A synthesis of classic and modern neurobehavioral literature dealing with the principles by which complex, purposive, and intelligent behavior is generated, this book features:
* papers by C.S. Sherrington, E. von Holst, D.M. Wilson, G. Fraenkel, H. Mittelstaedt, and P. Weiss
* clear descriptions of three types of elementary units of behavior -- the reflex, the oscillator, and the servomechanism
* a review of the diverse manifestations of hierarchical structure in the neural mechanisms underlying coordinated action.
This volume has proven to be of great value to psychologists, neurobiologists, and philosophers interested in the problem of action and how it may be approached in light of modern neurobehavioral research. It has been designed for use as a supplemental text in courses in physiological psychology, neurobiology and behavior, and those courses in cognitive and developmental psychology that place particular emphasis on understanding how complex behavior patterns are implemented.

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1 | Introduction and Overview: De Anima and Animals |
The windmill stands on a plain, moving only when acted upon by a palpable external force, the wind. Its movements are relatively simple, extremely stereotyped, and obviously molded by the structure of the mechanism.
Beneath one of the footings, a wild rat digs a burrow. There does not seem to be any external force that initiates the rat's movements. Its movements are bafflingly complex and not at all stereotyped. The precise form of these movements varies constantly. These variations are not random. They are almost always functionally appropriate. The variations enable the rat to overcome obstacles to its continued tunneling. They adapt the digging pattern to the fluctuating conditions with which it must cope. Finally, it is not at all clear how, or even if, the observable structure of the rat determines any but the outermost limits on the form of its movements.
The movements of animals differ so strikingly from the movements of inanimate objects that throughout most of the history of analytic thought about natural phenomena it was taken virtually for granted that these movements betrayed the presence of processes of a nonphysical nature. The very term animal derives from the Greek word animos, by way of the Latin anima. The original Greek meaning was âwind.â Greek and Latin philosophers used the word to refer to some active but insubstantial principle or aspect of reality that was present in âanimalsâ but absent from the ordinary objects of the physical world. This concept of anima was transmuted into the concept of a soul as Hellenic thought fused with Hebraic thought. The presence of anima was invoked in order to explain the phenomena of organismic movements. So great was the apparent discrepancy between the movements of animals and the movements of ordinary physical objects that a special constituent seemed clearly called for.
In the late Renaissance, analytic thinkers first confronted man made machines that made intricate lifelike movements in the absence of any apparent external forces. These animated machines were the fancy clocks and mechanical dolls that were a by product of the Renaissance explosion in man's mechanical ingenuity (see Fig. 1.1). These clockwork animals and statues suggested to Descartes that at least some aspects of animal movement might be explainable on purely physical principles. One could explain some animal movement in exactly the same way as one would explain the actions of a machine, that is, by describing the structure of the inner mechanism and invoking one or another kind of physical causality.
But the behavior of the animated statues of Descartesâ time was only superficially lifelike. Upon close examination, it lacked intelligence. There was no indication that thought or thoughtlike processes played a role in patterning the movements of these machines. The movements of these machines did not adapt in an intelligent way when circumstances were altered so as to render the normal pattern of movement nonfunctional.
As a philosopher engaged in writing out a philosophical essay, Descartes was intensely aware of the role that thought plays in patterning some kinds of human action. He did not think that the more intelligent actions, the ones shaped by thought, could be explained in the same way one would explain the actions of a machine. In his famous dictum, âI think, therefore I am,â the âIâ refers to a special nonphysical constituent of Descartes, the thinking constituent. This constituent is the sovereign soul. Its deliberations initiate and direct our more intelligent actions, as for example, the actions we perform when we play chess, write out the proof of a theorem, or write out a philosophical essay. This soul is by definition free of the dictates of physical determinism. âCogito ergo sumâ is an ad hominem argument for the existence of this nonphysical constituent, supposedly directing the movements of the hand that holds the philosopher's pen.
It seemed to Descartesâand it still seems to most of usâthat one could never build a machine capable of composing philosophical essays. Nor did it seem that this was for want of small enough or precise enough gears, nor any other such trivial reason. Rather it seemed that the processes underlying man's more thought-filled actions must be such that they could not in principle be embodied in the workings of a machine. These principles, however vague we may be about what exactly they are, seem to possess a subtlety and refinement that precludes their realization in anything subject to the gross constraints of the physical world. Our intuition fairly screams that the principles governing our more intelligent actions require for their realization a domain free of the constraints of space and time, mass and energyâthe constraints that fetter operations in the physical domain. Our thoughts require, in short, a mental domain, the domain of intelligence.

FIG. 1.1. The 17th and 18th centuries saw the construction of the first lifelike automatons, culminating in: (a) Jaques Vaucanson's duck, which swam, flapped its wings, preened itself, ate food and excreted the feces-like results of its âdigestionâ, (b) Pierre Jacquet-Droz's âscrivener,â a doll that wrote out the words âWelcome to Neuchâtelâ after dipping its pen in an ink well and shaking it twice. Later Droz, in collaboration with his son, constructed a âdraughtsmanâ whose movements were so lifelike that the elder Droz was tried for sorcery. [Reproduced from: Eco, U., & Zorzoli, G. B. The picture history of inventions. New York: Macmillan, 1963].
One of the characteristics of human action that seems to betray the presence of some nonphysical âintelligence,â is the extraordinary flexibility manifest in human action. Bruner (1970) comments with bemused chagrin on the motor flexibility displayed by his stepson, who, it appears, employs this flexibility to humble his distinguished father on the squash court.
My stepson who, I assure you, is not so stylish a squash player as I am but a cleverer one, has beaten me all too regularly by such feats as hitting a return beneath a raised leg when caught facing the rear wall of the court! When humans can do this type of substitution in real time, we say they are good athletes; there are situations not so constrained by timing where we would be more likely to say that the performer who showed a flair for appropriate substitutions was âcleverâ rather than a good athlete [p. 66].
What is remarkable about the movements of skilled athletes is not only the wide variety of actions used to achieve the same general end but also the rapidity with which the particular actions are altered in order to cope with changes in circumstance. The flexible and rapid adoption of new action sequences in response to changes in circumstance is so closely allied to our intuitions about intelligence itself that Bartlett (1958) begins his influential book on thinking with a lengthy discussion of the characteristics of skilled action. If, therefore, one can describe the kinds of neural circuitry and organizational principles that enable animals to make rapid but functionally appropriate modifications of ongoing patterns of movement, one has begun to describe the physical basis of intelligence.
PHYSICAL REALIZABILITY
In this book, I assume that we are allowed no recourse to physically unrealizable principles and processes in order to explain what underlies the organization of action, no matter how intelligent that action appears. I reject, in other words, the distinction between âintelligentâ actions and machine actions. I assume that the intelligence of animal action is simply a consequence of the intricacy and subtlety of construction in the machine that generates that action, namely, the central nervous system of the animal. Since an orderly temporal sequence of muscular contractions underlies any animal action, a scientific analysis of the organization of this action is concerned with specifying the types of physically realizable processes that underlie the generation of orderly temporal sequences of commands to the muscles of the body. Thus, one constraint imposed on the discussion at the outset is that we consider only processes that can be specified in sufficient detail so that an embodiment or physical realization of the process (i.e., a working model) can be built.
Such a commitment does not imply the metaphysical belief that physical reality is the only reality. Computer programs are certainly real. To believe otherwise would be to believe that IBM invests vast sums of money every year to develop and copyright unrealities. Yet computer programs are not physical entities. A computer program is a sequence of instructions causing the computer to do first this, then that, and so on. In order for instructions to be executed by a computer, they must be embodied in some physical form, such as a set of holes in a paper card, or a sequence of magnetized spots on a tape. But IBM does not copyright any physical embodiment of the sequence of instructions. A sequence of instructions is an abstraction. It has no weight, no energy, no position in space and time. In short, it has none of the attributes that physical things have. Computer programs are, in fact, an illustration of the fact that conceptions are real; where by conceptions I mean coherent sets of principles. And by principles I mean explicit rules or laws that determine how something will behave, as, for example, the instructions in a computer program determine how the computer will behave. In the final analysis, what this book is about are the conceptions by which we may understand the generation of animal action. However, these are required to be conceptions of a particular kind, namely conceptions that may be embodied in the structure of a machine.
In practice, the commitment to physically realizable conceptions means largely that 1 hope to use only precise and explicit conceptions rather than vague and implicit ones. An excellent test of the precision and explicitness of a conception is to build a physical embodiment of it, or to find one that is already built. Thus, for example, in Chapter 6, one can convince oneself of the precision and explicitness of the concept of a tropotaxis simply by noting that the Sidewinder missile constitutes a physical embodiment of this concept. It is in this spirit, that I occasionally illustrate the conceptions presented in this book by reference to electronic (e.g., p. 57) or mechanical embodiments of them.
One of the odd characteristics of the mental versus physical dualism that has been a central feature of Western thought for several centuries, is that precise and explicit principles that were necessarily mental (in the sense of not physically realizable) have very seldom been put forward. The principles that many firm dualists have put forward in order to explain events supposedly occurring in the mental domain have been physically realizable, at least insofar as the principles were precise and explicit. For example, the laws of association formulated by 18th and 19th Century English philosophers, all of whom were dualists, are easily given a physical realization. It is easy to construct a machine that exemplifies the law of contiguity, which states that the more often two inputs have occurred together, the more readily the occurrence of one input will activate the record of the other. Other laws of association, insofar as they are explicit and unambiguous, are readily simulated on a computer. Since a belief in dualism generally rests on an intuition that the actions of the mind are inexplicable by physically realizable principles, it is curious that the laws of the mind formulated by dualist philosophers should be of a kind that are easily given a physical embodiment. If one constructed a machine that operated exactly in accord with the laws that determine the operation of the mind, in what sense could one claim that the machine did not have a mind?
It might be objected here that any and all precisely formulated principles may be given a physical realization. I believe, however, that a principle or a conception may be precise and explicit and yet not be physically realizable. Higher mathematics seems to be full of such conceptions. I say seems to be, because some bizarre mathematical conceptions, such as non-Euclidian geometries, have a disconcerting tendency to be the best representations of physical reality, when physical reality is probed deeply enough. Nonetheless, certain mathematical conceptionsâsuch as the function that is 1 for all rational values of its argument and 0 for all irrational valuesâcannot have a physical realization, despite their mathematical precision and explicitness. That is to say, the relation described by this precise but bizarre function could not hold between any physical variables. This function could not describe, for example, the relation between time and the velocity, mass, energy, and so on, of any physical entity. Nor could a computer print any finite segment of this function in any finite amount of time. Thus, it is possible to have principles of the kind to be treasured in any dualistic account of action, that is, in any account where action is thought to be determined by physically unrealizable principles. A commitment to physically realizable principles does exclude certain principles that could be thought to determine action.
Some parapsychologists seem to believe that one mind may influence the action of another without the expenditure of any energy in the physical sense of energy. If this belief should prove true, then there are indeed physically unrealizable principles determining human behavior. However, believers in the occult do not seem inclined to formulate those physically unrealizable principles in a precise way. They seem content merely to emphasize their nonphysicalness. So, to repeat, in practice the commitment to physically realizable conceptions is a commitment to precise and explicit conceptions.
A further constraint, honored strongly during the early part of the book and less strongly later on, is that there be compelling experimental demonstrations that processes of a suggested type really are at work in determining the temporal ordering of muscle commands in a living organism. This commitment reflects my scientific upbringing. I am a physiological psychologist. I am concerned not only with the conceptions by which we may understand the generation of animal action, but also the way in which those conceptions are embodied in the organ of that action, namely the central nervous system. In so far as possible, I want to indicate in this book how various principles are, or at least might be, embodied by neural circuits, functioning in accord with known principles of neurophysiology.
In short, I cannot resist the temptation to neurologize. In some cases, the existence of neural circuits of the kind posited by the neurologizing is supported by experimental observations at the neurophysiological level. In most cases, the neurophysiological evidence for the proposed circuits is at best suggestive. In some cases, the proposed circuits are rank speculation. In all cases, however, the proposed circuits do at least function in accord with experimentally demonstrated principles of neurophysiology. The purpose in suggesting specific circuits is only to show, where possible, that a neurophysiological embodiment of a given conception may readily be imagined.
The danger in proposing neurophysiological embodiments is that the reader may mistake the embodiment for the conception itself. In the hope of forestalling this, I aver here and now that most of the neural circuits proposed in the chapters that follow will no doubt prove to be wrong, in details if not in toto. The conceptions they embody will, however, prove to be correct; or so I hope. That is, when we have an experimentally documented picture of the neural circuit mediating a particular behavioral function, it is to be hoped that that circuit will be a recognizable embodiment of the conception by which that function was âexplainedâ in these pages.
THE INTELLIGENT COCKROACH
In attempting to demonstrate that the kinds of processes invoked to explain the organization of action are physically realized in living organisms, I frequently consider experimental work on organisms as lowly as the snail and the cockroach. Descartes was willing to consign the motions of nonhuman animals to the domain of phenomena that might be explainable on purely physical principles. Had he been aware of the intelligence that is manifest in the movements of such lowly animals, he would perhaps have been less willing to strip animals of their anima.
The cockroach, unlike man, has not two but six legs that must be moved in an orderly sequence in order for the roach to progress out of the light and into the dark, hidden areas where it quite justifiably feels safest. The roach that one sees scurrying out of some suddenly illuminated area is moving his six legs in a sequence that would please the most fastidious engineer. At any moment, three of the legsâthe front and back legs on one side and the middle leg on the other sideâare planted on the ground to form a tripodal support, while the other three legs are being lifted and moved forward. When one triplet of legs has been lifted and advanced, it then supports the body while the other triplet is lifted and advanced. Thus, the sequence of leg movements of the scurrying roach is organized in such a way that at every moment of the sequence the body is held up by a stable tripod. The tripod is stable because the triangle formed by the triplet of planted legs encloses the vertical axis (the center of gravity) of the roach's body.
Our appreciation for the complexity of the organizing principles underlying the roach's leg movements is heightened when we consider the number of individual components (muscles) that must be suitably ordered into action for the legs to exhibit the alternating tripod sequence of the rapidly running roach. Oversimplifying somewhat, the motion of each leg is controlled by the contraction and relaxation of six muscles. In order for the six legs of the roach to be moved in an orderly tripodal sequence, 6 Ă 6 = 36 muscles must be contracted and relaxed in an orderly sequence.
If the alternating-tripods sequence were the only sequence that the cockroach used in forward progression, we might be impressed by the intricacy of the processes that could organize the activity of 36 muscles, but such intricacy would be clearly within the design capabilities of even a Renaissance clockwork mechanician. The Renaissance clockmaker would be more severely taxed, however, if we asked him to make a machine that exhibited all of the leg movement sequences exhibited by the cockroach in forward progression. Th...
Table of contents
- Front Cover
- Half Title
- Title Page
- Copyright
- Dedication
- Content
- Preface
- 1. Introduction and Overview: De Anima and Animals
- 2. The Sherringtonian Reflex
- 3. Sherringtonâs Combinatorial Principles
- 4. Von Holstâs Coupled Oscillators
- 5. The Role of Coupled Oscillators in Locomotion
- 6. Servomechanisms: The Control of Taxes in the Coastal Snail
- 7. Reafference and Efference Copy
- 8. The Hierarchical Structuring of Action
- 9. Manifestations of Hierarchical Organization in Action
- 10. Central Motive States
- 11. Representation of the World and the Organization of Action
- 12. Some Recent Trends
- Glossary
- References
- Author Index
- Subject Index
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