W.S. McCulloch


While my Interest in the functional organization of the nervous system for the control of posture and movement sprang from the study of its diseases in neurological patients, my experiments and those of my numerous collaborators were performed just on cats and monkeys.

I shall make use of information gathered by many others - clinicians and physiologists but I will have to be very sketchy where they would be precise and detailed, for I would like you to see at a glance how the whole system looks. It is the general characteristic of this organization, rather than its details in dissimilar animals, that is our first concern. Special tricks should come later.

Here, we shall not be concerned with the properties of single neurons or their parts, except as these affect the function of the circuits mediating control. Each neuron computes some functions of its inputs and then emits impulses over its axon, and this, rather than the patterns of connections and codings, is the precise physical mechanism that matters here. All sensory cells proper are connected by the afferent peripheral neurons (bipolar cells that look much alike on their input and output sides) to the central nervous system that contains our computing neurons. These talk to each other and to so-called motor neurons, or efferent peripheral neurons, signaling to muscles and to the relay neurons that control smooth muscles and glands. About 150 years ago, Magendie described a reflex in terms of a peripheral activity which sent impulses into the back of the brain and spinal cord, causing impulses that came out the front, or ventral root, which went to the place of peripheral activity and there stopped or reversed the activity that gave rise to the incoming impulses. This is clearly an inverse, or negative, feedback of signals conveying information, not energy or some other physical quantity. Reflexes are the simplest units of the organization of control. Each would be essentially a governor if it had a fixed, or constant, comparator in its return loop, but since this can be determined by activity of other neurons, it is best to think of them as servo systems controlling muscles.

In carnivores and primates there exist short arcs with direct connection of afferent to efferent neurons, but these are not to be found in most species, and, even in those that have them, are supplemented by arcs through other central neurons — called internuncials.

Reflexes concerned with motion at a joint are so hooked up internally that contraction of muscles to move them one way is accompanied by relaxation of their antagonists. I speak of such reflexes as underlying postures like standing and motions like walking. The receptors involved are of two major kinds: one in joints and tendons, signaling positions and accelerations, the other within the muscle bodies, signaling stretch. To these organs come so-called gamma efferent fine fibers that tune the receptor so that the repetition rate of its impulses over afferent neurons can be set to determine a length of the muscle appropriate to the posture or motion.

This trick of setting receptive filters occurs In the eye, and In the ear, both for auditory sequelae ofthe cochlea and for signals of acceleration from the vestibule.

Beside reflexes so elicited, called Extensor and Flexor reflexes, there are reflexes elicited by painful inputs that pull away the injured part — the Flexion reflexes — that always have their only path through internuncial neurons.

In lower segmental forms each segment is relatively independent, but with the development of arms and legs several segments have become rather richly interconnected in various ways. The afferent peripheral neurons themselves reach an increasing number of segments, and increasing numbers and lengths of intersegmental connections appear over spino-spinal fibers. In the lateral cell mass of the spinal cord, the lateral reticular nucleus evolves to control alternating motions like walking and running, and simultaneous ones like sitting, squatting, and standing. Similarly, higher in the cord, the same goes for the forelegs or arms, and in the brain stem for respiration. This is perhaps best described by so-called half-centers that can be alternated or synchronized by their inputs from the rest of the central nervous system.

I first realized how autonomous these larger control devices were when I saw a patient who had been shot through the spine and had more than two segments of his spinal cord destroyed at the level of the chest. His legs continued to walk as long as his feet touched his bedclothes. He had postural contractions for defecation and had erections and ejaculations, and developed an automatic bladder. This is even more spectacular in Shurrager's work, when after a similar destruction of the spinal segments in newborn puppies, the forequarters learned how to make them walk, run, and jump appropriately by putting proper strains on the hind quarters.

Next, there are long spino-spinal reflex connections relating the activity of the forequarter to the hindquarter and, finally, relating all of these to the head and neck reflexes.

Thus we have: (1) segmental reflexes, (2) neighboring intersegmental reflexes, and (3) long intersegmental reflexes, each exerting control over those of the more local controls and, finally, over the most local reflexes, or simplest servo systems.

While there are interesting and somewhat similar hierarchies in our house-keeping circuits, we are not concerned with them in these problems of posture and motion, for we are not considering the command system where all of these interact in our decisions, mediated by the core of the reticular formation.

In front of, or above all these, we have the so-called suprasegmental structures which, beside requiring all information from below, have distance receptors for smell, taste, sound, and sight, but most notably receptors for accelerating the vestibules. I know of no important tuning of receptors for chemical sense. The others all have them. Something like a tenth of all the large axons in the optic stalk go from the brain to the eye, but there are not yet any certain functions that they are known to perform, and, from the nature and locations of their junctions in the eye, it would not be safe to say whether they excite or inhibit events in the retina. In the ear, both the cochlea for audition and in the vestibule for detection and measurement of acceleration, they are far less numerous and more homogeneous, and evidence, thus far, suggests that they are all inhibitory at the base of receptor cells themselves.

I know of no direct, or almost direct, relation of smell to the organs controlling posture or movement. The eye has a direct path to two little hills on the back of the midbrain called the superior colliculi, which are indirectly connected to the third, fourth, and sixth interlocked nuclei that determine the direction of gaze, the opening of the eye, and the constriction of the pupil. The dilatation of the pupil has an extra path over the sympathetic system, usually demonstrated by the response to pain, chiefly in the face and neck. A second path to the controlling nuclei comes from the vestibular mechanism, in part directly, and in part via the cerebellum. The direct part determines that the eyes retain their direction of gaze when the head moves, thereby helping to keep the image in place on the retina. Signals from the neck muscles have a similar effect. We shall come later to the cerebellar path, for its effects are much alike in all motor systems. Though it is hard to see it in man, the ear toward which the eyes turn is drawn backward. In animals who show it well, after removal of the brain ahead of the superior colliculi, a click to one ear turns the eyes there and pulls back that ear. I do not know its anatomic path in any detail. The point in going into these details is that one must think of these many structures as having built-in connections that conduct these reactions. There are similar connections concerning the tongue and the jaw in swallowing and in respiration, but they are less familiar and have been demonstrated by your first speaker.

To return to visual input, note that in mammals there is a large direct path to a part of the thalamus, or anteroom for the cerebral cortex, called the lateral geniculate – or outer knee – where signals from the left halves of both retinas play on the left one and the right halves on the right one, whence both are relayed to the visual area of the cortex that maps the left visual field on the left hemisphere, and the right on the right; and both maps are upside down. Adjacent to that visual cortex is a strip whence impulses descend to the superior colliculi to adjust the direction of gaze on the basis of the cortical visual image. This is but one instance of a general cortical scheme for each receptive field, for vision, touch, and sound each has its own neighboring strip that directs the receptors for its sensory modality. In us the cortex has usurped so much authority over lower structures that its damage produces some irrevocable loss of performance, but even in man this control generally goes over very indirect paths to determine performance. Let us, therefore, ignore it for the present and look at lower structures.

Under the cortex and against its anteroom lie the basal ganglia which extend into the lower portion of the midbrain. They have inputs from many sensory modalities and the cortex plays on them. Diseases of these structures, or of their inputs and outputs, produce wrong muscular tensions, spasticities and rigidities, lack of blinking, a set facial expression, pill-rolling tremor of the hand, etc. When they are working normally, they yield those smooth motions that we regard as natural volitional acts. They first fix the axis of the body, then move the hip and shoulder, then the knee and elbow, then the ankle and wrist, and last, the foot and hand, so that these motions seem to flow outward. When they are damaged, volition itself is diminished and sometimes fails without special provocation. When a single point in them is stimulated in the chronic decorticate cat, it goes through the graceful motion of scooping a goldfish into its mouth, or some similarly programmed activity, according to the point stimulated. The most revealing demonstration of the role of the basal ganglia in determining the posture and motion of the body on the body, as opposed to guiding it by external clues, is that of Paul Yakovlev who takes two patients so rigid and tremerous that they cannot feed themselves, and seats them opposite each other where each can easily feed the other. Think, then, of these structures as a rich storehouse of programs of typical voluntary acts that run half-centers of lateral reticular formations to produce the required postures and movements.

When I speak of these motions as natural, I do not mean that they are necessarily innate. Birds have no cortex or thalamus worthy of that name, yet they can learn tunes and even speeches by heart. How long these programs may continue a performance I do not know, but your first speaker has a habit of whistling a Hungarian tune, and his starling has learned it, and variations on it, and will sing them for minutes on end. His wife is a pianist, and from her the bird learned a surprisingly long passage of Mozart. Surely these bespeak long acquired programs.

How fast these programmed acts can alternate is seen clearly in the smooth alternating movements such as one uses in a vibrato or a trill reaching a maximum frequency of acts at 10/sec, which is 20 reversals/sec. This is lost with some lesions of these structures, or replaced by a tremor whose frequency is, at most, some 10/sec.

Finally, I want to speak of the big bulge on the back of the hind brain. Its oldest portions receive signals from both vestibules for balance, and from the old portion of the inferior olive, which has paths to it from old parts of the brain stem and from the spinal cord, and it sends axons to the big cells of the cortex of the cerebellum, say one to each, called climbing fibers. These big cells send axons to its nuclei, which differ in number and size from species to species. The nuclei then send these axons back to the reticular formation. As we go up the vertebrate phylum, the cerebellum grows into a host of ridges running athwartship, and these cells are lined up along the ridges like telephone poles. Specialized cells grow up connecting the rows and, finally, an input appears from the body and all parts of the brain. The input ends on incredibly many small cells whose axons go outward and divide into two thin branches running like wires through the telephone poles, i.e., transversely. They bring to it signals of every sensory modality, especially vestibular and those that report position and motions.

Now the business of the cerebellum can be simply stated. It must bring to rest at the right place and time whatever is put in motion. Most of our acts are ballistic. We jolt a muscle into contraction and jerk a part into motion, and we shadow the jerk by a counterjerk so timed as to stop the part at its target. Thus, the cerebellum is at least an interval clock. When it is out of commission, eyes jerk toward a target and undershoot or overshoot. Feet slap, stamp, or fail to reach the ground. Words become expressions of syllables. A small lesion disturbing the timing of the left arm in a first fiddler ends his career.

With the evolution of the great cerebellar cortex has come the development of a new larger inferior olive and a corresponding development of its efferent nuclei. This is naturally so, for to do its job it must be informed by the cerebral cortex of the details of the environment, by the basal ganglia of the program under way, by the spinal cord and vestibules of the positions and accelerations of the head, the body, and the arms and legs in great detail.

But once one has such an interval clock that can be tapped at all points, one has an ideal autocorrelation to bring signals up out of noise. This is important in navigating by weak signals. Birds have big cerebellums, and in the weak electrical fish that detects a 1-mm glass rod at 1 meter by the difference in signal that returns to it through brackish water, the cerebellum fills the bulk of the head.

In this synopsis I have briefly touched upon every topic in order that you might see the system of control of posture and motion as a whole. To be fair, I should add that I have carefully avoided the command system of the reticular core which commits the general himself to fight or fly, to sleep or wake, to eat or to make love. And I have avoided its War College, or long-range computer of strategies, the frontal pole of the cortex. I trust you will forgive me.


For further research:

Wordcloud: Acceleration, Activity, Acts, Arms, Axons, Body, Brain, Called, Cells, Cerebellum, Concerned, Connections, Control, Cord, Cortex, Details, Determine, Direct, Ear, Efferent, Eye, Finally, Head, Impulses, Information, Inputs, Lateral, Learned, Motion, Muscles, Neurons, Nuclei, Organization, Path, Performance, Peripheral, Posture, Programs, Receptors, Reflexes, Reticular, Segments, Signals, Similar, Spinal, Structures, System, Tune, Vestibules, Visual

Keywords: System, Posture, Information, Tricks, Organization, Cortex, Wiring, Cells, Neurons

Google Books:

Google Scholar:


1 Reprinted from Biomechanics, pp. 181-185. Bootzin, D. and Muffley, H.C. (Eds). Publ. by Plenum Press, N.Y., 1969.
2 This work was supported principally by the National Institutes of Health, Grant 5 ROI NB-04985-04.