This target article suggests a new interpretation of efferent influences on sensory receptor activity and the role of the senses in forming knowledge. Experimental data and a thought experiment about a hypothetical motor-only organism suggest that the senses are not transmitters of environmental information; rather, they create a direct connection between the organism and the environment that makes possible a dynamic organism-environment system. In this system efferent influences on receptor activity are especially critical, because with their help the receptors can be adjusted in relation to the parts of the environment that are most important in achieving behavioral results. Perception joins new parts of the environment to the organism-environment system; thus knowledge is formed by perception through a reorganization (a widening and differentiation) of the organism-environment system rather than through the transmission of information from the environment. With the help of efferent effects on receptors, each organism creates its own particular world. These considerations have implications for experimental work in the neurophysiology and psychology of perception as well as for the philosophy of knowledge formation.
1. During the present century several scientists have stressed the mutual dependence of the organism and environment. Koffka (1935), for example, described an organism as a system consisting of both the body of the organism and its behavioral environment. There have been several attempts, especially during the last decade, to treat organisms as complex dynamic systems with very intimate connections with the environment (Thelen, 1995; Tani and Nolfi, 1997; Freeman, 1995) or even including parts of the environment (Gibson, 1979; Maturana and Varela, 1987; Jarvilehto, 1998a).
2. One of the basic problems in understanding the characteristics of such systems has been the question of knowledge formation. From ancient times the senses have been thought to have the role of channels through which knowledge arrives into the organism from the environment. The concept of the senses as "windows to knowledge" seemed so strong and irrefutable that attempts to treat organism and environment as one system usually broke down right there and the system had to be divided into two subsystems. In dealing with perception, Koffka (1935) divided the animal-environment system into two: (1) the environmental stimuli being represented in (2) the animal in the form of isomorphic fields. Gibson (1979) used the metaphor of "resonance," implying that the animal and environment were resonating as two separate subsystems.
3. The arguments of sensory physiologists seem indisputable: the eye responds to light and transmits a picture of the environment. Let the philosophers speculate otherwise -- in any case the light stimulus is outside and perception inside! Although in the history of philosophy and psychology there has always been some dispute about whether human knowledge is based directly on the functioning of the senses or is in some sense constructed by thinking (empiricism versus rationalism), there has been no question about the role of the senses as transmitters of at least some kinds of raw data.
4. In the theory of the organism-environment system (Jarvilehto, 1994,1998a and b), organism and environment are functionally inseparable and form only one unitary system which is organized for useful behavioral results. Thus, knowledge formation cannot be based on any transfer process from the environment into the organism, because there are not two systems between which this transfer could occur. Mental activity is the activity of the whole organism-environment system, and the traditional psychological concepts (such as perception) only describe different aspects of the organisation of this total system. New knowledge is created by perception when new parts of the environment join the organism-environment system while changing its structure. An increase in knowledge means a widening and differentiation of the system, which makes new kinds of behavioral acts and new results of behavior possible. Hence knowledge as such is not based on any direct action of the senses.
5. Such a conclusion may seem contrary to the facts. Some earlier ideas go in the same direction, however, particularly those in which the role of movement has been stressed in perceptual activity. Already in 1855 Alexander Bain proposed that sensory and motor action together constitute conscious perception. He stressed the role of eye movements as to determining a large extent what we see. If the eyes move in a circle, we see a circle; the perception of a straight line is based on linear movement of the eyes. The content of perception is related directly to the character of the motor activity.
6. The founder of experimental psychology, Wilhelm Wundt, likewise recognized the importance of motor activity, in visual illusions, for example. The horizontal-vertical illusion was his typical example: here we have an illusory lengthening of the vertical line, because the eyes must move upwards along the line and oppose gravity and thus the energy needed for the eye movement is greater than with the horizontal movement of the eyes. Wundt (1897) writes: "The phenomena of seeing teach us that the idea of distance between two points depends on the motor energy of the eye used when the eye moves this distance.... The motor energy becomes a component of the idea by combining with the sensation which we may perceive." (Wundt, 1897, p. 133)
7. Wundt thus regarded sensation and motor energy as separate components of an idea; in addition to the sensory stimulation, movements are essential for perception. Thus, perception is not simply the copying of the environmental stimuli.
8. Several researchers have recently developed "motor" theories of perception associated with these early ideas (for a review, see Coren, 1986), with perception is always a result of co-operation between the sensory organs and muscles. However, these theories usually preserve the traditional view of the senses as transmitters of environmental information. Movements are only thought to modify the process of formation of knowledge; they are not considered authentic parts of this process.
9. The traditional concept of the senses as transmitters of knowledge is based explicitly on the idea of two systems (organism and environment) between which the transfer of knowledge occurs. This relationship has been formulated in recent decades with the help of information theory, developed originally for the description of automata (Shannon, 1948). Knowledge formation is based on information transmission carried out through signals (stimuli), in which the information is stored with the help of a code. Applied to the senses, this means stimuli are transformed into nervous activity in the receptors according to a well-defined rule, the neural code, which may later be used by the central nervous system in decoding, or reading the information from the neural signal (e.g. Somjen, 1972).
10. There have been several candidates for neural codes: firing frequency in the neuron, intervals between the discharges, patterns of intervals, number of fibers or cells activated, neural location, etc. Regardless of what the code is, the information processing approach presupposes that there must be a decoder in the organism system -- a group of cells, some brain area, or a homunculus -- which can read the information from the signals. Such a decoding process is possible only if this decoder knows the code used in the modification of the signal in the periphery, and if the code stays constant or does not change without advance warning. This decoding is possible only if the relations between the cells in the periphery and the central nervous system stay constant under different action situations. However, the experimental findings during the last decade have challenged precisely this basic assumption.
11. Many recent neurophysiological studies have shown that neural responses do not simply follow stimuli; they often have a dynamic character, with no simple dependence on stimulus parameters. For example, if the same stimulus is repeated or presented under different conditions, the responses may vary considerably. This is true both of specific cells in the central nervous system and of receptor cells in the periphery.
12. Until recently it has been undisputed that the peripheral nervous system acts as a kind of passive transducer coding environmental stimuli for use in the central nervous system. Receptor cells not only have connections to the central nervous system through afferent fibers, but efferent fibers from the central nervous system may also influence the activity of the sensory neurons. Such connections have been found for audition, vision, the sense of balance and skin senses (Alexandrov and Jarvilehto, 1993; Liberman et al., 1990; Biondi and Grandori, 1976; Highstein, 1991; Mikkelsen, 1992).
13. Recent experimental results show that efferent connections may influence sensory organs depending on the behavioral situation and the goals of the experimental subject (animal/man). We have studied the responses of cutaneous peripheral neural units while the subject performed a variety of tasks (Astrand et al. 1986).
14. In the one experimental condition, subjects attended to tactile pulses of varying intensity applied to the receptive field of a mechanoreceptive unit and rated the intensity of their touch sensations numerically. In another condition, the identical pulses were applied to the receptive field of the same unit, but the subject's task was to count deviant tones in a rapidly presented series of standard tones. Thus, this task had nothing to do with the tactile stimuli presented. In both conditions peripheral responses of the single mechanoreceptive units were recorded by microelectodes from the radial nerve at the wrist level (for the recording technique, see Jarvilehto, 1976 ).
15. The thresholds and response characteristics of the recorded mechanoreceptive units were found to change with the task the subject was given. When the subject attended to the touch stimuli the thresholds of the units were lower, more impulses were elicited with identical stimuli, and the latencies of the responses were shorter than during the counting task. From the point of view of the "coding," this would mean that the nervous system could not identify identical stimuli from one condition to another. Hence, the central nervous system would not receive unequivocal information from identical events in the environment during the two tasks.
16. Such results could also be interpreted as showing only that the dynamic changes in the receptors are not related to the tactile stimuli as such, but rather indicate a general sensitization of the receptors while attending to certain kinds of stimuli. It could be further assumed that this state is somehow indicated to the central decoder, which can then correct the incoming signals accordingly. Even with such an interpretation, however, we should admit that it is doubtful that there is unequivocal neural coding in the peripheral nervous system; it is not an automatic or mechanical transducer of the physical parameters of environmental stimuli.
17. In our research with freely moving rabbits (Alexandrov et al., 1986) we found that the attention of the subject did not play a decisive role in this process. The dynamic changes at the receptor level are not simply due to attention or to the use of a certain receptive field sensitized in a certain task. Such changes are related instead to the whole behavioral situation.
18. By pressing a pedal, a freely moving rabbit in a cage acquired food We recorded unit activity directly from the optic nerve at a point before it enters the lateral geniculate body. When the rabbit was performing the food-acquisition task activity in the units in the optic nerve covaried with certain phases of the rabbit's behavior. The units were always activated, for example, when the animal was approaching the pedal or moving to the automatic feeder. This activity could be interpreted as responses of the optic nerve units to visual stimulation by the pedal or the feeder.
19. Before starting the recordings, we had taught the rabbit to perform the task with its eyes covered with non-transparent cups, preventing the use of any visual information. When we closed the rabbit's eyes so that no visual stimulus could influence the retina, the optic nerve unit continued to show activity as the rabbit approached the pedal. This activation could not be related to any direct visual effects of the environment; for many units it seemed to be independent of visual stimulation. Consequently, such activations could not be due to the effects of stimuli; they had to be mediated over the efferent influences upon the retina. On the basis of their latencies to direct visual stimulation, we could also show that the unit discharges were not from efferent fibers; they reflected activations of the ganglion cells.
20. Such results challenge the attention hypothesis, because when the eyes of the rabbit are closed, there is nothing to be attended to in the visual modality. Thus, there should be no reason either to modulate the peripheral activity or to sensitize the receptors. The results should instead be interpreted as showing that unequivocal coding of environmental information is difficult, if not impossible at all levels of the nervous system.
21. The finding that there is no simple coding of stimulus information by the receptors has far-reaching consequences. First, we must conclude that the application of information theory to sensory function is problematic. Second, this finding means that knowledge about environmental features and events is not based simply on the assumed transduction in the sensory systems.
22. If the receptors do not code environmental information and transmit it to the central nervous system, then how is knowledge formed and why do the organisms have receptors? The idea of a transfer of knowledge from the environment into the organism is a cogent one, because it is based on our everyday experience and on the commonsense explanation of causal factors in behavior. If the hypothesis does not hold, are there any other possibilities? Why are there efferent influences at all? If, during evolution, receptors developed in organs responsible for the exact coding of environmental stimuli, it is difficult to see why their action should be distorted by the central nervous system in the form of efferent influences. We could of course suppose, as indicated by the attention hypothesis, that the influences on receptors are controlled in such a way that a model of influences is stored in the central nervous system when they are exerted in the periphery; this model would then be used in the correction of the incoming information.
23. Even so we have the question of how the central nervous system would "know" how much the receptors should be influenced. And if the knowledge comes through receptors, how could anything about the behavioral situation be known before the information from the receptors was received? Moreover, if this situation was already known then it would no longer be necessary to modify the action of the receptors.
24. Could we even imagine knowledge formation without the help of receptors? Let us perform a thought experiment: Imagine an organism with no receptors, only motor organs. Such an organism is, of course, impossible, because a receptor is simply a cell which is connected both to the organism and the environment. As no organism can develop without an environment, it necessarily has such cells and could not live without such cells. But let us imagine such an organism for the purposes of our thought experiment.
25. Could such an organism have knowledge about its environment, from the structures outside its surface boundary, or would it be restricted to its inner life only? We must understand the concept of knowledge broadly here, as the possibility of acting appropriately in the environment. Could such an organism learn something about the environment to which it would have no direct access through senses?
26. Let us put our organism into an environment which consists of a cube with smooth walls filled with a homogeneous energy field (like water). The organism is able to swim in the field by using two pairs of fins which move it in two dimensions: forwards/backwards or right/left. A sensitive and dynamic set of interneurons joins the pairs of fins so that only one pair can be used at once. The muscles of the fins and the interneurons feed from some mysterious inner energy which the organism can obtain from the energy field in the form of induction when its body is moving relative to it. If the movement of the organism stops, the amount of inner energy for one pair of fins goes down and is finally exhausted, but the other pair still has its own energy store which it can use when the first pair is no longer working, thereby restoring the movement of the organism in some other direction. These fins then work as long as the movement continues while the energy of the other fins is restored. If the movement of the organism stops completely, it cannot restore the energy and dies.
27. The organism moves in one direction inside the cube by moving one pair of fins. This movement inhibits, via interneurons, the movements of the other pair. During the movement, the organism can induce more inner energy from the homogeneous energy field and would thus move indefinitely if the walls did not exist. When it hits the wall, preventing its movement forward, the original pair of fins still moves, until its energy store is depleted. Then it stops and the inhibition on the other pair disappears and they start to move, propelling the organism in some other direction. This movement continues until the organism hits another wall, stops, and the other fins again begin to move.
28. Let us now further suppose that the connections of the interneurons between the pairs of fins are such that they can be dynamically changed. The continuous movement of the organism in different directions within the cube accordingly begins to change these connections so that the use of energy by the fins and the induction of energy from the field becomes optimal. The organism already begins to turn before it hits the wall, developing continuous movement even within the walled space.
29. Thus, it seems that the organism comes to know the structure of its environment in the sense that it can anticipate the walls and the instant of hitting them. The walls and the organism begin to form one system, the result of which is the continuous movement. The walls of the cube are elements of this system in the sense that their existence partly explains the action of the organism (turning). Essential in the functioning of such system is the number of interneurons, their dynamics, and the constancy of the environment. In a randomly changing environment, constant connections between the interneuron could not be formed.
30. It would probably not be too difficult to build a computer simulation of the actions of this kind of organism (cf. Tanji and Nolfi, 1997). In any case, the thought experiment so far seems to show that an organism can be connected to its environment in a reasonable, functional way in the absence of any receptors: even without senses it can come to know its environment. What do we need receptors for, then?
31. The thought experiment is unrealistic as there are no organisms without some kind of receptor. Even the idea of inducing energy from the field assumes some sort of general receptor. All organisms have cells that can use environmental energy (such as photoreceptors) or whose function can be distorted by energy gradients (such as mechanoreceptors).
32. The significance of receptors may be seen when the conditions of our thought experiment are changed by adding one hole (a receptor) to the surface of the organism through which it can use directly certain kinds of energy foci (concentrated spots) in the field. The environment of the organism is thus no longer homogeneous, but consists of energy gradients; the walls no longer exist. The receptor hole has a certain size, making possible the direct use of only certain energy spots. Let us further suppose that the main energy for the movement must come from such spots; the induction from the energy field is no longer a sufficient energy source. Hence the organism must every now and then hit such energy spots with the receptor to have enough energy for its life process. Let us further assume that the energy spots remain in certain locations and are immediately restored as soon as they are used; so far the environment is constant. We can also assume that there are now many pairs of fins, making movement possible in any direction. These fins also have reciprocal innervation, however, so movement in one direction inhibits the fins working in the opposite direction.
33. Now the organism moves in this heterogeneous environment. If it does not hit any energy spots, it dies. Eventually, one of the organisms (we now assume there are many of them) encounters a spot which gives it energy to move further in that direction. Slowly, the energy for this direction is depleted and other fins start working, turning the organism in another direction. Again one spot is found and then direction is changed. If there are enough dynamic interneurons connecting the fins, the organism starts to move from one energy spot to another, optimising its energy consumption in the same way as the organism within four walls. Such an organism could then in principal live forever, but its life process would be very sensitive to any change in the structure of the environment.
34. We now proceed to the last part of our thought experiment and assume a heterogeneous environment which is continuously changing. The location and size of the energy spot is continuously changing. We also add to the receptors efferent fibers that can regulate the size and the quality of the receptor hole. The organism can now use different kinds of energy spots of varying size. What follows?
35. First of all, most organisms with fixed receptors disappear and the new organisms with efferent control of receptors begin to show behavior which differs in principle from the behavior of the earlier organisms. When the organism does not get an energy supply with one size or quality of receptor, it changes the receptor hole so that it can also fit the energy spots of other sizes and qualities. Thus, the organism starts to search, to investigate its environment. There is no longer random movement which brings the organism by chance to a fixed energy spot; the organism can locate spots of different sizes and qualities and can also search for other spots if the original ones disappear. Through this fitting process, it begins to become a functional whole with its environment, which it can join in many qualitatively different places. The organism begins to "perceive" its environment.
36. One hopes that this thought experiment gives a better idea of why receptors exist even if they are not transmitters of information, and why efferent influences are important for all receptors. The receptors provide the possibility of direct contact with the parts of the environment necessary for successful behavior and the efferent influences help in the search for new, useful aspects of the environment. The properties of the receptors are continuously modified, and receptor patterns are created which fit useful environmental energy configurations, making new behavioral success possible (cf. Freeman 1997). Perception is the process in which certain parts of the environment, defined by dynamically changing receptors, are joined into the structure of the organism-environment system; perception involves the whole organism-environment system.
37. The earlier researchers presenting motor theories of perception were right insofar as they saw the significance of both movement and sensory processes as the basis of perception. From the point of view of the theory of the organism-environment system presented here, however, those theories were incomplete, in the sense that they were still based on the idea of information transmission from the environment; the movement was seen only as a component modifying the sensations arriving through the senses. If perception is a process involving the whole organism-environment system, however, then there is no causal relation between movement and perception. The movements of the organism are an expression of the reorganization of the system; they are mere parts of the perceptual process, like the events in the receptors or in the environment.
38. Perception is not a linear process proceeding from the stimulus to the percept but a circle involving both the sensory and motor organs and the events in the environment. A perceptual process does not start with the stimulus; rather, the stimulus is an END of the process, like the last piece of a jig-saw puzzle, which fits in its place only because all the other pieces have been placed in a particular way. It is just this joining of the other pieces, their co-ordinated organization, which leaves a certain kind of hole into which this last piece can be fitted. The organization of the other pieces defines the possible last piece with which to finish the puzzle. Similarly, a stimulus is present only if there is an organisation into which it can be fitted. This relation to the percept is no more causal than that of the last piece of the puzzle in relation to the constructed picture. The stimulus is a part of the process of reorganizing the structure of the organism-environment system that is the basis of new knowledge.
39. It is still necessary, however, to consider briefly what kind of knowledge was created in our thought experiment. Most mistakes associated with the concept of "knowing" are connected to the idea that "knowledge" is only that which may be reported, told to another person or to oneself. Such a way of thinking neglects all knowledge which is not shared with other people. However, every living organism must necessarily know something insofar as it can act in its world. It is precisely the structure of the organism-environment system which makes the behavior and behavioral results possible, and it is just this structure which is knowledge in a broad sense.
40. Hence we should not think that the organism in our experiment knows something about its environment in the usual sense: that it has knowledge of its own existence or that it knows that it is confined to a space of certain form. This sort of knowledge presupposes consciousness, which is based on the co-operation of many organism-environment systems (Jarvilehto and Veresov,1998c). Such a system is created by communication; thus language, for example, is not a means of information transmission, but the way to produce common organisation and common results. The knowledge which may be communicated is only part of all the knowledge existing in the social system. The organism of the thought experiment thus "knows" the cube or parts of its environment only in the sense that it may join specific parts of environment to its structure, in order to obtain useful behavioral results, but it is not conscious of its world.
41. It is precisely the development of the sensitivity of the receptor to different types of energy and its efferent control which makes possible the widening and differentiation of the behavioral environment. If the sensitivity of the receptor increases, there is a corresponding expansion in the behavioral environment, and if it decreases, this leads to the disappearance of the parts of the environment which earlier belonged to the system. Mead (1934) had already pointed this out beautifully in the 1930's, probably without knowing anything about the possibility of efferent influences:
We have seen that the individual organism in some sense determines its own environment by its sensitivity. The only environment to which the organism can react is one that its sensitivity reveals. The sort of environment that can exist for the organism, then, is one that the organism in some sense determines. If in the development of the form there is an increase in the diversity of sensitivity there will be an increase in the responses of the organism to its environment, that is the organism will have a correspondingly larger environment.... In this sense it selects and picks out what constitutes its environment. It selects that to which it responds and makes use of it for its own purposes, purposes involved in its life-processes. It utilises the earth on which it treads and through which it burrows, and the trees that it climbs; but only when it is sensitive to them. (Mead, 1934, 245)
I thank my wife, Mrs. Anna Jarvilehto, M.A., for many fruitful discussions and co-operation in the preparation of the target article, and Ms. Suzy McAnsh for helpful reading of the manuscript.
Alexandrov YuI, Grichenko YuV, Shvyrkov B, Jarvilehto T, Soininen K (1986) System-specific activity of optic tract fibers in open and closed eye behavior. The Soviet Journal of Psychology 7: 299-308.
Alexandrov YuI, Jarvilehto T (1993) Activity versus reactivity in psychology and neuropsychology. Ecological Psychology 5: 85-103.
Astrand K, Hamalainen H, Alexandrov YuI, Jarvilehto T (1986) Response characteristics of peripheral mechanoreceptive units in man: relation to the sensation magnitude and to the subject's task. Electroencephalography and Clinical Neurophysiology 64: 438-446.
Bain A (1855) The Senses and The Intellect. London: Longmans, Green.
Biondi E, Grandori F (1976) Do efferent fibers to hair cells intervene in acoustic stimulus peripheral coding? International Journal of Bio-Medical Computing 7: 205-211.
Coren S (1986) An efferent component in the visual perception of direction and extent. Psychological Review 93: 391-410.
Freeman WJ (1995) Societies of Brains. A Study in the Neuroscience of Love and Hate. Hillsdale, NJ: Erlbaum.
Freeman WJ (1997) A neurobiological interpretation of semiotics: meaning, representation, and causality. Proceedings: Conference on Semiotics and Machine Intelligence, National Institute of Standards & Technology Gaithersburg MD.
Gibson, J. J. (1979) The Ecological Approach to Visual Perception. Boston: Houghton Mifflin.
Highstein SM (1991) The central nervous system efferent control of the organs of balance and equilibrium. Neuroscience Research: 12, 13-30.
Jarvilehto T (1977) Neural basis of cutaneous sensations analysed by microelectrode recordings from human peripheral nerves - a review. Scandinavian Journal of Psychology 18: 348-359.
Jarvilehto T (1994) Man and His Environment. Essentials of Systemic Psychology. Oulu: Pohjoinen, 224 p. (In Finnish).
Jarvilehto T (1994) Learning as formation of man-environment system. In: Proceedings of the International Workshop on CLCE, ed. by Levonen, J.J. and Tukiainen, M.T., p. 7-8. Joensuu: Joensuu University Press. http://wwwedu.oulu.fi/homepage/tjarvile/learn.htm
Jarvilehto T (1998a) The theory of the organism-environment system: I. Description of the theory. Integrative Physiological and Behavioral Science, 33, in press. http://wwwedu.oulu.fi/homepage/tjarvile/chap1.htm
Jarvilehto T (1998b) The theory of the organism-environment system:
Jarvilehto T, Veresov N (1998c) Consciousness, cooperation and communication. ISCRAT, Aarhus, Denmark. http://wwwedu.oulu.fi/homepage/tjarvile/iscrat.htm
Koffka K (1935) Principles of Gestalt Psychology. London: Bradford.
Liberman MC, Dodds LW, Pierce S (1990) Afferent and efferent innervation of the cat cochlea: quantitative analysis with light and electron microscopy. Journal of Comparative Neurology 301: 443-460.
Maturana HR, Varela FJ (1987) The tree of knowledge: the biological roots of human understanding. Boston: Shambhala.
Mead GH (1934) Mind, Self, and Society. Chicago: Chicago Univ. Press.
Mikkelsen JD (1992) Visualization of efferent retinal projections by immunohistochemical identification of cholera toxin subunit B. Brain Research Bulletin 28: 619-623.
Shannon CE (1948) A mathematical theory of communication. Bell System Technical Journal 27: 379-423 and 623-656.
Spinoza B (1677/1985) Ethics. In the Collected Works of Spinoza (Ed. E. Curley), 408-617. New Jersey: Princeton Univ. Press.
Somjen G (1972) Sensory coding in the mammalian nervous system. New York: Meredith.
Tani J, Nolfi S (1997) Self-organization of modules and their hierarchy in robot learning problems: A dynamical systems approach. Sony Computer Science Laboratory Inc., Technical Report: SCSL-TR-97-008.
Thelen E, Smith LB (1994) A Dynamic Systems Approach to the Development of Cognition and Action. Cambridge MA: MIT Press.
Uexkuell J von., Kriszat G (1932) Streifzuge durch die Umwelten von Tieren und Menschen. Frankfurt am Main: Fischer. Reprinted in J. Schiller (Ed) Instinctive Behavior. New York: International Univ. Press, 1957.
Wundt W (1897) Outlines of Psychology. Leipzig: Engelmann.