through the utricular and saccular nerves to the vestibular branch of the vestibulocochlear nerve. The otolith organs, in this way, act as a three-dimensional system, a complex type of spirit level, for monitoring the tilt of the head from moment to moment.

The three semicircular canals provide information on movements of the head. They are set at right angles to each other in three planes and consist of ducts filled with a fluid called endolymph. One end of each canal has a small expanded or dilated area called the ampulla. In each ampulla, there is a ridge or swelling upwards from the base of the canal called the crista. On top of the crista, a group of hair cells projects upwards and is covered by a small mass of gelatinous material called the cupula. When the head moves, the movement of the cupula, because of its inertia, is delayed slightly compared to that of the head. This drags the hair cells on the crista out of their resting position, causing them to generate nerve impulses. Smooth movement is insufficient to stimulate the semicircular canals; there must be a change in the rate of movement, either acceleration or deceleration. These nerve impulses are collected in the ampullary nerves and are also fed into the vestibular branch of the vestibulocochlear nerve.

Reflex standing

If an animal is to stand normally, the muscles used in standing must be able to maintain the necessary tone. Magnus found that spinal animals, those in which the whole brain had been extirpated, were capable of complex movements when they were suspended in an upright position. They were, for example, able to make running and walking movements when the pads of their feet were stimulated, showing that these actions are controlled in the spinal cord. But these animals collapsed if they were placed in a standing position. Magnus remarks:

The centres of the spinal cord can indeed cause and regulate very complicated combinations of movements, but they are unable to give the muscles that steady and enduring tone which is necessary for simple standing.

When more of the brain was left in place by making the cut further up the brainstem, somewhere between the medulla oblongata and the foremost part of the midbrain, the animal was able to stand. But it did so in a state of what is called decerebrate rigidity. The antigravity muscles, the extensors of the limbs, the extensors of the back, the elevators of the neck and tail, and the closing muscles of the jaws, had abnormally high tone, whereas their antagonists, the flexors, had virtually none. The overall result was that, although the animal could stand if it were placed on its feet, the distribution of tone was abnormal and the animal’s posture was stiff and distorted.17

Magnus makes the additional comment:

The stimuli inducing the enduring tone of the standing muscles in decerebrate rigidity arise from different sources, the proprioceptive sense organs in the contracted muscles themselves playing the most prominent role.

He is pointing out here that excessive muscle tone, once it has developed, has a tendency to become self-sustaining. This is because when there is excess tension in the muscles their own internal sensing organs, their proprioceptors, are stimulated to produce signals to the nervous system which result in that state being maintained.

Normal distribution of tone

In normal standing, the extensor and flexor muscles have the level of tone required to keep them in balance with each other. Magnus found that this occurred when the cut in the brain was made at such a level that the thalamus was included, producing what the researchers called a mid-brain animal or a thalamus animal. In these creatures, he found that both the distribution of muscle tone and the standing posture were more or less normal.

He says:

In the thalamus animal the extensors of the limbs just have sufficient tension to balance the weight of the body against gravity, so that every force tending to raise or lower the body can easily move it in one or the other direction.

This was a persuasive experimental demonstration that in the case of these animals normal standing, including gentle movement around the equilibrium position, even though it involves complex interactions throughout the whole skeletal muscle system, was working as a wholly reflex activity and was able to take place in the absence of the cerebral cortex.

Attitude

Magnus uses the term attitude to refer to how the parts of the body relate positionally to each other. The attitudinal reflexes come into action when the position or the tone in one part changes in relation to the rest of the body. An example of this is when a part of the body is braced or stiffened. As this happens, the attitudinal reflexes bring about compensatory changes in the rest of the body so that the muscular system remains in an overall state of balanced tone.

Magnus remarks:

It is noteworthy that these reflexes are most easily evoked from the foremost part of the body, from the head, in which the teleceptive sense organs are situated, so that distance stimuli influencing the position of the head can in this way also impress different attitudes upon the whole body. One can, in fact, in the decerebrate animal, by simply changing the position of the head, give to the body a great number of attitudes, resembling closely the normal harmonious attitudes of the intact animal.

By the teleceptive sense organs, Magnus means those sense organs which detect objects at a distance, as opposed to the proprioceptors which detect changes inside the body. The eyes are the most important teleceptors in humans and many other animals; but hearing and the sense of smell are equally or more important in others. He is pointing out that when these teleceptive organs detect an object it tends to evoke changes in the position of the head; we look towards the object the eyes have detected or seek the source of the smell. The change in the position of the head, through the medium of the vestibular system and the neck proprioceptors, brings about reflex changes in the muscles in the rest of the body.

As Magnus describes it:

It is possible, by giving to the head different positions, to change the distribution of tone in the whole body musculature... The most striking reactions appear in the extensors of the limbs and in the neck muscles. The effects observed are the result of combined reflexes from the labyrinths and from proprioceptive neck receptors, and ... in this way, it is possible to impress upon the whole body different adapted attitudes by changing only the position of the head.

As an example of the attitudinal reflexes at work in an intact animal, Magnus instances a cat standing in the middle of a room. A mouse runs along the foot of one wall, attracting the cat’s attention. The simple act of turning its head to watch the mouse evokes a series of attitudinal reflexes which automatically put the cat into a posture of readiness, with the weight on three paws, and the other slightly lifted and ready to move. The result is that if a signal to pounce were to come from its cortex, the cat is perfectly poised for action.

Magnus’ description of what is taking place here is a model of meticulous observation and analysis:

The distribution of excitability in the motor centres of the spinal cord is rearranged by the turning of the neck, so that, if for some reason running movements begin, the limb which has no static function will always make the first step. In this way, the moving mouse impresses on the cat, through the mediation of tonic neck reflexes an attitude, by which the cat is focussed towards the mouse and made ready for movement. The only thing the cat has to do is to decide: to jump or not to jump; all other things have been prepared beforehand reflexly under the influence of the mouse, which will be the object of the resulting jump.

Even when the eyes are not involved, the attitudinal reflexes can be evoked by simply moving the head. Magnus was able to demonstrate this by working with decerebrate animals in which any influence of the eyes is negated by the absence of the visual cortex. He found that by altering the position of the head the distribution of tension or tone (often referred to as tonus in older texts) was changed through the entire musculature. These experiments also showed that the distribution of tone remained constant as long as the position of the head remained the same.

He says:

The changed distribution of tonus in the extensor muscles of the limbs continues as long as the head retains its specific relation to the trunk, making way for another distribution of tension immediately upon alteration of the position of the head with respect to the trunk. It has been found that for most changes of the relation of the head to the body either the extremities on the right and left side, or of the fore and hind limbs react in an opposite way.

The point in the above quotation about limbs on the right and left sides reacting in an opposite way refers to what Sherrington called the crossed reflex which he examined in considerable detail. Sherrington found that many of the leg reflexes in animals evoked a contrary reflex in the opposite sense and in the opposite leg. If reflex extension is induced in left hind leg, for example, it tends to stimulate a flexion reflex in the right foreleg; such a pattern of reflexes is evident, for example, in walking. Magnus was pointing out that simply turning the head to one side tends to produce a similar crossed-reflex pattern. He also makes the point that the attitudinal reflexes can maintain a particular attitude for a very long time without the muscles becoming tired.

He says:

These reflexes are called tonic, because they last as long as the head keeps a certain position; and that not only for minutes and hours, but for days, months and even years...We are accustomed to believe that muscular action is liable to fatigue, and this, of course, is true for movements, and especially for movements performed against resistance. But muscular action concerned in keeping some part of the body in constant and unchanging position gives rise to much less fatigue, and the attitudinal tonic reflexes evoked from the head appear to be practically indefatigable.

The fact that these attitudinal tonic reflexes can last for years is indeed remarkable. Magnus’ observations prefigure the findings by later scientists that it is the non-fatigable red fibers in muscles that are primarily involved in posture.

The righting reflexes

The righting reflexes restore an animal to its normal posture if it is displaced from this by its own actions or by an external force. These reflexes, unlike the tonic attitudinal reflexes, can bring about major movements of the body. The two types of reflex, however, tend to shade seamlessly into each other and in the normal intact animal there is no clear demarcation between them. As Sherrington said:

Naturally, the distinction between reflexes of attitude and reflexes of movement is not in all cases sharp and abrupt. Between a short lasting attitude and a slowly progressing movement the difference is hardly more than one of degree.

Magnus remarks that the righting reflexes are best studied in an animal in which the cut in the brain has been made at a level which leaves the thalamus in place. In this case, Magnus says:

Not only is the distribution of tone a normal one, but also the righting function is fully developed, and the animal is able, from all abnormal positions, to come back reflexively into the normal position. The reflexes which co-operate in attaining this result are the “righting reflexes.” They can best be studied in the mid-brain or thalamus animal, in which the fore-brain has been removed, so that no voluntary corrections of abnormal sensations are possible.

When a thalamus animal is lifted by the body and held in space with the head and neck free, the head retains its position no matter how the rest of the body is moved about. As Magnus observes “Whatever situation one gives to the hind part of the body, the head is kept, as by a magic force, in its normal position in space.” He describes these reflexes which bring about the automatic preservation of the normal orientation of the head as the “head righting reflexes”.

In other experiments of this kind, however, Magnus found that if the labyrinths are extirpated, the head shows no tendency to hold its position when the body is moved. In this case, the position and orientation of the head are determined by what is happening in the rest of the body. Without the labyrinths, in other words, the nervous system is deprived of an absolute measure of the relationship of the head to the horizontal or vertical. In everyday human life a hint of this may be experienced as the feeling of impaired balance that sometimes accompanies an inner ear infection; the reason is that the infection has interfered with the working of the labyrinths and their role in detecting changes in the position and orientation of the head.

If the head is displaced from its normal position and the labyrinths are in place, the head righting reflexes bring about a cascade of further reflexes through the body. Magnus demonstrated this using a decerebrate animal lying on its side. When the head is lifted and turned to face forward, a twist is induced in the neck. As a result, the proprioceptive sense organs in the muscles, tendons and joints of the neck are stimulated; this activates the reflexes which bring the thorax back into the normal relationship with the head, thereby untwisting the neck. This, in turn, leaves the lumbar area twisted relative to the thorax, which brings further reflexes into action, causing the lower body to untwist itself, so that the whole body is now brought into its normal position.

This is a simplified description of what happens in practice since the tactile sensors in the skin are also stimulated by the contact with the floor and provide further input to the various reflex systems. In the intact animal, there is also input from the eyes. Magnus fully recognizes this and points out that there is a considerable degree of redundancy, or duplication, in the way the righting reflexes are stimulated and carry out their tasks, saying: The integrity of every single factor of this complicated function is doubly ensured. The head is righted by labyrinthine, tactile, and optical stimuli; the body by proprioceptive and tactile stimuli. The tactile stimuli act separately upon the body and upon the head. The orientation of the head and of the body takes place in relation to gravity, sustaining surface (ground etc), distant environment (optical), and to the different parts of the body – a very complex combination of reflexes. It is indeed an interesting task to watch the cooperation and interference of these reflexes during the movements of various animals in their ordinary life.

The ability to twist the body into the appropriate position and get up from the ground is obviously of critical importance to the survival of any animal and this is why it is “doubly ensured” by the reflex system. But among the various systems involved it is particularly notable how changes in the position of the head relative to the rest of the body, through the mediation of the neck, have major effects throughout the whole of the body’s musculature.

The optical righting reflexes

A further set of reflexes explored by Magnus are known as the optical righting reflexes; these are triggered by movements of the eyes in their sockets. Since the visual centers in the cortex are involved in the processing of nerve impulses coming from the retina of the eye, these reflexes are only found when the cerebral cortex is present. The way in which movements of the eyes can influence the whole functioning of the body was a subject which interested Sherrington greatly. He had written at length about it in The Integrative action of the nervous system, well before Magnus began his research into the postural reflexes. Sherrington remarked on how the movements of the eyes have a ...tendency to work or control the musculature of the animal as a whole – as a single machine – to impel locomotion or to cut it short by the assumption of some total posture, some attitude which involves steady posture not of one limb or one appendage alone, but of all, so as to maintain an attitude of the body as a whole.

An obvious example of this is the cat watching the mouse described above by Magnus. If we pay close attention to what is happening in ourselves as the direction of our gaze shifts, we can also notice the way our body gradually adapts to the direction of the gaze, most evidently when we are following an object with close attention – when bird-watching for example – but also in the way minute changes occur in the muscles throughout the body as the gaze flickers about in normal activity.

Discussing the same question of the way the eyes influence the rest of the body, Magnus said:

...if the attention of the animal is attracted by something in its environment, and it therefore fixes the latter with its eyes, the head is immediately brought to the normal position and kept so as long as the optical attention is focussed on the object. So a teleceptor has gained influence upon the righting apparatus. This is the only righting reflex having its centre not in the brainstem but higher up in the cortex cerebri.

He goes on to describe what happens when food is held in front of an animal and lowered so that the animal bends its head downwards towards the belly, in the ventral direction, or lifted so that animal moves its head backwards, in the dorsal direction. This is an everyday sequence of actions to which the great majority of people would give little thought. But to Magnus it was a matter of major significance which showed that by means of

...stimuli transferred to the animal by the distance receptors (eye, ear, nose), it is possible to impress upon the body of the animal different attitudes from distant points of the environment. A cat which sees some food lying on the ground flexes the head in the ventral direction and this causes the fore-limbs to relax so that the snout is moved towards the food; but if a piece of meat be held high in the air the optic stimulus causes dorsiflexion of the head. This evokes strong extension of the fore-limbs without marked extension of the hind-limbs. The body of the animal is not only focused on the meat, but is also brought into a position which is optimum for the springing reflex, so that by a strong sudden simultaneous extension of the hind-limbs the animal can reach the meat.

It is evident that a great deal of neurological and muscular activity is involved in such simple actions. Taking just the eyes, the position of each in its socket is determined by the action of six extraocular or extrinsic muscles. These provide the eye with a high degree of mobility enabling it to rotate up, down or sideways. They must also work in a meticulously coordinated way to ensure that the binocular vision they enjoy when they are in their resting position, centralized in their sockets and looking straight ahead, is maintained as the eyes swivel from object to object. Added to that, the eyes must be able to maintain this level of coordinated control as the head itself moves about. Magnus describes the system which controls this as an “...extremely well- adjusted central apparatus which governs the positions of the eyes.”

Characteristically, he was intent on disentangling the various systems involved in the workings of this central apparatus. He carried out a long series of experiments by means of which he was able to separate the different and complementary responses to eye movements evoked by the vestibular system and by the neck proprioceptors. From this work he was able to conclude that when

...the animal brings its head into a new position, it makes a movement, and, in doing this stimulates the ampullae of the semicircular canals, which gives rise to short-lasting motor reflexes acting on the eye muscles. ...The canals begin, the otoliths and neck receptors complete and steady the reaction: a very finely adapted mechanism indeed.

Magnus’ research sheds light on the complexity of the interactions between the eyes and the muscles involved in posture. A simple impression of some of the factors involved can be obtained by standing quietly and observing how much easier it is to stay in balance when the eyes are open than when they are kept closed.

A central nervous apparatus

At the conclusion of some fifteen years of intensive laboratory research, Magnus and his team had experimented and reasoned their way from the top of the spinal cord upwards through the brainstem and midbrain. He could confidently say they had identified the locations and functions of the main neural centers controlling the postural reflexes. Magnus summarized their findings as follows:

...the principal results of the study are that the centers for the body posture and the labyrinth reflexes are arranged in three great functional groups in the brain stem.
1. From the entrance of the vestibular nerve backward to the upper cervical cord; the centers for the labyrinth and neck reflexes on the whole body musculature with the exception of the righting reflexes.
2. Between the entrance of the eighth nerve and the eye muscle nuclei; the centers for the labyrinth reflexes on the eyes.
3. In the midbrain: the centers for the righting reflexes...

This region of the brain from the top of the spinal cord up to, and including, the midbrain is not just concerned with posture; it is densely packed with other functions. Here, for example, are found the centers for the twelve cranial nerves which control the visual, auditory and gustatory systems, as well as the detailed functioning of the eyelids, lips, forehead and general facial muscles. It is sometimes known as the reptilian brain. It is here, rather than in the cortex, that the control centers for the various aspects of posture investigated by Magnus are located.

The segmental nature of the nervous system was well-investigated long before Magnus began his work. Scientists knew that each segment of the vertebrate neuromuscular system was controlled by the nerves entering and leaving the spinal cord through the gap between the vertebrae at the level of the segment. Sherrington’s puzzle, to which he had devoted The integrative action of the nervous system was how the neuromuscular system managed to ensure that this assembly of segments was able to act in a coordinated way. Posture, requiring the coordination of a continuing flood of instructions to more or less the whole of the musculature in response to the multitudinous inputs from the proprioceptors and the exteroceptors, those organs sensing the external world, was an extreme example.

This is how Magnus put it in the Croonian Lecture in 1925:

The lower centres for the muscles of the different parts of the body are arranged segmentally in the spinal cord; the higher centres in the brainstem put them into combined action and in this way govern the posture of the animal as a whole. We have here a very good example of what Sherrington has called the “integrative action of the nervous system”. And integration is particularly necessary in the case of posture, because nervous excitations arising from different sense organs are flowing towards the postural centres in the brain-stem, and must be combined so that a harmonising effect will result.

In Body Posture he summarizes his conclusions:

The result of the present study is that in the brain stem, from the upper cervical cord to the midbrain, lies a complicated central nervous apparatus that governs the entire body posture in a coordinated manner. It unites the musculature of the whole body in a common performance...

But although he was happy that he had identified this area of the lower brain as the location of the key nerve centers necessary for the normal functioning of the postural reflexes, he saw this conclusion as the starting point for further investigation. As he said:

...at least a beginning has been made with the anatomic-physiologic disentangling of the central apparatus for the body posture. Apart from establishing the general arrangements of centers and pathways in various parts of the brain stem, it has been possible to ascertain the function (or a part of the function) of at least one anatomically known nucleus, and to determine the anatomic position of the centers for a few physiologic functions.

Magus’ enduring legacy is the comprehensive and unified understanding he was able to develop of what is involved in animal posture. It is noteworthy how well his work has endured and the extent to which it has become the commonplace of neuroscience. A modern textbook on the central nervous system, for example, nowhere refers to Magnus by name but describes the postural reflexes and their role as follows:

The tasks of these reflexes are to maintain an appropriate posture of the body, to help regain equilibrium when it has been disturbed, and to ensure the optimal starting positions for the execution of specific movements. Postural reflexes produce the automatic movements that help us regain equilibrium quickly, for example, when slipping on ice. It is a common experience that these compensatory movements happen so rapidly that only afterwards are we aware of the movements we performed.

Magnus pointed out that the postural reflexes have another critically important role, that of constantly recalibrating the senses. This is necessary because, in the course of any particular phasic action, not only is the normal resting relationship between the body parts changed, but the body’s relationship to the external world is also altered. Magnus says that the postural reflexes restore the normal or baseline conditions to which the exteroceptive and proprioceptive sense organs refer.

In his conclusion to the second Cameron Lecture he puts it this way:

By the action of the subcortical mechanisms described in these lectures the different sense organs are always brought into the normal relation with the external world. For the nerve endings in the skin this is accomplished by the above described attitudinal and righting reflexes. In the case of the eyes a very complicated reflex mechanism has been developed differing in various species of animals, which regulates the position of the eyes in relation to the environment. Here also labyrinthine and neck reflexes come into play.

He then adds some further explanatory words, re-emphasizing the importance of this function of the postural reflexes in continually recalibrating the sensory organs as the body performs its activities, whether voluntary or reflex:

The result of all these arrangements is that the sense organs are righted in relation to the external world, so that every sensory impression, before being transmitted to the cortex cerebri, has already acquired a certain special condition (local sign) depending on the previous righting function acting on the whole body or parts of it. In this way the action of involuntary brain-stem centres plays a very important part in conscious activities, especially as regards spatial sensations.

Co-opting and modifying the postural reflexes

It is easy to accept that Sherrington’s spider is all reflex, and Magnus’ cat, at least when it comes to responding to the sight of a mouse is little different. In both cases, their behavior is firmly, and predictably, determined by their reflex systems. Humans, however, are more volitional and less reflex in their behavior than even their nearest animal relations; the human capacity for long-term planning is an obvious example. Moreover, the dividing line between reflex and volitional in humans is not rigidly demarcated. As Sherrington says:

The transition from reflex action to volitional is not abrupt and sharp. Familiar instances of individual acquisition of motor coordination are furnished by cases in which short, simple movements, whether reflex or not, are by practice under volition combined into new sequences and become in time habitual in the sense that they no longer require concentration of attention upon them for their execution. As I write, my mind is not preoccupied with how my fingers form the letters; my attention is simply fixed on the thoughts the words express. But there was a time when the formation of letters, as each one was written, would have occupied my whole attention.

Sherrington is here describing the way in which the cortex can co-opt elements of the postural reflexes into new patterns of activity. He takes the example of handwriting, a far from innate ability, in which his cortex directs his writing hand into the formation of the letters, while his reflexes deal with the details of the necessary flexing, relaxing and movements of his wrist and fingers.

In her work with brain-damaged people, Berta Bobath fully subscribed to this view of the interaction of the cerebrum with the lower brain systems controlling the postural reflexes, as in the following:

A large part of our voluntary movements is automatic and outside consciousness, and this applies especially to the postural adjustment of the various parts of the body which accompany them. For the maintenance of posture and equilibrium, the nervous system utilises lower centres of integration with their phylogenetically and ontogenetically older patterns of coordination. These centres are in the brainstem, cerebellum, midbrain and basal ganglia.

She also argues that the highly developed human cortex exercises a much higher degree of control over the postural reflex system than happens in the animals on which Magnus worked. Discussing Magnus’ finding that normal standing takes place in decerebrate animals as long as the thalamus is present, she says:

This state of normal muscle tone and normal righting ability in the absence of cortical control does not hold good for man. Here the development of the cerebral cortex has led to an inhibition of the activity of subcortical centres. They have lost their autonomy and become relegated into the background of human motor activity. In the process of evolution man has become dependent on intact cortical activity for the maintenance of the upright posture in standing and walking, and for the complex activities of arms and legs in prehension and skilled movements.

In her work, she was dealing with the people in which pathological conditions, such as cerebral palsy, have caused a disruption in proper communication between the higher and lower brain centers. Her relevance to the present discussion is that her work provides an intermediate case between Magnus’ work in which the cerebrum is absent and that of the intact and properly-functioning human brain in which the cerebrum is effective in co-opting the postural reflexes as required.

The conditions being considered here are much less dramatic than those studied by Magnus and Bobath but are still concerned with the relationship between the cerebrum and the lower brain centres. The problem for humans arises because, in addition to their greater cerebral capacity which enables them to override their postural reflexes, they also have a neuromuscular system with a higher degree of plasticity than probably any other vertebrate. Some of the new ways people devise of using the musculature can override their postural reflexes so thoroughly that they are almost completely suppressed. Although no brain lesions are involved, this still represents a disruption of proper communication between the upper and lower brain in which the volitional, or habitual, patterns of muscle use have become impervious to the restorative promptings of the postural reflexes.

The capacity of humans to relegate their postural reflexes to the background or co-opt them into new patterns of activity in a way and to a degree impossible for any other vertebrate creature goes a long way to explain the extraordinary versatility of human behavior. It is why people are able to learn new skills and adapt themselves to a huge variety of different patterns of action, from gymnastics and ballet dancing to spending their days slumped crookedly in front of a computer screen. It is why dogs and bears make poor dancers compared to even a moderately well-coordinated human.

Overriding the postural reflexes can also bring problems. In time, after a new mode of using the body has been adopted, it can become so habitual that the person has no awareness of the extent to which the restorative action of the postural reflexes has been suppressed. One way of describing what has happened is to say the “setting” of the physiological a priori has been changed so that any reversion to allowing the postural reflexes to function properly feels wrong and the cortex steps in to ensure it is quickly “corrected”. The tendency to restore the musculature to its innate state of harmony and balance is reduced or eliminated. The effectiveness of the recalibration of the senses after phasic activity is reduced and the body gradually accumulates a series of distortions in its functioning.

This subtle but cumulative malfunctioning of the relationship between the voluntary and the reflex systems produces distorted patterns of activity that are visible everywhere. A prime example is walking. The ability to walk is an innate capacity in humans, manifesting itself in normal children from around the end of their first year. From this stage onwards, this essentially reflex activity can be co-opted in a wide variety of ways of walking depending on the influences to which the developing child and adult are subjected. Marching, slouching, shuffling, sticking the head forward, teetering on high heels, any number of new and often profoundly damaging muscular patterns can be learned and adopted permanently. These distortions of the natural gait are often so distinctive that many people can be recognized by their idiosyncratic way of walking.

The intensive training regimes to which gymnasts and ballet dancers subject themselves enable them to display extraordinary grace and skill in their performances. But the same training can cause many of these talented people to lose touch with their postural reflex systems. The result is that they no longer benefit from the restorative powers of these reflexes so that spinal and postural problems become increasingly common as they grow older. The habitual walk with turned-out toes which some ballet dancers develop, nick-named the “ballerina’s waddle,” which can lead in time to a wide variety of back and other problems, is but one of the symptoms of a training regime in which the postural reflexes are suppressed.

References

Berthoz, A., The Brain’s Sense of Movement

Feldenkrais, M. Body and Mature Behavior

MAGNUS, R. (1924) Body Posture (Korperstellung) - Julius Springer, Berlin (English translation published by US Department of Commerce, 1987)

  • (1924) Korperstellung (Body Posture) - US Department of Commerce, New Delhi, English translation (1987)
  • (1925) Animal posture - Proceedings of the Royal Society of London. Series B. Vol 98 339-353
  • (1926a) Some results of studies in the physiology of posture, Part I - The Lancet, Vol 208 531- 536
  • (1926b) Some results of studies in the physiology of posture, Part II - The Lancet, Vol 208 585- 588
  • (1930) Lane lectures on experimental pharmacology and medicine - Stanford University Press, Stanford

McCOMAS, A. J. (1996) Skeletal Muscle: form and function - Human Kinetics, Champaign, Illinois

SHERRINGTON, C. (1906) The integrative action of the nervous system - Cambridge University Press, Cambridge (1947 edition)