The perceptual basis of all motor activity includes all known senses. However, this discussion will be restricted to those perceptual mechanisms which are universally concerned with performing motor activity, eliminating occasional sensory participants in motor activity such as taste, audition, and other senses not ordinarily concerned with motor activity.

The physiological mechanisms which are universal for all motor activities form the physiological-perceptual basis upon which the organism can mount accurate motor responses in dealing with its environment. This physiological basis must be functioning properly before the organism can make any accurate motor response to his environment. This universal sensory basis of all motor activity has been called body spatial orientation. It includes postural mechanisms and also conscious perception of the body’s image in relation to its environment. For example, we can close our eyes and still be aware of our posture with regard to gravity. In combination with primarily visual recall, we can also perceive a correct image of the spatial relationship of our body within a room, such as how close we are to the front or back wall. These are obviously important functions because they serve as the fundamental basis upon which we build up all of our motor activity. Even with a perfectly normal motor system in a very well coordinated individual, if sensory information either preparatory to or during the act is not accurate, the motor system cannot accomplish the desired results. Such a person will be clumsy, he will fumble, and he will reach for things where he thinks they are but not where they actually are.

In the following discussion, I will identify each of the different major physiological components of the body which help to spatially orient the body in relation in relationship to its environment and delineate the contribution of each component. These are the various sensory receptors, which help to create a conscious, accurate awareness of our body’s position in space, during both static posture and motor activity an obvious requirement for the successful performance of motor activity.

To start, consider a person looking at a visually fixated object. The person has his eyes open, somewhere in his environment, and is looking at an object in the landscape or in the room. The person wants to know what position his body has in relation to this object. He may wait to reach for it or he may want to locomote toward it. He may want to avoid it if it is a threat, but it is essential in all cases that he correctly assess the angle and the distance and the overall spatial relationship existing between the visually fixated object and the organism, which is the person himself. The first spatial orientational component involved, obviously, is vision itself. The rather redundant term of eye vision is used because there are other eye components for body spatial orientation. Vision shows the spatial relationships between objects you can see. You can tell from familiar objects in the visual field how large or how small the object of interest is. You see a very small man and you know that men are usually more than five feet or so tall, so you know he is very far away. If the colors are indistinct and there are other cues, such as objects of known size like telephone poles in between, this also helps. Thus the actual conformation of the retinal image give a lot of information about the relationship between the visually fixated object and the organism who is looking at that object.

Now of course, the human being has two eyes and they are capable of binocular vision. That is, a human can focus both eyes on the same object. Some other animals cannot do this. Horses, for example, have divergent eyes and cannot focus them both on the same spot in the environment; eagles have eyes pointing in almost opposite directions; but man can focus both eyes on one object and this creates an angle of convergence between the visual axes of the two eyes. For near objects, the convergence angle for focusing the two eyes on the object is larger than for more distant objects. So within up to about 30 feet distance from the individual, the biologic measuring of the convergence angle is considered to be an accurate means for judging how far an object is from the individual, merely by gazing at it. The receptors for this physiological component are located in the extra ocular muscles of the eye. These very complex sensory organs, called muscle spindles, are stretch sensitive.

The main function of this group of receptors is to tell us the position of the eyeball in relation to our head. This is important in looking at different objects without moving the head. We can look at different objects just by moving our eyes, and can tell that something is up and to our right, for example, rather than down and to our left, if we do not move our head, by knowing that our eyes are looking up and to the right in relation to our head.
When we look at another point in our environment, our eyes assume a different position in relation to the skull. These sensing devices, the muscle spindles in the extra ocular muscles, also measure the position of the two eyeballs in relation to each other, so that they help judge distance and also the spatial relationships between visually fixated objects.

We have now discussed (a)the visual spatial relationship between the visually fixated object and other related environmental objects,(b) the angular relationship between the fixated object and the viewer’s head, and (c) the distance of the object from the viewer’s head.

Now we come to another important component. It is important to be able to measure the angles between the head and the body, because we would not be well-oriented if we had our head floating in space, so to speak, without relating it to our feet and our body and especially without relating it to our limbs. The limbs with which we execute most of our motor acts are, after all, located on the trunk of the body, not on the head. In order to make accurate grasps and accurate motions with the hands and feet in relation to visually fixated objects, we must connect the eyes that are in the head with the arms and legs which are attached to the trunk of the body. The connection is, of course, through the neck, which is called the cervical component of body spatial orientation. The nerve fibers from these receptors arise from the C-2 and C-3 dorsal roots high in the neck and transmit all sensation that comes in from the cervical region.

Next, as we come to the vestibular component, containing the familiar semicircular canals. Unfortunately we have overemphasized the importance of these structures, and relate all body and spatial orientation and posture, and equilibrium and balance, to the semicircular canals and the otolith structures, which together with their neuronal structures we can call the vestibular apparatus. This is erroneous, and a great deal of important evidence proves that cervical structures are at least as important. Clinical studies on humans and experiments on humans, and animals, have all clearly shown that the cervical component is as important as the vestibular system in the total orientation of the body in relation to visually fixated objects. However the vestibular apparatus is very important. There are two major structures embedded in the mastoid bone behind each ear; one is the semicircular canals and the other is the neighboring otolith structures.

The semicircular canals will sense any angular or rotary acceleration or deceleration of the head. With rotation of the head the fluid in these canals lags behind due to fluid inertia, and the fluid movement causes pressure on the sensory receptors in these canals, which fires the associated nerves and causes, therefore, certain responses. This is the same type of system that is used by engineers in guiding missles and is called an inertial guidance system. The engineers usually set up the “canals” in three basic planes at right angles to each other in order to cover all possible directions of movement, just like the arrangements in the naturally occurring biological canals. Once a missle is set on a path, any deviation from that path can be sensed by such a device, just as the human can sense deviations from a path of travel, or deviations from the static posture of the head, by the same type of mechanism. In contrast to this, the otoliths are considered generally to be sensitive only to gravity rather than to rotary accelerations and decelerations.

Of course, any accelerations, whether rotary or linear or even any static shifts in head posture in relation to gravity, will generally be sensed by the cervical components as well as the vestibular component. Ordinarily, applying a force to either the head or the body produces inertial effects on both the head and the canal fluid, thus simultaneously stimulating the cervical and vestibular components.

In our sequential consideration of body spatial orientation to a visually fixated environmental object, the cervical and vestibular components have now added the capability of determining: (a) the spatial relationship between the head and the trunk, (b) the static position of the head in relation to gravity, and (c) the directions and amounts of accelerations and/or decelerations to which the head or body, or both, may be subjected.

Now we proceed to the body contact receptors. These are activated by contact with whatever is supporting us against the pull of gravity. When we are sitting, the pertinent receptors are the cutaneous and muscle receptors in the buttocks. When we are standing, the pertinent sensors are located mainly in the soles of the feet. These receptors yield vital cues for the total orientation of the body. They are of local significance only if subjected to pressures which bear no relationship to posture. If you are standing, sensors in the soles of your feet offer major cues for which way is up and which way is down. Therefore, the general receptors of touch and pressure take on special significance for total body spatial orientation by indicating where the supporting pressure is and therefore which direction is up and which direction is down.

Studies done many years ago show that when certain receptors are denervated or detached in cats, they can stand and maintain their posture adequately, but they are not able to climb complicated things like ladders as effectively as with normal intact limb sensors.

The pertinent receptors are located within the articular capsules which bridge all joints and are called joint proprioceptors. In addition to these joint proprioceptors, there are tendon and muscle receptors. The muscle receptor is a typical muscle spindle and it is similar to the muscle spindles that are found in the extra ocular muscles of the eyes. Tendon receptors respond to stretch, but their importance in judging the angle of the limb has not been appreciated. It is now felt that the major detection or determination of the position of our limbs in space (without having to look at them) is due to the joint receptors. Some experiments I conducted on humans showed that touch and also muscle tendon receptors play significant roles as well, although their contribution to position sense accuracy is quantitatively smaller than the joint proprioceptors. Thus joint sensors are probably most important, but all of these receptors have to function together properly in order to give us our normal human accuracy of approximately 3.5 cm. as measured at the end of the index finger of an outstretched arm in pointing experiments. This represents the accuracy of position judgment arising from the human shoulder.

By the addition of the body contact component and the limb position and motion component of body spatial orientation, the organism can now also detect the point of body contact with the environment, the direction of gravity, and the position and rate of motion of the traction of the body.

It is important to realize that a normal individual can have some orientational components degraded and still retain some spatial orientation ability. However, the more inputs that are destroyed or confused, the lesser is his total ability to accurately perform motor acts, like placing his limbs on certain spots or pointing to a certain area, and any tests that validly measure motor positional accuracy will reveal an increasing deterioration of performance. There is a lot of overlap in the functions of the individual orientational components, so that a malfunction in some of these components can be partially compensated for by other components. However, each component plays a unique role as well, so that if the input from any one component is abolished, some specific function in the total ability will be lost. Therefore, we must think of body spatial orientation as the major perceptual basis for motor activity. It is the vital perceptual base from which we are able to move out effectively into the different environmental situations which call for motor responses from us.

It is interesting to consider what happens when one of the major components is deactivated. This should be a promising research approach for revealing the contribution of a component to overall body spatial orientation function. Such experiments are best done on animals since one should like to cut the nerves or otherwise destroy on of the component inputs to see how the total motor orientational performance of such an organism would be affected. We decided to pursue this research approach and we selected the pigtail monkey a primate as we are to serve as the experimental subject. The two major components which were selected for the first phase of this study were the vestibular and the cervical components. Vestibular destruction was performed first to inactivate the vestibular apparatus. All of the semicircular canals and the otoliths were destroyed by performing bilateral labyrinthectomies. (This also destroyed the hearing part of the ear.) In related experiments, we also inactivated the cervical component by destroying the first three dorsal cervical roots in otherwise normal animals.

The animals displayed normal strength postoperatively, which tended to confirm the absence of any motor damage during surgery. Histological slides made of monkey spinal cords following autopsy showed no damage to the motor system nor to any other part of the brain and spinal cord except for the dorsal cervical nerves that had been cut.

The test of spatial orientation precision was the climbing of a pegboard. The monkeys had to actually place their four limbs in proper sequence on separate, randomly staggered pegs in order to climb up and get food from a hopper at the top of the pegboard. The monkeys were interested in the food hopper because they were always fasted the day previous to the experiment. Climbing times were clocked during a test and motion picture films were taken for permanent records. We were able to demonstrate the vast potency of these two different physiological components of orientation for accurate motor coordination. (A climbing ladder was also used, with individually retracted or extended pegs to change the climbing pattern.)

We need proper objective quantitative tests in order to measure spatial orientation. A person might appear clumsy, not performing well, and yet the real trouble might be not a lack of motivation or of motor ability at all, but a sensory orientational malfunction. There are no really good tests, but we are developing some improved tests for humans and subhuman primates, and the present experiments show what can be done in objective quantitative orientational testing.

Originally, each animal was tested over a long period of time and the whole colony of animals stabilized their performance in the test situation before anything was done to them. Their performance times improved and then leveled off after about 100 days.

After labyrinthectomy the performance vent down very markedly, and after 50 days it still was only about half of normal and tended to level off at that level of inferior performance. The same results were obtained for the neck. There was a drop in performance at the point of surgery, and then some fairly fast recovery, leveling off at a subnormal level in about 50 days (at a somewhat higher level than for labyrinthectomies).

In some experiments, both operations were performed on the same animals, the second after recovery from the first. When both surgical procedures are combined, the total deficit is much greater than with either procedure separately. Thus the defects are cumulative, as would be expected from two different physiological components.

The vestibular apparatus seemed most concerned with maintenance of posture. These animals fell over more when they were trying to walk, but they did not miss as much when they were actually climbing or had things to hold onto which they could visually fixate. The converse appeared for the cervical component of spatial orientation. In this case the animals, although obviously not normal, walked relatively well, with very little falling over or complete staggering. However, these animals missed much more often when reaching with their hands for discrete objects on which they had fixed their gaze. A general principle (which needs much more study before being validated) seems to be emerging. The cervical sensory component is concerned primarily with spatial orientation of visually fixated objects. It enables us to relate the viewed object to the limbs that are going to deal with that object. In contrast, the vestibular apparatus seems more concerned with which end is up and maintenance of body posture in relation to gravity.

In summary, it is clear that these different sensory inputs contribute to total body spatial orientation for an organism and are extremely important in this role. Even with perfectly normal motor coordination and operation of the motor system, very bad motor performance may result from defective performance of some of these sensory inputs. Each one of these inputs makes an important contribution to total body spatial orientation and the total function is degraded although not necessarily to extinction, by interfering with any one of these inputs.

Another important aspect of the multicomponent nature of body spatial orientation in humans in ordinary environmental situations is the reflex response to orientational movements. When something in the environment attracts the attention of the individual, he moves his eyes toward the attracting object. If it is far from his starting position of gaze, his head will move as well as his eyes. The eyes may reach the target and come to rest with the head reaching its resting position soon thereafter. The head may not deviate as far from its neutral position position as the eyes. For example, if the object is 90 degrees right, the eyes will move toward the new object first, the head lagging behind but following, and the resting “on target” position may be a 45 degree right turn of the eyes, for the necessary total 90 degrees of deviation. The eyes start slowing down a little bit short of the target, while the head keeps moving, and then they both continue briefly to their resting target positions. Thus the necessary motion for visual fixation is carried out partly by the extra ocular muscles, and partly by the neck muscles.

The body’s orientational problem is greatly simplified if correct posture is maintained once the individual has fixated on the new object; and this is achieved by the physiological components of orientation discussed above. Now what happens as a result of these motions of the eyes, head, and postural structures? Obviously, these motions will activate eye, head and body proprioceptors. There are two general classifications of response that follow stimulation of these receptors. First, certain reflex effects occur, and second, perceptual effectsppear. These are different although they come from the same sensory receptor and therefore have a common afferent neuron as input. However, the afferents soon branch within the spinal cord, and each goes to a different part of the nervous system and each has a different type of neuro anatomical connection, and therefore each will perform a different function. One branch pathway serves a reflex function and the other, a perceptual function.

A classical reflex effect results from activations of neck receptors and is called the “tonic neck and labyrinthine reflex.” Basically, this involves extension of both limbs on the side toward which the head is turned and flexion of limbs on the opposite side. For many years, it was thought that these reflex responses did not occur In normal individuals, but they were readily demonstrated in hydrocephalic children where there is a great deal of brain damage. It was believed that the normal cerebral cortex inhibited these basic reflex patterns and thus the patterns were only significant as a clinical pathological sign, indicating loss of brain function. There is very convincing evidence now that this is not true. It has been shown that all of us exhibit tonic neck and labyrinthine reflexes when we move our head in relation to our body. The reflex will not usually produce major extensions and flexions of the limbs as is seen in decerebrated subjects, but it will alter the physiological tone of the muscles. Significant changes in motoneuron firing can be shown with equipment sensitive enough to measure it. Overt reflex effects do not appear in normal humans, but reflex effects are nonetheless present and play a significant role in body spatial orientation during and following head movements. Without actual motion of the limbs there is nonetheless a difference in muscle tension arising from activation of head and cervical receptors. The tone in the extensor muscles is increased on the side toward which the head is turned and the extensor tone on the opposite side is decreased.

This reflex tone can create stressful situations and it must be considered whenever neck motion occurs. If you want to train an individual to do certain motor acts which oppose these natural reflex changes, the individual may have problems in going against a basic physiological pattern of response. It has also been found that elevating the head causes extension of both forelimbs and flexion of the hind limbs. Similarly, depressing the head toward the chest will cause flexion of the forelimbs and extension of the hind limbs. Any of these head motions will thus produce tonic changes in the muscles, and if it is your happy lot in life to train people in motor activity which requires opposite responses, the training task becomes more difficult. For example, in basketball shooting you may desire the person to look up with his eyes and head at the basket while simultaneously flexing his extended arms in order to get ready for shooting. This can be an especially difficult training task since you would first have to train him to erase the basic reflex linkage between the head and the arms before you could proceed to train him in the correct response. The tonic neck and labyrinthine reflex would facilitate arm extension during head elevation while you actually want arm flexion during head elevation.

The most widely studied responses to vestibular stimulation are the nystagmus movements. These are involuntary, rhythmical, back and forth motions of the eyes which go very fast and therefore are hard to see, but are relatively easy to record. All that is required is electrodes at the two corners of the eye, recording the voltage difference between the two. The only difficulty is that nobody has ever shown what normal function, if any, is served by nystagmus.
It is definitely considered to be an abnormal sign in many cases. Positional nystagmus is a clinical sign that indicates undue pressure in the fluid inside the ear which affects the hearing organ as well as the canals. It is highly questionable whether nystagmus ordinarily occurs or validly measures any normal useful function involved in body spatial orientation. But it is recorded widely, nonetheless, as a measure of vestibular ocular reflexes. The clinician usually measures nystagmus by irrigating the ear with hot or cold water, thus setting up convection currents inside the canals and simulating acceleration stimulation. Rotating a person in a chair also produces nystagmus, but may produce unpleasant effects of dizziness and nausea.

The vestibular apparatus has been considered responsible for certain other reflex responses of the eye. When the head is moved into different positions, a compensatory reflex movement of the eye occurs, related to the direction of the movement and postural relationship between the position of the body and head with the visually fixated objects. These compensatory eye movements were thought to be a response of vestibular apparatus. However, with the vestibular apparatus destroyed, the compensatory movements of the eye still occurred in response to postural shifts. These are normal eye adjustments which occur in all people under proper conditions, and they reduce the deviation from the visual axes from the horizontal when head position is tilted from its normal vertical position. Compensatory reflex movements of the eye are typically opposite to the direction of the shift in posture. It has been proven that these responses are mainly brought about by the neck receptors, since if the first three dorsal cervical roots are cut, the normal compensating eye reflex movements do not occur in response to a change in posture. Possibly the vestibular receptors contribute something to these spatial orientation reflexes. Unfortunately, people who work on the vestibular apparatus in this type of experiment do not inactivate the neck receptors, and since they usually employ rotation or motion of the total organism as a stimulus, they are unjustified in assuming that any reflex change in the eyes or any conscious perception of the body orientation changes are due to the vestibular apparatus. This is not only unfortunate, it is completely incorrect. Any positional movement of the body will stimulate cervical as well as vestibular mechanisms.

It has been shown that nystagmus eye movements can arise as a result of pure neck receptor stimulation. Vestibular stimulation can be prevented in humans by the simple expedience of preventing head movement. A person can be seated on a swivel so that his body can be moved while the head is kept constant in relation to the environment. Such movements will produce movements only in the neck, and yet will evoke nystagmus responses. So even in regard to nystagmus, which seems to be the most authenticated reflex adjustment of the vestibular apparatus, it is clear that this response arises from cervical receptors as well as from vestibular areas.

I think we must mature beyond the simple “one physiological input” concept. We must at least include these three major physiological components: (a) the position of the eye in relation to the skull, which is the extra ocular sensory device, (b) the vestibular component, which orients the head in relation to gravity and to the acceleration of the body, and (c) the cervical component, which orients the head in relation to the body and measures acceleration because of the inertial lag of the head in relation to the trunk.

All of these components contain reflex mechanisms which can produce illusions, and with correct experimentation of humans these can be shown. For example, one can change the direction of gravity unknown to a human subject by changing the speed at which he is being driven around on a human centrifuge. The subject is then asked to adjust a fixated spot of light in the darkened cupola of the centrifuge while he is being rotated. The subject obtains the impression that the spot of light at which he is looking has shifted upward, but actually it has remained stationary. The amount of apparent shift is proportional to the apparent shift in direction of gravity, which in turn is proportional to the amount of centrifugal force.

It is thus clear, that while the reflex responses of these physiological components of body spatial orientation do not produce a conscious awareness in themselves, nonetheless they manipulate the body, the hands, the head and the eyes. These reflex motor movements are bound to affect the conscious perception of body spatial orientation, which after all is composed of inputs from visual, vestibular, cervical and body movement receptors.

This conscious perception can be measured quantitatively by a test of verticality and horizontality. If you stimulate cervical muscles, for example, on the left side of the neck, the apparent vertical will seem to shift toward the other side, even though there has been no actual movement of the head nor of the environment. Similarly, in kinesthetic judgment of that which is vertical, as measured by a person feeling a ruler or yardstick which can be swiveled and then placing it in whatever position he considers to be vertical, that person makes greater errors when his body is tilted than when it is in the perfect vertical. Again, the errors are predominately toward the opposite side from that toward which he is tilted. He tends to feel that the environment has shifted with him.

However, we have no good test of body spatial orientation at the conscious level. We can measure depth perception as a specific entity. We can measure our ability to negotiate complicated motor acts, much as is done with monkeys in climbing pegs, and we can do this with people too. A rail test has been used which is really little more than a modification of the police “walk a straight line” test for alcoholic disorientation, the only innovation being the use of walking rails of different widths. However all of these tests are measuring different individual features of total body spatial orientation and there is still a great need for some good measure in humans of body spatial orientation as a total function.

In the remaining space I would like to point out that serious physiological affronts to the organism are often introduced by workers in human behavior, by ignoring the importance of physiological stress. Orientational reflex effects are often ignored, as are spatial disorientations, both of which are introduced by environmental motor activity that a subject is being asked to perform. But the person’s performance can subject him to a tremendous amount of physiological stress. The fact that somebody can do something does not mean that this is the right way to do it or that this is a good way to do it. We have not measured physiological stresses enough.

I am interested in doing a study of school children in elementary and private schools in Philadelphia, using children in different learning situations with different postures and measuring what the actual physiological stress is. We want to measure two things specifically: first, muscular effort, by measuring the electroatvographic (emg) recording on the surface of different postural muscles. From this we get a direct specific measurement of which muscles are being physiologically involved or stressed. We can present different postural situations, different desk relationships, different sitting positions, while requesting performance of different visually oriented tasks. Secondly, we want to make some traditional physiological measurements such as heart rate, respiratory rate, and oxygen consumption. All measurements should be made with telemetry, so as not to interfere with the classroom situation or with the patient. A student performing in an awkward postural and orientational situation can have significant quantitative changes in these measures, since total physiological energy requirement and, therefore, the responses of the heart and circulatory and respiratory systems would be changed. Furthermore, specific muscles can be individually stressed in certain postures even though the general body might not show much stress.

Such recording of physiological effort and stress in unencumbered human subjects is within the present state of the art and this sort of study should have been done long ago. A number of years ago, a study in Texas showed that exposure of children to classroom situations actually increases the incidence of postural defects. (Examples of postural defects are: dropped shoulders, development of one leg longer than the other, a tilted pelvis, or other deviations which orthopedists and others would consider defects.) For example, in grade 1A the children came in with 7.1 per cent postural problems. Grade 2 was up to 26.6 per cent; grade 3, 28.3 per cent; grade 4, 40 per cent, and grade 4B, 46.1 per cent. These data are statistically analyzed to show that the differences were significant. Thus it is clear that in this school system the normal classroom environment was introducing postural problems. Apparently, the students were chronically exposed to a stressful situation. While individuals respond in different ways to stress, it seems clear that in these students, postural stress developed which became manifest as postural deformations. It could be that the student is asked to perform tasks that strain his total perception of spatial orientation, or that introduce spatial reflexes which make them difficult to perform, and he makes postural adjustments in order to minimize these stresses.

This is a form of adaptation and we all know how well the human body can adapt; but I would close with a plea that we do not try to force the human to adapt at all costs to his physiological system. We should assume that everybody can perform well in his motor task if we find the right sensory-motor conditions for each individual requirement. We should set for ourselves the goal of minimizing physiological stress. We must change from saying “How can I drive the person harder so he will begin to perform the way we want under the conditions prevailing?” and replace this crude and physiologically insulting approach with the more sophisticated and physiologically more correct approach of “How can I manipulate the environment and man’s relationship to it so as to reduce body stress to a minimum and facilitate the task?” Simply put, it means that we must stop concentrating everything on forcing the man to adapt to the task. Instead we should force the task environment complex to adapt to man and his natural physiological norms and capabilities. This is not only a more humanistic approach but it also makes infinitely better sense biologically.